Abstract
Soil is living medium and it acts as a precarious reserve in agriculture and food production. To enhance crop yields for ever-increasing human population, chemical fertilizers are being applied in the soil. But, the haphazard usage of fertilizers, predominantly nitrogenous and phosphorus, headed to considerable contamination of soil, air and water. Moreover, unwarranted consumption of these agrochemicals also cause lethal effects on soil microorganisms and disturbs the soil fertility. Due to current public apprehensions about the side effects of these agrochemicals, understanding plant and rhizospheric microbial interactions is gaining momentum. It is considered to be important to effectively manage level of nitrogen in soil through biological nitrogen fixation (BNF) to maintain agricultural sustainability. The fixed N is directly taken up in the plants and is less vulnerable to volatilization, denitrification and leaching. Thus, mutualistic symbiosis amongst legume plant and nodulating rhizobia plays a key role in ecological environments. Legume-rhizobia symbioses provide approximately 45% of N used in agriculture and contributions of BNF from the symbiotic association accounts for at least 70 million metric tons per year into terrestrial ecosystems. In agricultural systems, about 80% of BNF contributed by symbiotic association made between leguminous plants and species of Rhizobium, Bradyrhizobium, Sinorhizobium, Azorhizobium, Mesorhizobium and Allorhizobium. The populations of these root-nodule forming bacteria can be changed ecologically, agronomically, edaphically and genetically to increase legume production and soil productivity. Moreover, legume-rhizobia symbioses also provide non-polluting and economical ways to augment N2-fixing potential under stress conditions. Scientists have identified numerous symbiotic systems tolerant in harsh situations of salinity, alkalinity, acidity, drought, toxic metals have been recognized and alteration in rhizobial population under stressed environments can be an indicator of soil fertility. Moreover, interactions among rhizobia, plant growth-promoting rhizobacteria (PGPR) and mycorrhiza as well show significant part in increasing soil fertility and crop yields. In this chapter, significance of biological nitrogen fixation in persistent food supply, influence of extreme environments on legume-rhizobia symbiosis as well as interaction of rhizobia with belowground microbial species are discussed. The eco-friendly approach to increase crop production and soil health by inoculation of symbiotic bacteria as biofertilizers is described for sustainable agriculture.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
7.1 Introduction
Legumes can be considered as key source of proteins in vegetarian diet in developing countries (Nedumaran et al. 2015). Therefore there is a need to improve the yield of legumes and to sustain soil fertility. Legumes utilized for human feed comprise of dry and green beans, broad beans, dry and green peas, chickpeas, lentils, soybeans, lupins, mung beans and peanuts. Nitrogen (N) and phosphorus (P) are major regulating nutrients for growth of leguminous plants. Replenishment of these nutrients to the legume crops is mostly done through application of inorganic nitrogenous and phosphate fertilizers to soil. Addition of nitrogenous fertilizers is the major external input for maximizing crop yield in agriculture. Inadequate usage of these chemical fertilizers has contaminated environment and causes various health hazards. Moreover, due to the low use efficiency of nitrogen fertilizers among plant nutrients and their continuous use leads to slow deterioration in soil health (Newbould 1989; Bockman 1997) and a decline in crop yield (Bohlool et al. 1992). Additional drawbacks of N-fertilizers include speeding up the depletion of non-renewable energy resources. Along with high usage of N fertilizers in developed countries, volatilization of N oxides (greenhouse gases) into environment and leaching of NO3 − into ground water, is also a major threat for global N cycle.
Due to exponential growth of population, its demand of the day to implement new means of improving food production that are well-suited with sustainability and preservation of environmental quality (Sindhu and Dadarwal 1995b; Sharma et al. 2018a, b). Moreover, rates of nitrogenous and phosphatic fertilizers is continuously increasing in developing countries and these fertilizers are not only unaffordable or unavailable in many countries but also have other drawbacks. Therefore, it is actually critical task for farmers to add-on N and P fertilizers in soil to escape the nutrient insufficiencies. Viable agriculture consist of effective management of agricultural assets to fulfill shifting human requirements, while preserving or increasing environmental superiority and safeguarding natural assets. Thus sustainability deliberations requires substitutes to nitrogen fertilizer. Biological nitrogen fixation can be considered as substitute in farming practices as it uses capability of several nitrogen-fixing bacteria to transform atmospheric nitrogen into the plant usable, ammonia using the nitrogenase enzyme (Bohlool et al.1992).
Legumes are grown approximately on 252 million hectares of land, leading to about 90 Tg of dinitrogen being fixed per year, with major contributors to overall N2 fixation through legume–Rhizobium symbiosis (Smith and Giller 1992). The growth of grain legumes such as field pea (Pisum sativum L.), followed by the subsequent decomposition of N rich residues helps to replenish N removed by harvesting. This leads to savings of fertilizer N and brings about enrichment of soil N, which is available to subsequent crops (Jensen and Hauggaard-Nielsen 2003). By using nitrogen-fixing species of microorganisms in cropping systems dependency of agricultural crops on chemical nitrogenous fertilizers can be reduced. Moreover, biologically fixed nitrogen resides within soil organic matter in bounded form and hence it is considerably less vulnerable to chemical alterations as well as physical losses like volatilization and leaching. Considering adverse environmental effects of chemical fertilizers and growing prices, use of plant growth promoting rhizobacteria (PGPR) and rhizobia is valuable for sustainable agricultural system (Fernández et al. 2007; Shiri-Janagard et al. 2012; Uribe et al. 2012; Sindhu et al. 2018). A lot of information exists on the positive influence of Rhizobium and Bradyrhizobium on legumes in terms of biological nitrogen fixation (Werner 2005) and in cereal–legumes crop rotation systems. Moreover, coinoculation of symbiotic bacteria with PGPR is another approach which has been found to improve root and shoot weight, plant vigour, nitrogen fixation and grain production in legumes (Valverde et al. 2006; Yadegari et al. 2008; Verma et al. 2013; Sindhu et al. 2017).
This chapter describes diversity detected among different symbiotic bacteria and contribution of different rhizobia in increasing the growth and yield of legume crops as well as various biotechnological approaches undertaken for improving biological nitrogen fixation. The various limitations faced to improve crop productivity by inoculation with bacterial strains and opportunities of getting anticipated profits by confirming the establishment and survival of inoculated microbes in soil has also been discovered.
7.2 Role of Nitrogen Fixation by Bacteria in Cereal and Legume Crops
Majority of naturally augmented nitrogen in soils is from symbiotic or asymbiotic biological fixation carried out by microorganisms. As per an estimate annually roughly 100 Tg N, is needed for production of world’s grain and oilseed crops (David and Ian 2000). Legume crops possess remarkable potential for biological nitrogen fixation in soil ecosystems (Brockwell et al. 1995). There exist roughly 700 genera and around 13,000 species of legumes and from such a large variety of legumes only a small part was studied for nodulation and nitrogen fixation efficiency (Sprent and Sprent 1990). Assessments showed that symbiotic association of Rhizobium with approximately 100 agriculturally significant legumes, add roughly half the annual amount of BNF inflowing soil ecosystems (Tate 1995). Legume symbioses add approximately 70 million metric tonnes of N per yea, from which half is derived from cool and warm temperature zones and rest is resulting from tropics (Brockwell et al. 1995; Freiberg et al. 1997).
The success and sustainability of many food crops, forage and green manure legumes is mainly obligated to their symbiotic association with particular nitrogen-fixing rhizobia (Menna et al. 2006). A peculiar characteristic that distinguishes rhizobia from other nitrogen-fixing bacteria is their unique ability to elicit the development of a specialized nodule to form a symbiotic association with their legume host (Lindstrom et al. 2006) (Fig. 7.1). This association converts atmospheric inert N2 to a renewable source of fixed N for agriculture with expected values falling in range of 57–600 kg of N ha−1 year−1 (Zahran 1999; Ramankutty et al. 2018). In contrast to application of inorganic N-fertilizers. N input through the process of BNF not only maintains the soil’s N reserves but can also conserve natural resources. In that way, BNF plays significant role in nourishing throughput of soils.
Nodulation and nitrogen fixation is illustrated in chickpea plant. The coordinated and controlled expression of nodulation genes of rhizobia in response to plant-released flavonoids synthesize the nodulation factor that leads to nodule organogenesis. The differentiated bacteroids in the nodules utilize nitrogenase enzyme to convert atmospheric nitrogen into ammonia.
Some bacteria and cyanobacteria have developed capacity to convert atmospheric nitrogen in to ammonia using nitrogenase enzyme and supply this important nutrient into agricultural soils. BNF take place in the free-living state, in association with or in symbiosis with plants (Table 7.1). Inoculation of various strains of diazotrophic bacteria carried out to increase amount of nitrogen as nutrients to several leguminous and non-leguminous crops. Vast areas of aerable land in Australia, India, Russia and United Kingdom inoculated with non-symbiotic N2-fixing bacteria such as Azotobacter, Azospirillum, Bacillus and Klebsiella spp. with the goal of improving plant yield (Lynch 1983; Sloger et al. 1992; Di Benedetto et al. 2017). In symbiotic system, Rhizobium species have been effectively utilized globally as a bioinoculant leading to effective establishment of N2-fixing symbiosis with leguminous crops (Eaglesham 1989; Thies et al. 1991; Dahale et al. 2016). Other N2-fixing symbionts, such as Frankia spp. have also been successfully introduced into soil (Sougoufara et al. 1989; Clawson et al. 1998).
Another approach to improve nitrogen budget of crops is to inoculate symbiotic bacteria with PGPR in leguminous crops to improve root and shoot weight, plant vigour, nitrogen fixation and grain yield in several legumes (Valverde et al. 2006; Yadegari et al. 2008; Verma et al. 2013; Sindhu et al. 2017). By modulating balance of deleterious vis a vis beneficial microbial activities in rhizosphere, PGPR are known to encourage plant growth directly by producing phytohormones, by improving nutrient accessibility and acquisition or eliciting plant defense mechanisms, which in turn, leads to increased nutrient acquisition and growth (Sindhu et al. 2014, 2016) or induce systemic resistance against harmful microorganisms (Liu et al. 1995a, b). Therefore, synergistic consortia of microbes having various metabolic abilities (N2 fixation, P mobilization, synthesis of plant growth hormones and bioactive molecules) can definitely perform better than single inoculations. However, type of inoculums, method of inoculation and agricultural practices can influence the effect of the inoculation. The effect of multiple inoculants with symbiotic N2 fixing rhizobia, asymbiotic free-living N2 fixing bacteria and phosphate solubilising bacteria or cyanobacteria found to stimulate plant biomass in different legumes.
Symbiotic association between leguminous plants and Rhizobium is the best comprehensively studied nitrogen-fixing system. This symbiotic association fixes around 70–80% of the total BNF per year (Ishizuka 1992). Nitrogen fixation capacity of symbiotic rhizobia range from 57 to 600 kg N ha−1 yearly (Elkan 1992). Among legumes, soybean is leading crop legume, comprising of 50% of the global crop legume area and soybean was reported to fix 16.4 million tones N annually, representing 77% of the nitrogen fixed by the crop legumes (Herridge et al. 2008). Increase in legume production are usually equal to those estimated from inoculation of 30–80 kg of fertilizer-N ha−1. Inputs of fixed N for alfalfa, red clover, pea, soybean, cowpea and vetch are expected to be nearly 23–335 kg of N ha−1 year−1 (Tate 1995; Wani et al. 1995). Thus, efficiency of various legume species and their microsymbionts has been found variable (Table 7.1). In general, faba bean (Vicia faba) and pigeon pea (Cajanus cajan) have been found to be very efficient; soybean (Glycine max), ground nut (Arachis hypogaea) and cowpea (Vigna unguiculata) to be average; and common bean (Phaseolus vulgaris) and pea (Pisum sativum) less efficient for nitrogen fixation (Hardarson 1993; Pinto et al.2007). The Azolla-Anabaena symbiotic system proved to add 45–450 kg N ha−1 and Frankia-actinorhizal symbiosis deliver 2–362 kg N ha−1 (Elkan 1992).
Sindhu and Dadarwal (1992) carried out experiment to evaluate comparative efficiency of nitrogen fixed by Rhizobium strains in chickpea using non-nodulating genotype PM233 obtained from wild type nodulating genotype ICC640. Due to nitrogen fixation by Rhizobium strains Ca534 and Ca219 in nodulating genotype ICC640, significant increase in plant dry weight was obtained over application of 80 kg N ha−1 through urea in non-nodulating mutant PM233. The results reveal the fact that effective symbiosis between rhizobia and chickpea can supplement more than 80 kg N ha−1. Profits of nitrogen fixation in legume crops to succeeding cereal crops are considerable and carry on for several years as a result of gradually slow mineralization. In green manuring crops greater amount of benefits of rhizobia and plant symbiosis were observed and about 532 kg N could be assimilated by 60 days with nitrogen N accumulation rate of 10.8 kg N ha−1 day−1 (Peoples and Herridge 1990).
Fixed nitrogen is also made accessible to an intercrop or succeeding crop. Generally more than 50% of the crops grown in Africa, India and Latin America are either intercropped or rotated with nitrogen-fixing crops (Fujiata et al.1992). Hence biological nitrogen fixation assists as an efficient way to reduce reliance on chemical fertilizers by supplying nitrogen to symbiont as well as builds up soil nitrogen for subsequent crops. However, numerous soil environmental causes viz. temperature, moisture, acidity, available nitrogen, phosphorus, calcium and molybdenum content affect nitrogen fixation (Somasegaran and Bohlool 1990; Zhang et al.1996). Application of efficient strain of rhizobia on legumes generally resulted in substantial rise in production of several legume crops (Eaglesham 1989; Thies et al.1991) (Table 7.2). Although, numerous reports also showed unpredictability in attaining the yield increases ensuing application of rhizobial strains (Miller and May 1991).
7.3 Rhizobial Diversity
Phylogenetically rhizobia are very different, demonstrating numerous lineages. Rhizobia presently comprise of 12 genera and beyond 113 species of α- and β-proteobacteria (Sawada et al. 2003). Rhizobia are distributed in the following genera: Aminobacter (1), Azorhizobium (3), Bradyrhizobium (15), Devosia (1), Mesorhizobium (29), Methylobacterium (1), Microvirga (3), Ochrobactrum (2), Phylobacterium (1), Rhizobium (43), Sinorhizobium/Ensifer (13) and Shinella (1). Additionally, there are 9 species of β-rhizobia, namely Burkholderia (6), Cupriavidus (2) and Herbaspirillum (1). Many new species of rhizobia are described each year and even strains from non-typical rhizobia genera are included to list of rhizobia, as strains from the Burkholderia genus (Chen et al. 2003, 2008). In general, rhizobia are heterotrophic and aerobic non-sporulated rods, however, there are Bradyrhizobium strains having ability of anaerobic growth (Polcyn and Luciński 2003), photosynthetic bradyrhizobia (So et al. 1994) and methylotrophic Methylobacterium strains (Sy et al. 2001). The complete genomic sequence of photosynthetic bradyrhizobia able to induce both root and stem nodules revealed that these strains lack the canonical nodABC genes required for Nod factor synthesis (Giraud et al. 2007).
Crook (2013) isolated Rhizobium sp. IRBG74 and A. caulinodans from Sesbania aculeata and Sesbania rostrata and capable of colonizing rice roots. Endophytic strain of Rhizobium sp. IRBG74 was also isolated from Sesbania cannabina, but it lacks nifV gene required for nitrogen fixation and hence unable to fix nitrogen. Rhizobium sp. IRBG74 initially grouped as Agrobacterium but as it do not possess Ti plasmid it was re-categorized as Rhizobium. This bacterium contain sym-plasmid having nifH together with nodA genes and it colonizes a wide range of Sesbania plants. Similarly, A. caulinodans ORS571 is capable of nitrogen fixing endophytic colonization (Chen and Zhu 2013; Venkateshwaran et al. 2013).
Plant genotype was also found to have effect on existence and dissemination of rhizobial species in soil. For example, Phaseolus vulgaris and Mimosa affinis show difference in rhizobial nodulation specificity. P. vulgaris is can be nodulated by six rhizobial species, viz. R. etli, R. giardinii, R. gallicum, R. tropici, R. leguminosarum bv. phaseoli and Bradyrhizobium spp., whereas Mimosa affinis showed nodulation specificity for R. etli alone (Wang et al. 1999). Genistoid legumes (brooms) in Canary Islands, Morocco and Spain are nodulated by four distinct rhizobial strains viz. B. japonicum, B. canariense and two unidentified species (Vineusa et al. 2005).
Abiotic factors like pH, rainfall, soil type and temperature also influence diversity of rhizobial species, whereas soil types may influence composition of rhizobial community which is ascertained from the fact that legumes grown in different geographical locations nodulated by different rhizobial species/genera. For example, Glycine max (soybean) generally nodulated by B. japonicum; but surprisingly soybean grown in Xinjiang region of China showed colonization of root by Mesorhizobium tianshanense and Sinorhizobium fredii. Sameway, R. leguminosarum bv. viciae and bv. trifolii geberallly nodulates beans in Leon, France, but beans grown in Andalucia region showed presence of R. etli, R. gallicum and S. fredii in addition to R. leguminosarum bv. viciae and bv. trifolii (Velázquez et al. 2001). Conventionally, Mesorhizobium ciceri and Mesorhizobium mediterranean isolated form nodules of Cicer arietinum, but Cicer arietinum grown under water deficient conditions in Tunisia showed colonization by Ensifer meliloti (formerly Sinorhizobium meliloti) (Romdhane et al. 2009). Similarly, E. meliloti also been isolated from C. arietinum plants growing in Almora and Terai region of Uttarakhand Himalayas (Rajwar et al. 2013). Type of soil also restricts distribution and diversity of rhizobia which was clearly confirmed by characterization of different rhizobial species from Caragana plant growing in three eco-regions of China differing in soil types. Mesorhizobium genospecies I, II, IV, VI and VII were identified from Caragana plants growing in sandy soils of Mongolia. M. temperatum, M. tianshanense, M. septentrionale, M. genospecies III, R. yanglingense and Rhizobium sp. IV were isolated form Caragana plants grown in saline/alkaline soils and M. plurifarium, M. genospecies V and VII, and Rhizobium sp. IV in fertile/forest soils of Northwestern Yunnan region (Lu et al. 2009).
Delamuta et al. (2017) evaluated phylogenetic relationship between 45 Bradyrhizobium strains isolated from different legumes i.e., Arachis hypogaea, Acacia auriculiformis, Glycine max, Lespedeza striata, Lupinus albus, Stylosanthes sp. and Vigna unguiculata, based on nodY/K and nifH genes of and compared their 16S rRNA gene phylogeny and genetic diversity by rep-PCR. 16S rRNA tree revealed that strains were dispersed into two clusters – B. japonicum and B. elkanii – with numerous strains being alike within each clade. The rep-PCR examination also discovered high intra-species diversity. Grouping of strains in the nodY/K and nifH trees was undistinguishable. Thirty nine strains obtained from soybean grouped with Bradyrhizobium type species and five others in distinct positions. Only one strain isolated from Stylosanthes sp. displayed similar nodY/K and nifH sequences to soybean strains and it also nodulated soybean. nodC sequences comparison showed same clusters as observed in the nodY/K and nifH phylograms. The analysis of symbiotic genes showed that a large group of strains from the B. elkanii superclade contained new symbiovar sojae, whereas for alternative group, comprising B. pachyrhizi, the symbiovar pachyrhizi could be projected.
7.4 Nodulation of Legume Roots
Mutualistic, nitrogen-fixing relations amongst Fabaceae family plants and soil bacteria Azorhizobium, Bradyrhizobium, Mesorhizobium and Rhizobium (as a group designated rhizobia) contribute considerably to crop yield. This symbiosis between legume plants and rhizobia also offers an interesting model to study the intricacy of various mechanisms that control plant cell partition and nodulation. In the absence of the host, free-living rhizobia are in their saprophytic phase and compete with other soil microflora for limited nutrient resources. The population densities of rhizobia are usually low when legumes are not a large component of the plant community (Woomer et al. 1988; Kucey and Hynes 1989), demonstrating that symbiotic form is crucial for formation of a considerable saprophytic inhabitants of rhizobia in the soil. Natural rhizobial population as well as inoculated rhizobia was found to be different in their tolerance to key environmental clues and thereby influence persistence and existence of distinct species in soil (Vidor and Miller 1980; Defez et al. 2017).
Nodulation (nod) genes of rhizobia required for infection and nodulation are classified as universal, host-specific and regulatory nod genes (Fig. 7.2). Nodulation genes are principally classified into three classes: (a) regulatory nodD and nodVW genes enabling activation of and host specific nod gene transcription, (b) the common nodABC, nodM and nodIJ genes, which are functionally and physically conserved amongst different rhizobia, and (c) host specific nod genes, which are variable with bacterial species and strains. Alteration of host specific nod genes generally do not counterpart with cloned genes from other rhizobia. The structural arrangement and regulation of nodulation genes of Rhizobium, Bradyrhizobium and Azorhizobium has been reviewed recently (Long 1996; Spaink 1996; Hanin et al.1999; Appelbaum 2018). Expression of structural nod genes was governed by flavonoid signals from plants transcription of nodD regulatory gene is regulated by specificity of flavanoids and hence believed to be partial determining factor of strain/host specificity. The common nod genes are involved in manufacturing of basic lipochitin-oligosaccharide molecule and host specific nodulation genes add various substituents at reducing or non-reducing ends of Nod factors (Perret et al. 2000; Sindhu and Dadarwal 2001a, b, c). Alteration of host specific nod genes may end in either a postponement in nodulation or a variation in host range (Denarie et al. 1992). Expression of structural nod genes results in synthesis of specific extracellular lipo-oligosaccharide compounds termed as nodulation factors (NF) which stimulate root-hair deformation, cortical cell division and other responses in prone legume root.
Nodulation genes ( nod, nol, noe)Sinorhizobium meliloti and Bradyrhizobium japonicum are represented. Universal nodulation genes are depicted in yellow colour and regulatory nodulation genes are shown in light blue colour, whereas host-specific nodulation genes are shown in light green colour. Regulatory nodD product interact with specific flavonoids, then binds with nod boxes (n′) and cause activation of transcriptional operon of other nodulation genes
Legume roots release flavonoids in the root exudates and rhizobia which colonize soil in neighborhood of root hair are attracted through chemotaxis in response to the flavonoids. The flavonoids and isoflavonoids secreted by roots of legumes bind with the regulatory protein NodD, which subsequently bind to conserved nod-box in the promoters of bacterial nodulation genes to encourage their expression. The nod genes code for enzymes for synthesis of Nod factors. Strain-specific combinations of nodulation genes (nod, nol or noe) code for addition of several decorations to core structure (Sindhu et al. 1999a, b). Examples of NF substituents are hydrogen (R1–R6), carbamoyl (R1–R3), acetyl (R1–R4), sulfate (R4), fucose (R4) and arabinose (R6) (Fig. 7.3). The perception of NFs by the plant in turn triggers several early symbiotic reactions in the plant root, for example ion fluxes, calcium spiking, root hair deformation, cortical cell division and synthesis of an infection thread that directs the bacteria to the emerging primordium. Several elements of signaling pathway leading to nodulation have been characterized: the putative NF receptors (which belong to the lysine motif receptor-like kinase family, LysM–RLK), a cation channel, a leucine-rich repeat receptor kinase (LRR–RK), a calcium/calmodulin-dependent protein kinase (CCaMK), a cytokinin receptor and various transcriptional factors. Transmembrane Nod factor receptors recognize Nod factor in a strain- and ecotype-specific manner. Alteration of Nod factor such as the length and saturation of the acyl group determine host specificity. Nod factor receptor activation stimulates root hair deformation enabling them to lodge small number of bacteria which further grow in to a colony within nodule. Modulation of host range was also done through surface polysaccharides such as EPS from S. meliloti. Recognition of polysaccharides by R genes present in some ecotypes or varieties of plants restricts host range which culminate in the transcriptional activation of other nod genes (Downie 1994; Russelle et al. 2008).
Nodulation factor synthesized by Rhizobium strains. Host specific nodulation genes (nod, nol or noe) results in several decorations or modifications on the basic core structure
Rhizobia encourage formation of nodules on legumes by either a NF-dependent or a NF-independent process. Gully et al. (2017) reported whole genome sequence of Bradyrhizobium sp. strain ORS285, capable of nodulating Aeschynomene legumes using two different approaches that vary in requisite of Nod factors. In NF strategy, plant signals of the flavonoid family are received by bacterial NodD regulatory proteins that encourage synthesis of lipochitooligosaccharidic NFs that activate nodule organogenesis (Oldroyd and Downie 2008). Some steps of this process are subject to variation: (i) alternative plant compounds (e.g. betaines, jasmonate, xanthones, vanillin, etc.) can start nod gene expression but these compounds usually act at higher concentrations than (iso) flavonoids (Cooper 2007); (ii) beside NodD, additional regulators can modulate expression of nod genes like NolR (in some Rhizobium and Sinorhizobium species) or NolA and the two component system NodV/NodW (in Bradyrhizobium japonicum); and (iii) synthesis of the Nod factor support is regulated by canonical nodABC genes existing in all rhizobia.
The rhizobia adhere to root hairs all over the root but root hairs that are most responsive to Rhizobium infection are just behind the apical meristem at the site of emergence of root hairs. In the infectible root zone, rhizobia adhere to surface of root hair either through an acidic extracellular polysaccharide or via definite calcium-dependent protein, rhicadhesin, cellulose fibrils (Mateos et al. 1995; Smit et al. 1987) and legume root lectin (Kijne et al. 1988). Lipooligosaccharides (Nod factors) produced by the infecting rhizobia cause characteristic curling and deformations of root hair and cortical cell divisions in well-suited host (Lerouge et al. 1990; Broughten et al. 2000). The deformed root hairs in various legumes may form different structures, including corkscrews, branches, twists, spirals and shepherd’s crooks. Cao et al. (2017) described that a stable regulation of innate immunity is probably essential during process of nodulation starting from rhizobial infection, symbiotic establishment and maintenance. Following initial infection processes, plant immune responses can also be stimulated in nodules and expected to result in nodule senescence. Mutualism believed to be derived from a pathogenic relationship that reduced over time to a condition in which both partners can benefit. Generally rhizobia overcome host immune response by actively suppressing it to permit infection and symbiosis establishment. Whereas plants developed mechanisms to limit nutrient supply to symbiont and thereby checking number of nodules on plant so that protecting themselves form overburden.
In Medicago sativa, nodule development is closely linked to Nod factor (NF) synthesis by S. meliloti (Lerouge et al. 1990). S. meliloti starts two analogous, nodule-specific, procedures to develop unspecified nodules nearby root proto-xylem ends: (i) rhizobial colonization pathway, that includes infection thread development in root hairs and cortical cells, and (ii) nodule organogenesis pathway, that includes stimulation of cell divisions in root cortical, endodermal and pericycle cell layers to generate a nodule primordium and then, a nodule meristem (Timmers et al. 1999; Xiao et al. 2014; Djordjevic et al. 2015). Rhizobial NFs hurriedly trigger nuclear calcium oscillations in root hair cells (Levy et al. 2004; Miwa et al. 2006), which transcriptionally activates central symbiotic (SYM) genes e.g. nodule commencement (MtNIN), nodulation signaling pathway 1 and 2 (MtNSP1 and 2) (Kaló et al. 2005; Smit et al. 2005) and MtCLV3/ESR-related 12 and 13 (MtCLE12 and 13) (Mortier et al. 2010; Saur et al. 2011). Nodulation is also positively and negatively controlled by complex communications with numerous hormones and peptides (Mortier et al. 2010, 2012; Larrainzar et al. 2015; van Zeijl et al. 2015). Together, these signals, along with NF/SYM pathway, control nodulation process and frequency on root system (Oldroyd 2013). A large number of infection threads will not result in to nodule formation (Djordjevic et al. 1986) which shows effect of negative regulatory routes facilitated by ethylene-related and CLE-related pathways (Kassaw et al. 2015).
The rhizobia occupy root hair cell by means of host-derived infection thread, which is usually initiated from the most acutely curled region, starting as invagination of root hair cell membrane (Fig. 7.4). Rhizobia move down in root hair to cortical cell layers by interiorly budding tube-like infection thread. Rhizobia in infection thread are surrounded by mucigel composed of cell wall polysaccharides, plant-derived matrix glycoprotein and rhizobial exopolysaccharides (Callaham and Torrey 1981; Broughten et al. 2000). Growth of infection thread continues towards newly synthesized nodule primordium which is produced by stimulation of mitotic activity in root cortex as a result of rhizobial Nod factors that afterward develops into the nodule meristem (Dudley et al. 1987). Infection thread branches and leads towards cortex and a clearly apparent nodule grow on root. Nodules may have one or more rhizobial strains and can be either determinant (lack a persistent meristem and are spherical) or indeterminate (situated at distal end of cylindrically shaped lobes) (Russelle et al. 2008). Many infections are terminated due to a failure in communication between rhizobia and the host plant leading to strict regulation of nodule number by the plant. In the root cortex, infection threads branch and enter in to individual nodule cells and a new structure, infection droplet, is formed and rhizobia get released into nodule tissue cells by a process that is similar to endocytosis (Roth and Stacey 1989a) and then occupy an organelle-like cytoplasmic compartment, designated as “symbiosome”, which is surrounded by a plant-derived peribacteroid membrane (Roth and Stacey 1989b). This process keeps microbes “outside” the plant where rhizobia are intracellular but extracytoplasmic. Peribacteroid membrane-enclosed bacteria divide until cytoplasm of every infected plant cell comprises several thousand rhizobial cells. In late symbiotic zone, infected cells are entirely occupied with bacteria that have differentiated into their pleomorphic endosymbiotic bacteroids (Brewin 1991) especially express nitrogen fixation genes. The plant uses the fixed nitrogen as nitrogen source and delivers bacteroids with photosynthates and amino acids as carbon, energy and nitrogen sources.
Nodulation factor secreted by rhizobia cause root hair deformation. Rhizobia occupy root hair cell by means of a host-derived infection thread
In the nodule primordium, rhizobia are released from infection droplet which gets differentiated into nitrogen-fixing bacteroids.
The preset senescence of nitrogen-fixing bacteroids is fundamental portion of growth sequence in indeterminate nodules (Vasse et al. 1990). At this stage, growth and division of bacteroids is ceased and lysis of N2-fixing bacteroids as well as host cells occurs. In recent times some papain-like and legumain-like cysteine proteases, also known as vacuolar processing enzymes (VPEs), were recognized that were intensely expressed throughout the development of nodule senescence (van Wyk et al. 2014). In nodules, papain-like cysteine proteases have known functions in the regulation of bacterial symbiosis, nitrogen fixation and leghemoglobin synthesis (Vande Velde et al. 2006; Li et al. 2008). Inhibition of papain-like cysteine protease activity was found to increase soybean tolerance to drought and favoured increased nodulation (Quain et al. 2014, 2015). VPEs found to be a part in age-linked senescence and triggering of pre-proteases. With their caspase-like activity, they additionally play significant part in programmed cell death (Hara-Nishimura et al. 2005; Roberts et al. 2012). At the death of a nodule, the bounded rhizobia are exclusively positioned to obtain the plant nutrients from senescing nodule tissues to proliferate rapidly. The number of nodule-derived rhizobia entering the soil population, becomes low as numerous rhizobial cells get destroyed together with plant cells during nodule senescence (Pladys et al. 1991) and also, differentiated bacteroids could not easily shift from biotrophic to saprotrophic life in soil (Quispel 1988).
7.5 Mechanisms of Plant Growth Promotion by Rhizobia
Rhizobia acts through direct and indirect mechanisms for improvement of crop growth and yield (Fig. 7.5). Direct mechanisms for plant growth promotion includes nitrogen fixation (Machado et al. 2013), nutrient solubilization/mobilization or mineralization (Reimann et al. 2008; Yu et al. 2012; Abd-Alla 1994a; Kumar and Ram 2014; Prasad et al. 2015), production of phytohormones, vitamins etc. (Sahasrabudhe 2011; Ghosh et al. 2015; Jangu and Sindhu 2011) (Table 7.2). In addition to symbiotic N2 fixation, rhizobia also carry out non-symbiotic N2 fixation in association with non-legume plants. Nitrogen fixation by photosynthetic bradyrhizobia was observed in association with wild rice (Chaintreuil et al. 2000). In indirect mechanism rhizobia produces bioactive molecules which inhibits phytopathogens (Datta and Chakrabartty 2014; Sindhu et al. 2014, 2017). Functionally different plant growth promoting rhizobacteria under variable environmental situations and in crop cultivation systems may enable growth and development of plants using either one or multiple mechanisms of plant growth promotion.
Diagrammatic representation illustrating the direct and indirect mechanisms of plant growth promotion by rhizobia
7.5.1 Biological Nitrogen Fixation
Fixation of atmospheric nitrogen by microorganisms is significant constituent of sustainable agriculture systems (Sessitsch et al. 2002; Karunakaran et al. 2009). Rhizobium are well known for establishment of symbiotic association with leguminous crops (Patriarca et al. 2002; Gage 2004) forming nodules to transforms atmospheric nitrogen in to ammonia and make it available to plants. In symbiotic relationship leguminous plants provides energy and photosynthetic materials to bacteria and bacteria in turn provide nitrogen to plants for incorporation into cellular constituents like amino acids, proteins and other essential nitrogenous compounds (Gresshoff 2003).
Nodules are generally termed as nitrogen fixation factories and millions of bacteroids inside the nodules fix the atmospheric nitrogen continually. Moreover, number of nodules formed on host plant is usually linked with amount of nitrogen fixed in particular Rhizobium-legume association. However, the number of nodules formed on a particular legume plant varies in different Rhizobium-legume systems. For example, the number of nodules formed ranges from 25–50 under sterilized chillum jar conditions in summer legumes such as green gram (Vigna radiata L. Wilczek), cow pea [Vigna ungulculata (L.) (Wilczek)], black gram [V. mungo (L.) (Hepper)]. Usually, 5–20 nodules are formed on cluster bean [Cyamopsis tetragonoloba (L.) (Taub)] and pigeon pea (Cajanus cajan). On the other hand, 30–60 nodules are usually formed under sterilized conditions on winter legume chick pea [Cicer arietinum (L.)] (Fig. 7.6). Large number of small nodules (50–120) is formed in ground nut (Arachis hypogea). Various environmental factors such as addition of nitrogenous fertilizers to the legume crops and level of ethylene formed due to hydrolysis of ACC in the root environment has been found to adversely affect nodulation under field conditions. Varin et al. (2009) reported that N fertilisation repressed nitrogen fixation in clover but N2 fixation was improved by addition of sulphur (S). Sulfur fertilization improved the nodule length and number of nodules containing leghaemoglobin. Sulphur fertilization, improved photosynthesis and vegetative reproduction in white clover directly and indirectly through increase in nitrogen fixation. Sulfur dependent response allows plants to adapt to variety of abiotic conditions but its sensitivity to S nutrition would be a shortcoming for rivalry in a state of soil sulphur poverty. Whereas, S fertilization could help sustain such plants under nitrogen limiting status.
Nodules formed on chick pea (Cicer arietinum) plant under sterilized chillum jar conditions
Mathews and Carroll (2018) reported that many edaphic factors such as pH, nutrient deficiencies and toxicities, water, and temperature affect nodulation, but nitrate is unique in that it is generally not inhibitory to plant growth. Estimates of energy costs are generally greater for nitrogen fixation than for nitrate assimilation. Besides this, there are other developmental and ecological considerations which may have resulted in natural selection for nitrate inhibition of nodulation. Nitrate can be assimilated in either, or both, root and shoot tissue of plant, whereas nitrogen fixation needs development of a specific organ, root or stem nodule. In young white clover seedlings, for example, maximum activities of nitrate reductase precede the highest rates of nitrogenase activity by a matter of weeks. Indeed, plants that are dependent on nitrogen fixation as the sole nitrogen source do not grow as well as those which are supplemented with low noninhibitory or larger levels of nitrate. In the ecological context, it can be assumed that nitrate utilization by legumes decreases the amount of soil nitrate available to adjacent nonsymbiotic plants that are competing for other nutrients. Thus, preferential utilization of nitrate may be advantageous for legume species by decreasing the competitive ability of other plants that are unable to form a nitrogen-fixing symbiosis.
Sindhu and Dadarwal (2001c) evaluated efficiency of mutant Rhizobium strains for nodulation on chick pea (Cicer arietinum) grown in sterilized chillum jars. Mutants of strains Ca85 and Ca401 showed no nodulation efficiency whereas mutants of strains Ca181 and Ca534 were not able to nodulate the roots and also unable to fix nitrogen. Further mutants also displayed reduced nodulation and nitrogenase activity which in turn showed decreased shoot dry weight as compared to inoculation of wild type strains. Overall, it was concluded that acquirement of streptomycin resistance in Rhizobium sp. Cicer strains showed decreased symbiotic efficiency of the microbial strain in chick pea.
Nitrogen fixation capacity of the Rhizobium strains is usually deliberated as one of the key character affecting plant growth. Nitrogen fixation is detected either by growth of the organisms to grow on nitrogen free medium and can be measured via 15N incorporation (15N enrichment) and acetylene reduction. Urban et al. (1986) prompted Rhizobium trifolii strain 0403 in nitrogen free medium by treating the cells with 16.6 mM succinic acid and other nutrients and observed that organisms grew luxuriously on semisolid or liquid medium and fix nitrogen to satisfy their own requirement. Nitrogen fixation was determined through 15N incorporation (18% 15N enrichment in 1.5 doublings) and acetylene reduction. Nitrogen-fixing cells showed a maximum specific nitrogenase activity of 5 nmol of acetylene reduced/min/mg of protein at 0.04 atm (ca. 4.05 kPa) and 3% oxygen concentration in liquid medium. The generation time of organisms in liquid medium at 30 °C was 1–5 days, depending on oxygen concentration. Nodulation studies by Rhizobium trifolii strain 0403 in the white clover showed in vitro nitrogenase activity indicating that at least portion of population retained characteristics of wild-type strain 0403.
During nitrogen fixation, enzyme nitrogenase catalyzes reduction of nitrogen to ammonia concomitant reduction of protons to hydrogen. The energy loss in proton reduction leading to H2 evolution varies from 40 to 60% in the absence of an active uptake hydrogenase. Some of the Rhizobium strains have been identified, which has the capability to oxidize the evolved H2 leading to more nitrogen fixation. Dadarwal et al. (1985) surveyed Rhizobium strains nodulating summer legumes cow pea [Vigna ungulculata (L.) (Wilczek)], black gram [V. mungo (L.) (Hepper)] and cluster bean [Cyamopsis tetragonoloba (L.) (Taub)] and a winter legume chick pea [Cicer arietinum (L.)] in Northern Plains of India and screened for hydrogenase activity to determine distribution of Hup character in the native ecosystem. Around 56% of Rhizobium strains of summer legumes were Hup+ winter legume, chick pea, was all Hup−. Ex planta acetylene reduction activity was observed in most of the Hup+ but not in the Hup− strains of any of the host species. In summer legume, mixed inoculation of Hup+ and Hup− strains under sterilized as well as unsterilized soil conditions, showed that the host species were predominantly nodulated with Hup+ strain.
Sindhu and Dadarwal (1986) reported that reduction of triphenyl tetrazolium chloride and methylene blue dyes reduction tests were ambiguous for detection of Hup character in Rhizobium strains isolated from green gram, black gram, cow pea, pigeon pea, cluster bean and chick pea. Hup+ Rhizobium strains isolated from these legumes except Hup− strains obtained from chick pea (Cicer arietinum) invariably expressed nitrogenase activity under cultural conditions. Characterization of native Rhizobium strains on the basis of ex planta nitrogenase induction showed that 94% of the ex planta nitrogenase positive isolate were of Hup+ phenotype, whereas all the ex planta nitrogenase negative isolates were of Hup- phenotype in nodules. The expression of nitrogenase under cultural conditions was therefore, found to be a reliable method for identification of Rhizobium strains for Hup+ phenotype among the rhizobia of the “cowpea miscellany”. Mutants were derived from Rhizobium strains of cowpea miscellany Vigna group i.e., S24 and GR4 having ability to express ex-planta acetylene reduction activity (ARA) after mutagenesis with nitrosoguanidine (Sindhu and Dadarwal 1992). Approximately, 70% of the mutants of strain S24 and 82% mutants of strain GR4 were found to have increased ex-planta ARA in comparison to their respective parent strains. Six mutants of strain S24 and four of GR4 strain with increased ex-planta ARA were selected to study in planta H2 uptake and symbiotic performance in two host species: green gram (Vigna radiata) and black gram (Vigna mungo). Most of mutants showed increased H2 uptake in nodules and symbiotic affectivity of these selected mutants was also higher than the parent strain in both the legumes. The authors suggested that it is possible to obtain symbiotically superior mutants by mutagenesis taking desirable ex-planta character for initial selection followed by plant test.
Saini et al. (1996) isolated native rhizobia from root nodules of Sesbania bispinosa and from root and stem nodules of S. rostrata. Rhizobium strains were studied for occurrence of hydrogen uptake system (Hup), nitrate respiration (NR), ex planta expression of nitrogenase and relative symbiotic efficiency in relation to Hup and NR activities. The rhizobia of both the host species were found to have two types of uptake hydrogenases: (i) recycling hydrogenase activity expressed ex planta as well as in planta in nodules and (ii) hydrogenase activity expressed only in nodules but not under cultural conditions. Dissimilatory nitrate reduction leading to complete denitrification was found to be common among both Hup+ as well as Hup− isolates. Ex planta nitrogenase activity was not observed in any isolates from both the Sesbania species. Symbiotic effectivity of Hup+ isolates was at par with Hup isolates. There was no specificity with regard to host infectivity and the stem nodulating rhizobia from S. rostrata formed root nodules on S. bispinosa as well as on S. rostrata.
The amount and type of carbon sources, nitrogen level in growth medium, temperature and growth conditions have been found to affect expression of nitrogenase and hydrogenase enzymes. Sindhu and Dadarwal (1988) observed influence of temperature on nitrogenase and uptake hydrogenase activities in nodules of green gram (Vigna radiata L. Wilczek), black gram (V. mungo L. Hepper) and chick pea (Cicer arietinum L.), inoculated with different Rhizobium strains at three different temperatures. The optimum temperature for nodule nitrogenase activity was 35 °C in green gram and black gram (summer legumes), while it was below 25 °C, in the case of chick pea (winter legume). A majority of the Hup+ Rhizobium strains of the summer legumes had H2 recycling ability that recycled the evolved H2 produced in nodules by nitrogenase. With increase in temperature from 15 to 35 °C, the H2 uptake rates also increased in nodules. In nodules formed with Hup− strains, although the H2 evolution rates increased with increase in temperature in all the three legumes, however, green gram and black gram nodules (summer legumes) evolved significantly higher amounts of H2 than chickpea (winter legume). Also, irrespective of temperature optima for ARA, at lower temperature, the relative efficiency was high in all the three legumes. Sindhu and Dadarwal (1995a) determined nodule nitrogenase and H2 uptake activities in normal (undecapitated) and decapitated plants (removal of shoot 24 h before measurements) of green gram and black gram inoculated with two Hup+ Rhizobium strains which had H recycling ability in excess to the rates of H2 produced by nitrogenase in nodules. A significant decline in nodule nitrogenase activity was observed in decapitated plants as compared to uncut control plants at 40 and 50 days of plant growth. However, nodules of both, control and decapitated plants, of both host species showed hydrogen supported enhanced acetylene reduction activity (ARA). The H2 uptake rates of the two strains varied depending on host as well as on stage of plant growth. However, based on the relative ratio of H consumed per mole of C2H2 reduced in case of normal photosynthate supply as well as from the interruption of photosynthate supply (decapitated plants), it appears that photosynthate supply remains a limiting factor in nitrogen fixation under normal conditions of plant growth during symbiosis.
7.5.2 Production of Plant Growth Regulators
Plant growth regulators are organic compounds like plant hormones that stimulates plant’s physiological response at lower concentration and hence effect plant development. Based on chemical structures and mode of action, plant growth regulators are grouped into six different categories i.e., auxins; cytokinins; gibberellins; ethylene; inhibitors (abscisic acid, phenolics and alkaloids) (Ferguson and Lessenger 2006; Mishra et al. 2006); and brassinosteroids (Rao et al. 2002; Bajguz and Tretyn 2003). Concentration of plant growth regulators produced by PGPR may vary from organism to organism. Majority of PGPR and symbiotic rhizobia influence plant growth by production of auxins, cytokinins and gibberellins, strigolactones, abscisic acid and brassinosteroids.
7.5.2.1 Auxins
About 80 % of the PGPRs and rhizobia produces most efficient biomolecule for plant growth promotion i.e. auxins (Antoun et al. 1998; Schlindwein et al. 2008; Bhagat et al. 2014). Major classes of auxins synthesized by soil microbes includes indole acetic acid (IAA), indole butyric acid or analogous compounds resulting from tryptophan metabolism (Loper and Schroth 1986; Malik and Sindhu 2008; Solano et al. 2008). Auxins are phyto-hormones that encourage cell division and elongation. Vargas et al. (2009) reported a considerable difference in auxin production amongst rhizobial isolates from arrow leaf clover (Trifolium vesiculosum) white clover (T. repens) nodules. Arrow leaf clover isolates showed IAA production frequency in more than 90% isolates whereas only 15% isolates showed IAA production. IAA producing rhizobia showed more intense nodule formation as auxins was reported to influence nodulation process (Boiero et al. 2007). IAA alters root morphology by increasing number of secondary roots and thereby increasing surface area as well as size and weight of roots. Which ultimately results in to improvement of more extensive root architecture of legume plants (Dazzo and Yanni 2006). Inoculation with auxin-producing bacteria may also result in the formation of adventitious roots (Solano et al. 2008). Modification in root architecture by rhizobacterial IAA enhance nutrient absorption by plants which ultimately results in to enhancement of plant growth (Probanza et al. 1996). Similarly, Biswas et al. (2000) reported that inoculation of rice with R. trifolii improved dry matter and grain production, in addition to augmentation in N, P, K and Fe content in plant tissue.
7.5.2.2 Cytokinins and Gibberellins
Cytokinins influence cell division and cell enlargement, in addition to influencing seed dormancy, flowering, fruiting and plant senescence (Ferguson and Lessenger 2006). Certain strains of Rhizobium synthesize cytokinins in culture but is quantification and characterization was not possible (Sturtevant and Taller 1989; Wang et al. 1982) but it is found to be involved in nodule formation by rhizobia (Frugier et al. 2008) via an unknown mechanism. Gamas et al. (2017) reviewed that cytokinins were involved in the precise identification of symbiotic associates, beginning of bacterial infection in root hair cells and commencement of nodule in root cortex. Progressively multifaceted regulatory networks was found in which cytokinin (CK) play critical functions in various phases of primary symbiotic stages. Interestingly, these parts can be positive or negative, cell independent or non-cell independent, and differ, relying on time, root tissues and probably legume species. Current progresses showed interconnected role of cytokinines in establishment of symbiotic relationship with other signaling pathways during nodule initiation. Gibberellins improve seed germination (Miransari and Smith 2009), encourage general growth of plants and postpones aging (Ferguson and Lessenger 2006). Production of lower concentration of gibberellins documented from Rhizobium (Solano et al. 2008). Several reports showed free-living rhizobial strains can produce small quantity of gibberellin like substances. Gibberellin was also believed to play a key role in Rhizobium-legume symbiosis that may be significant suggestions to endophytic colonization of non-legumes by rhizobia. For example, infection of A. caulinodans in S. rostrata was through intercellular crack entrance facilitated by gibberellins which is key process of endophytic colonization of non-legumes by rhizobia and gibberellins produced by bacteria may simplify this process (Lievens et al. 2005).
7.5.2.3 Strigolactones
Strigolactones (SLs) play a key part in governing root growth, shoot branching and plant-symbionts interaction (Rehman et al. 2018). Strigolactones produced by rhizobia and PGPRs have been found to affect nodule development. The presumed constituents of SL synthesis enzymes GmMAX1a and GmMAX4a with tissue expression patterns were identified and governed by rhizobia infection and modified throughout nodule formation. Knockdown transgenic hairy root soybean lines of GmMAX1a and GmMAX4a displayed reduced nodule number due to less expression of numerous nodulation genes necessary for nodule formation. Hormone analysis showed that GmMAX1a and GmMAX4a knockdown hairy roots showed increased level of ABA and JA but considerably reduced auxin content. This study showed close interactions between SL and other hormone signaling in controlling plant development and legume-rhizobia interaction.
7.5.2.4 Abscisic Acid and Brassinosteroids
ABA produced by certain strains of rhizobia like B. japonicum USDA110 (Boiero et al. 2007) can provide drought tolerance to plants to some extent. However, increase of ABA concentration also showed negatively effect on nodule development in Trifolium repens and Lotus japonicas. Suzuki et al. (2004) showed inhibition of nodulation in plants inoculated with R. trifolii and latter supplemented with ABA. Inoculation of L. japonicus mutant that has lesser sensitivity to ABA, (Tominaga et al. 2010) caused improved nodulation in M. loti inoculated plants.
Brassinosteroids are the new group of hormones and having steroidal substances which enables plants to resist abiotic stresses. Brassinosteroids generally found to affect processes such as seed germination, rhizogenesis, flowering, senescence, abscission and maturation (Rao et al. 2002). Vardhini and Ram Rao (1999) showed that treatment of brassinosteroids in groundnut gave better nodule formation and nitrogen fixation (Arachis hypogaea) developed in natural soil (without inoculation of Rhizobium).
7.5.3 Amelioration of Abiotic and Biotic Stress by Rhizobia
Climate change is the greatest threat to world’s agricultural sustainability in the twenty-first century. Drastic changes in various climatic conditions increase the incidence of abiotic and biotic stresses, which can tremendously influence the global decrease in productivity of agricultural and horticultural crops (Grover et al. 2011; Papworth et al. 2015). Global warming and alteration in precipitation patterns, lead to several abiotic stresses like extremes temperatures, drought, flooding, salinity, metal stress and nutrient stress that creates harmful effects on food production (Barrios et al. 2008; Selvakumar et al. 2012). The probability of occurrence of extreme climatic events has increased in the last couple of decades and farmers lack the management options to sustain the agricultural productivity (Kalra et al. 2013). Abiotic stress hamper growth and production of crop, causing land degradation by making soil nutrient deficient and more stress prone. The abiotic stresses are usually interconnected with one another and function as a chain due to climatic variations (Grover et al. 2011).
The improvement in crop yields under unfavourable conditions by classical breeding or gene transfer techniques pose certain limitations in terms of ethical issues and time requirements (Ashraf and Akram 2009; Fleury et al. 2010). Again, drought stress tolerance is often a complicated phenomenon involving clusters of gene networks. Apart from classical breeding and transgenic approaches, application of plant growth promoting rhizosphere (PGPR) bacteria is an alternative eco-friendly strategy for improving plant fitness under understressed environments (Kim et al. 2012) (Table 7.3). Application of beneficial rhizosphere bacteria has recently been found to alleviate the abiotic stresses. Some bacterial species such as P. polymyxa, Achromobacter piechaudii and R. tropici provide tolerance to drought stress in Arabidopsis, tomato (Solanum lycopersicum) and common bean (Phaseolus vulgaris), respectively through accumulation of abscisic acid and due to degradation of reactive oxygen species and ACC (1-aminocyclopropane-1-carboxylate) (Mayak et al. 2004b; Yang et al. 2008). Salinity tolerance in plants is conferred by application of A. piechaudii and B. subtilis (Mayak et al. 2004a; Zhang et al. 2006).
Figueiredo et al. (2008) identified enhanced antioxidant enzymatic activity in common bean plants (Phaseolus vulgaris L.) coinoculated with R. tropici and P. polymyxa under drought stress conditions. Treatment of pea plants with Pseudomonas spp. containing ACC deaminase somewhat removed effects of drought stress (Arshad et al. 2008). Similarly, treatment of tomato (Solanum lycopersicum L.) and pepper (Capsicum annuum L.) seedlings with A. piechaudii ARV8 decreased the production of ethylene (ET) that may have contributed to the observed drought tolerance (Mayak et al. 2004b). Lim and Kim (2013) showed that pepper plants treated with B. licheniformis K11 withstand drought stress and had better survival compared to non-treated plants. The observed drought tolerance was attributed to ACC deaminase production by PGPR that reduced ET concentrations by cleaving ACC.
Efficiency of Bradyrhizobium strains for alleviating effect of water stress was assessed in peanut genotypes through determination of antioxidant enzymes activities, leaf gas exchanges and vegetative growth in greenhouse with three peanut genotypes (BRS Havana, CNPA76 AM and 2012-4) (Barbosa et al. 2018). In experiment two Bradyrhizobium strains (SEMIA6144 and ESA123) under two levels of irrigations i.e. with and without irrigation were used. Plants grown under water deficiency showed alteration in leaf gas exchange as well as antioxidant activities and reduction of vegetative growth parameters. The plants inoculated with Bradyrhizobium strains SEMIA6144 and ESA123 showed increase in vegetative growth parameters, especially those inoculated with Bradyrhizobium sp. ESA123 strain obtained from the semi-arid region of Northeast Brazil. At in silico analyzes, ESA123 presented 98.97% similarity with the type strain of B. kavangense. The results uncovered beneficial effects of the peanut-Bradyrhizobium interaction under water stress condition.
Similarly, the consortium effect of three ACC-deaminase producing rhizobacteria - Ochrobactrum pseudogrignonense RJ12, Pseudomonas sp. RJ15 and Bacillus subtilis RJ46 was evaluated on drought stress alleviation in Vigna mungo L. and Pisum sativum L (Saikia et al. 2018). Consortium treatment significantly increased seed germination percentage, root length, shoot length and dry weight of treated plants. An elevated synthesis of reactive oxygen species scavenging enzymes and cellular osmolytes, higher leaf chlorophyll content, increase in relative water content and root recovery intension were observed after consortium treatment in comparison with the uninoculated plants under drought conditions. The consortium treatment decreased the ACC accumulation and down-regulated ACC-oxidase gene expression, suggesting that the consortium could be an efficient bio-formulator for crop health improvement in drought affected acidic agricultural fields.
Rhizobial species has also been found to differ in their intrinsic osmotolerance measured by capacity to tolerate and grow under variable concentration of NaCl. B. japonicum, R. etli and R. leguminosarum showed sensitivity to salt by complete growth inhibition at 100 mM NaCl (Boncompagni et al. 1999); whereas growth of Mesorhizobium huakuii, R. tropici IIB and S. fredii inhibited at 200 mM NaCl showing moderate sensitivity, but S. meliloti and A. tumefaciens found to be highly salt tolerant and grow at 300 mM NaCl (Bernard et al. 1986). Rhizobium spp. from nodules of Acacia, Hedysarum, Leucaena and Prosopis plants can withstand salt concentration up to 500 mM NaCl (Zhang et al. 1991). Rhizobia tolerate stress because of accumulation osmoprotectants, improved production of exopolysaccharides, ROS-scavenging enzymes and heat shock proteins and chaperons through expression of NaCl-responsive loci (Vriezen et al. 2007). Choudhary and Sindhu (2017) found fifty five rhizobacterial strains from the chickpea rhizosphere soil and selected for their salt tolerance. At 3% NaCl concentration, 41.8% rhizobacterial isolates formed colonies and only 10.9% isolates showed growth at 4% NaCl concentration.
Capacity of rhizobia to tolerate abiotic stresses like heavy metals and pesticides, aids rhizobia to accomplish their advantageous PGP activities in stress environments. Plant responses to various environmental stress is equally dependent on host plant reaction and symbiosis procedure of rhizobial symbiosis (Yang et al. 2010). Grover et al. (2011) revise importance of microorganisms in adaptation of crops to different abiotic stresses. There are widespread reports on tolerance and nodule forming efficiency of Rhizobium and Bradyrhizobium to soil acidity, salinity, alkalinity, temperature and osmotic stress conditions (Graham 1992; Kulkarni and Nautiyal 2000; Defez et al. 2017). Osmoprotectants, compatible solutes/osmolytes, similarly perform a multiple functions as showed in S. meliloti by proline-betaine that helps as both osmoprotectant (under high osmotic stress) and energy source (under low osmotic stress) (Miller-Williams et al. 2006).
Plants being sessile, their growth and yield are strongly influenced by biotic stress. Biotic stress is caused by various pathogens, such as bacteria, viruses, fungi, nematodes, protists and insects. Common impacts of these biotic factors include imbalanced hormonal regulation, nutrient imbalance and physiological disorder results in a substantial decrease in agricultural production (Haggag et al. 2015). Microbial diseases cause malfunction in plants which result in decrease in ability of plant to live and preserve its ecological niche. Plant diseases result either in death or may greatly impair growth and yield of the plant. Pathogenic microorganisms generally deteriorate or extinguish plant tissues and decrease crop production ranging from 25 to 100% (Choudhary and Sindhu 2015). Among the different kind of diseases, root diseases are projected to give 10–15% yield losses globally. Biotic stress also has adverse impacts on plants co-evolution, population dynamics, ecosystem nutrient cycling, natural habitat ecology and horticultural plant health (Gusain et al. 2015). Global crop yields are reduced by 20–40% annually due to pests and diseases (Strange and Scott 2005).
Yadav et al. (2015) obtained 207 strains of M. ciceri, from root nodules of chickpea plants and selected for antagonistic influence against F. oxysporum f. sp. ciceri. Seven strains (MC69, MC84, MC96, MC99, MC180, MC183 and MC190) showed antagonistic effects against F. oxysporum f. sp. ciceri, but none of them was observed to produce antibiotic or solubilized tricalcium phosphate. Three isolates i.e., MC84, MC96 and MC99 showed siderophore production. MC99 was found to be best antagonistic strain as it manufactured maximum quantity of siderophore.
7.5.4 Bioremediation of Organic Pollutants by Rhizobia
Many free-living rhizobial strains in the genera Rhizobium, Sinorhizobium and Bradyrhizobium showed resistance to polycyclic aromatic hydrocarbon (PAHs), polychlorinated biphenyl (PCBs), aromatic heterocycles (i.e., pyridine) or other toxic organic compounds (Keum et al. 2006; Poonthrigpun et al. 2006; Tu et al. 2011). Ahmad et al. (1997) isolated and characterized a different R. meliloti strains from soils polluted with aromatic/chloroaromatic hydrocarbons. Moreover, acenaphthylene and phenanthrene are omnipresent polycyclic hydrocarbons in the environment. Rhizobium sp. strain CU-A1 can completely degrade acenaphthylene (600 mg l−1) within three days of inoculation via naphthalene- 1, 8-dicarboxylic acid metabolism pathway (Poonthrigpun et al. 2006). Sinorhizobium sp. C4 can consume phenanthrene as a only carbon source and 16 intermediary metabolites engaged in degradation pathway have been recognized (Keum et al. 2006).
Polychlorinated biphenyls are classified as persistent organic pollutants (POPs) varying in the number of chlorine atoms (1–10) bound to their biphenyl rings (Passatore et al. 2014). Tu et al. (2011) reported degradation of more than 70% of 2, 4, 4-TCB (PCB28) by S. meliloti ACCC17519. In trials under aerobic conditions, 2- hydroxy-6-oxo-6-phenylhex-2, 4-dienoic acid (HOPDA), the meta cleavage product in typical PCBs-degradative pathway, was recognized as principal intermediate using GC-MS during the biotransformation of 2, 4, 4-TCB by S. meliloti. Certain toxic aromatic acids and their hydroaromatic biosynthetic intermediates (i.e., quinate and shikimate) usually disseminated in plants and rhizosphere found to encourage growth of rhizobia (Parke et al. 1985). Mimosine [β-N-(3-hydroxy-4-pyrid-one)-amino propionic acid], an aromatic toxin manufactured by the roots of Leucaena sp., is toxic to both bacteria and eukaryotic cells (Awaya et al. 2005). Several Rhizobium strains forming nodules on Leucaena reported to have ability to use mimosine as a source of carbon and nitrogen (Soedarjo et al. 1995; Soedarjo and Borthakur 1998), emphasizing catabolic efficiency of aromatic compounds in rhizobia.
7.5.5 Impacts of Grain Legumes and Rhizobia on Atmosphere and Soil Quality
Inclusion of legumes into agricultural cycles helps in decreasing usage of fertilizers and energy in arable systems and subsequently reducing GHG (greenhouse gases) productions (Reckling et al. 2016). N fertilizer savings across Europe (Reckling et al. 2016), in cycles comprising leguminous crops, range around 277 kg ha−1 of CO2 annually (Jensen et al. 2012). In view of an effectiveness of 2.6–3.7 kg CO2 produced per kilogram of N synthesized, annual global fertilizer results in emission of 300 Tg of CO2 into the atmosphere annually (Jensen et al. 2012). Moreover, the CO2 exhaled from nodule containing roots of leguminous plants derives from atmosphere by photosynthetic activities. On the other hand, all CO2 released in process of N-fertilizer production comes from fossil energy, thus defining a net influence on atmospheric concentration of CO2 (Jensen et al. 2012). N2O accounts for 5–6% of the total atmospheric GHG (Crutzen et al. 2007) and agriculture represents chief source about 60% of mane-made N2O emissions; (Reay et al. 2012), because of both animal and crop production. A major quantity of these productions derives from use of nitrogenous fertilizers. Application of 100 kg of N fertilizer emits 1.0 kg of N2O (Jensen et al. 2012) though various quantities of emission rely on number of factors viz. nitrogen application rate, soil organic carbon content, soil pH and texture (Peoples et al. 2009; Rochester 2007). Denitrification reaction is prime source of N2O in majority of cropping and pasture systems (Peoples et al. 2004; Soussana et al. 2010).
In latest years, numerous experiments focussed on role of legumes to decrease GHG productions. Jeuffroy et al. (2013) proved that legumes produce about 5–7 times less GHG per unit area in comparison to other crops. Measurement of nitrous oxide fluxes showed that peas released 69 kg N2O ha−1 which was far less than winter wheat emitting 368 kg N2O ha−1 and rape producing 534 kg N2O ha−1. Clune et al. (2017) studied various life cycle assessment (LCA) experiments on GHG production for the period of 2000 to 2015 world over showing Global Warming Potential (GWP) values of pulses was very low (0.50–0.51 kg CO2 eq kg−1 produce or bone-free meat). Schwenke et al. (2015) taken us two field trials in black Vertosol in sub-tropical Australia, showed 385 g N2O-N ha−1 which was significantly higher as compared to emission from chickpea (166 g N2O-N ha−1), faba bean (166 g N2O-N ha−1) and field pea (135 g N2O-N ha−1). Similarly they have also reported that grain legumes showed significantly lower emission factor proving that nitrogen fixed by legumes is less emissive form of nitrogen input as compared to fertilizer nitrogen. However, the key factor determining effect of legumes for reducing greenhouse gas emission governed by management of agro-ecosystems in which they are incorporated. Senbayram et al. (2016) reported that mono cropping of faba bean showed threefold higher collective N2O release (441 g N2O ha−1) as compared to unfertilized wheat (152 g N2O ha−1). On the other hand, intercropping of faba bean with wheat gave 31% less N2O emissions fluxes as compared to nitrogen fertilized wheat. Nevertheless, benefits obtained by addition of legumes in crop rotations turn out to be noteworthy when market charges of Nitrogenous fertilizer are considered (Jensen et al. 2012).
7.6 Influence of Rhizobium Application on Yield of Leguminous Crops
Rhizobium was extensively studied because of its importance in agriculture and environment (Karaman et al. 2013; Nyoki and Ndakidemi 2014). Application of efficient strains of Rhizobium showed significant increase in nodulation, nitrogen absorption and crop yield (Thies et al. 1991; Wani et al. 2007a; Franche et al. 2009) (Table 7.4). Elsheikh (1998) inoculation of five guar (Cyamopsis tetragonoloba) cultivars, namely, HFG-75, HFG-182, HFG-363, HFG-408 and WB-195 with Bradyrhizobium strains TAL 169 and TAL 1371 (introduced) and strains ENRRI 16A and ENRRI 16C (local) significantly enhanced yield, protein, crude fibre and mineral content in guar under field conditions. Indigenous isolates showed higher influence on nodulation and plant growth parameters as compared to exogenous strains. Karasu and Dogan (2009) reported that seed treatment of chick pea (Cicer arietinum) seeds with R. cicero showed significantly higher seed yield, plant height, first pod height, number of pods per plant, number of seeds per plant, harvest index and 1000 seed weight as compared to treatments receiving various doses of nitrogen through ammonium nitrate (0, 30, 60, 90 and 120 kg ha−1). Native genotype as crop material provided maximum yield (2149.1 kg ha−1) among three chick pea genotypes utilized. Various mixtures of microorganisms utilized looking to the further research needs in this area (Gopalakrishnan et al. 2015). Utilization of appropriate species of microbes as an inoculant in N exhausted environments might be a superior method to increase legume growth and development.
The response of treatment of various rhizobial species on legumes under various stress conditions depends on the host plant response (Table 7.5), but this response can also be affected by rhizobia and progression of symbiosis (Yang et al. 2010). Grover et al. (2011) has reviewed the job of microbes in adaptation of crops to different abiotic stresses. Moreover, soil acidity, salinity, alkalinity, temperature and osmotic stress conditions have been found to affect the resistance and nodulation capacity of Rhizobium and Bradyrhizobium in the soil (Graham 1992; Kulkarni and Nautiyal 2000; Defez et al. 2017).
Mfilinge et al. (2014) reported that inoculation of soybean (Glycine max L.) with Rhizobium showed significant increase in crop growth and yield components viz. number of branches bearing pod per plant, total number of pods per plant and seed number per pods. Seed treatment of R. leguminosarum in pea and lentil showed increased pea nodulation, shoot/root diversity and pea seed yield (Bourion et al. 2017). Likewise, seedling height, nodule and shoot biomass of lentil were increased. Bourion et al. (2017) reported increase in nodulation of chickpea by inoculation of Rhizobium species with significantly higher plant growth, root dry weight and number of nodules in greenhouse and field. Ravikumar (2012) reported significantly higher plant height, fresh weight, roots, nodules, leaves, shoots and pods number, pod length and seed weight of Vigna mungo and Vigna radiata inoculated with Rhizobium as compared to uninoculated control. Height of soybean plants treated with Rhizobium under field conditions was significantly higher and stem girth was also improved in greenhouse and field experiments (Tairo and Ndakidemi 2013). Likewise, Nyoki and Ndakidemi (2014) showed inoculation of cowpea with rhizobial isolates gave significantly higher plant height as compared to control treatment.
7.7 Coinoculation Effect of PGPR with Rhizobium Strains
The plant growth promoting effects of Rhizobium species are boosted when coinoculated with other microbes (Table 7.6). In coinoculation, some microbes function as assistant to improve the efficiency of the other microorganisms. Therefore, coinoculation of certain bacteria with Rhizobium spp. Improve efficiency of the rhizobial spp. Which ultimately results in increased crop productivity. Recently, coinoculation of Pseudomonas, Enterobacter, Serratia and Bacillus spp. with Rhizobium/Bradyrhizobium showed increase in number of nodules, nitrogen fixation and plant biomass of green gram, chickpea and other legumes (Sindhu et al.1999a, b, 2002a, b; Goel et al.2000). Therefore, combined inoculation of nitrogen fixing bacteria and PGPR could be explored for enhancing nitrogen fixation in rhizosphere of cereal and legume crops.
Coinoculation of N2-fixing A. vinelandii with Rhizobium spp showed increased number of nodules in soybean, pea (Pisum sativum) and clover (Trifolium pratense) (Burns et al. 1981). Sameway, combined inoculation of A. brasilense with Rhizobium resulted in higher efficiency in soybean and groundnut (Iruthayathas et al. 1983; Raverkar and Konde 1988). Coinoculation of Rhizobium spp. and Azospirillum spp. showed increased root hair formation, number of root nodules and flavonoid content in root exudates in comparison to individual application of Rhizobium spp. (Itzigsohn et al. 1993, Burdman et al. 1997; Remans et al. 2007, 2008). Efficiency of Azospirillum on the legume-Rhizobium symbiosis was also observed to be genotype dependent. Azospirillum – Rhizobium combined inoculation in common bean (Phaseolus vulgaris L.) cv. DOR364 showed increase in rate of nitrogen fixation and yield at all sites in field trials (Remans et al. 2008). Coinoculation of A. lipoferum and R. leguminosarum bv. trifolli showed enhanced nodule formation in white clovers (Tchebotar et al. 1998). The mechanisms behind enhanced efficacy was believed to be increase in infection sites for Rhizobium spp. by Azospirillum which in turn leads to improved nodule formation while application of Rhizobium and Azospirillum was found to increase siderophore, vitamins and phytohormones biosynthesis (Cassan et al. 2009; Dardanelli et al. 2008). Azotobacter came out as a potential coinoculant for Rhizobium as it increases vitamins and phytohormones synthesis which ultimately results in increase in nodule formation (Akhtar et al. 2012).
Coinoculation of R. phaseoli with P. putida showed increased nodulation of beans (Phaseolus vulgaris) under greenhouse and field trial conditions but no significant increase in bean yield was observed indicating increase in nodule numbers and Rhizobium infection has not direct correlation with crop yield (Grimes and Mount 1984). Bolton et al. (1990) also observed that coinoculation of Rhizobium and Pseudomonas spp. increases nodulation of pea but no significant difference were observed in shoot dry matter. On the contrary, combined inoculation of rhizobia with other rhizobacteria showed increase in nodule number, root length, plant biomass and yield in various legume crops. For example, Chanway et al. (1989) reported that individual inoculation of nine PGPR strains showed no significant impact on pea growth in field, whereas it gave against significant increase in emergence, vigour, nodule development, nitrogen fixation and root weight in lentil under field conditions. Combined inoculation of these nine strains of PGPR along with Rhizobium sp. cicer strain Ca181 showed increase in nodule numbers and growth of chickpea with simultaneous reduction of wilt disease (Khot et al. 1996).
Coinoculation of the five strains of fluorescent pseudomonad and R. leguminosarum biovar viciae enhances shoot and root length as well as dry weight of Pisum sativum L. cv. Capella (Dileep Kumar et al. 2001). Goel et al. (2002) reported that coinoculation of chickpea with Pseudomonas strains MRS23 and CRP55b, and Mesorhizobium sp. Cicer strain Ca181 showed 68.2–115.4% increase in nodule numbers at 80 and 100 days after planting, respectively as compared to inoculation of Mesorhizobium sp. Cicer strain Ca181 alone under sterile conditions. Treatments receiving combined inoculation showed 1.18–1.35 times higher shoot ratio as compared to that of Mesorhizobium inoculation and 3.25–4.06 times higher shoot ratio as compared to uninoculated control. Sameway combined inoculation of B. japonicum and P. fluorescens showed increase in nodule numbers and growth of soybean (Li and Alexander 1988; Nishijima et al. 1988; Dashti et al. 1998), R. meliloti with Pseudomonas in alfalfa (Li and Alexander 1988; Knight and Langston-Unkefer 1988), R. leguminosarum with P. fluorescens strain F113 in pea (Andrade et al. 1998) and Mesorhizobium/Bradyrhizobium strains with Pseudomonas sp. in green gram [Vigna radiata (L.) wilczek] and chickpea (Sindhu et al. 1999a, b; Goel et al. 2000, 2002). Fox et al. (2011) reported that coinoculation of Medicago truncatula with Pseudomonas fluorescens WSM3457 and Sinorhizobium showed increase in number of infection sites number of root hairs. Moreover, coinoculation of P. aeruginosa and Mesorhizobium sp. showed significantly higher shoot and root dry weight, nodule numbers, grain and straw yield as well as phosphorus uptake in chickpea (Verma et al. 2013). Besides growth promotion chickpea plants receiving inoculation of consortium comprising of A. chroococcum, Trichoderma harzianum, Mesorhizobium and P. aeruginosa showed antagonistic activities against Rhizoctonia solani and Fusarium oxysporum (Verma et al. 2014).
Holl et al. (1988) stated that inoculation of Bacillus species to seeds or roots changed configuration of rhizosphere which ultimately increase growth and yield of various legumes. For example, Halverson and Handelsman (1991) concluded that under field conditions seed treatment with B. cereus UW85 gave 31 to 133% higher nodules than untreated soybeans after 28 and 35 days of planting. In soybean plant grown in sterilized soil-vermiculite mixtures, application of UW85 through seed treatment showed 34 to 61% increase in nodulation at 28 days after planting. It was suggested that UW85 influenced nodule formation afterward planting by encouraging bradyrhizobial colonization or by defeating the termination of colonization process. In another experiment, Turner and Backman (1991) showed that seed treatment of peanut seeds with B. subtilis enhance germination and seedling emergence, improved nodulation by Rhizobium spp., enriched plant nutrition, decreased incidence of root cankers caused by Rhizoctonia solani AG-4 and increased root growth. Srinivasan et al. (1997) reported increase in nodule numbers in Phaseolus vulgaris by combined inoculation of R. etli strain TAL182 and B. megaterium S49 as it increased root hair propagation and lateral root development. Podile (1995) reported increase in nodule numbers, plant dry matter and grain yield of pigeon pea by combined inoculation of Bacillus sp. and rhizobia. Similar effects were observed in white clover (Holl et al. 1988). Sindhu et al. (2002a) reported that combined inoculation of Bacillus strains with efficient Bradyrhizobium strain S24 gave 1.28–3.55 times increase in dry mass at 40 days after sowing. Reports suggest that Bacillus strains can increase nodulation and nitrogen fixation at 40 days of plant growth (Mishra et al. 2009; Singh et al. 2011; Stajkovic et al. 2011). Elkoca et al. (2007) also showed increase in root weight and yield of chickpea by coinoculation of Rhizobium and Bacillus spp. Increase in nitrogen fixation and nodule formation was observed in the pigeon pea plants receiving combined inoculation of Azospirillum, Bacillus spp. and Rhizobium (Remans et al. 2008; Rajendran et al. 2008) (Table 7.6).
Mishra et al. (2009) showed that coinocualtion of R. leguminosarum-PR1 and PGPR B. thuringiensis-KR1, obtained from the nodules of Kudzu vine (Pueraria thunbergiana), promoted plant growth of field pea and lentil (Lens culinaris L.) under Jensen’s tube, growth pouch and non-sterile soil, respectively. Combined inoculation of R. leguminosarum-PR1 and B. thuringiensis-KR1 (106 cfu. ml−1) showed 85 and 73% increase in nodulation in pea and lentil, respectively as compared to individual treatment of R. leguminosarum-PR1. Similarly there was also higher shoot weight, root weight and total biomass was observed in combined inoculation treatments as compared to rhizobial application alone. There was 1.04 to 1.15 times and 1.03 to 1.06 times increase in shoot dry weight of pea and lentil, respectively by combined inoculation of different cell density of B. thuringiensis-KR1 as compared to inoculation of R. leguminosarum-PR1 alone at 42 days of sowing. Cell population of 106 cfu. ml−1 was found to be critical as higher cell density displayed inhibitory effects on plant growth and nodulation whereas lower one showed reduced cell retrieval and plant growth. Sameway increased nodule number and biomass yield were obtained upon combined inoculation of B. japonicum SB1 and B. thuringiensis-KR1 in soybean (Mishra et al. 2009).
Coinoculation of Rhizobium and P-solubilizing bacteria improved more plant growth as compared to individual applications (Morel et al. 2012; Walpola and Yoon 2013). Bai et al. (2003) stated that coinoculation of Bacillus strains with B. japonicum in soybean showed significant increases in nodulation, nodule weight, shoot weight, root weight, total biomass, total nitrogen and grain yield. Tariq et al. (2012) reported improvement in nodulation efficiency and grain yield by combined inoculation of plant growth promoting bacteria with crop specific rhizobia in legumes. Remans et al. (2007) showed Rhizobium isolates can effectively nodulate bean plants when coinoculated with phosphate solubilizing bacteria. Barbosa et al. (2007) showed that coinoculation of Bradyrhizobium sp. and Paenibacillus polymyxa Loutit (L) and Bacillus sp. (LBF410) can induce nodulation and increased root dry matter in Vigna unguiculata. Sameway, synergistic promotion of nitrogen fixation was observed upon coinoculation of endophytic PGPB and Rhizobium species in lentils (Khanna and Sharma 2011; Saini and Khanna 2012). In certain cases, PGPR strain which showed ability to increase efficiency of the Rhizobium strains in one legume does not showed same impact with another legume. For instance, Bacillus sp. strain CECT450 showed ability to improve nodule formation on common bean upon coinoculation with R. tropici CIAT 899, whereas it decreased nodule formation in soybean upon coinoculaion with B. japonicum USDA 110 (Camacho et al. 2001). Sameway, Elkoca et al. (2007) showed dual and triple mixtures of PGPR with Rhizobium OSU-142 and M-3 displayed no substantial result on common bean yield as compared to single inoculations of these bacteria except for B. subtilis strain OSU-142 + B. megaterium strain M-3, inoculation. Difference in response of coinoculation displayed necessity to develop suitable blends of rhizobia strain and PGPR for specific sites to improve growth of common bean.
Choudhary and Sindhu (2017) reported that coinoculation of chickpea with ACC deaminase producing Mesorhizobium strain MBD26 and rhizobacterial isolate RHD18 produced 59 nodules per plant and showed 112.9% increase in plant dry weight in comparison to untreated plants at 50 days of sowing. In presence of salt, bacterial inoculation displayed 31.2% increase in plant dry weight in comparison to untreated plants under in vitro conditions. At 80 days of sowing, combined inoculation of Mesorhizobium isolate MBD26 with rhizobacterial isolate RHD18 showed significant increase in nodule number (78 nodules/plant) and 141.9% increase in shoot dry weight in comparison to uninoculated controls.
7.8 Strategies for Improving N2 fixation
Research efforts for improving nitrogen fixation ability of various strain of nitrogen fixing free living or symbiotic microorganisms were intensified recently as they could provide an alternative source of chemical fertilizers and thereby reduce our reliance on chemical nitrogenous fertilizers. Selection of appropriate approach for improving nitrogen fixation ability of microbial strains depends largely on state in which microbial strain carry out nitrogen fixation either free-living or symbiotically and genes to be targeted for strain improvement i.e. either nitrogen fixation (nif, fix) or nodulation (nod, nol, noe) genes. Till date, efforts to improve nitrogen fixation capacity of symbiotic nitrogen fixers of genus Rhizobium and Bradyrhizobium were intensively done as they form symbiotic relations with agronomically significant legumes (Shantharam and Mattoo 1997; Schmidt et al. 2017).
Numerous approaches were projected to enhance nitrogen fixation in legume crops either by (i) improvement of nodulation and extending host range by transfer of symbiotic plasmid or cloning of nodulation genes; (ii) enrichment of nitrogen fixation; (iii) breeding of legume cultivars for improved nodulation with efficient strains and (iv) nodulation and nitrogen fixation in non-legume crops. Another methodology used comprises the genetic management of non-legumes to integrate nif genes from bacteria (Dixon et al.1997; Gough et al.1997) or expansion of host range for symbiosis amongst rhizobia and non-legumes (Trinick and Hadobas 1995; Sindhu and Dadarwal 2001b).
7.8.1 Intensification of Nodulation and Expansion of Host Range
Rhizobium-legume relations are frequently host specific and there exist concept of cross inoculation groups wherein specific Rhizobium strain can efficiently colonize specific host plant which make them restricted to colonize narrow range of crops (Brewin 1991). Some particular rhizobia linked with the families Cicereae, Trifolieae and Vicieae have limited host ranges (Broughten and Perret 1999). In other symbiotic relationships, host specificity differs significantly between the symbiontic partners. A. caulinodans nodulates only Sesbania rostrata and R. meliloti nodules found on Medicago, Melilotus and Trigonella plants, while Rhizobium sp. NGR234, nodulates above 137 genera of legumes and non-legumes like Parasponia andersonii (Young and Johnston 1989).
In actual field situations, legumes encounter large number of rhizobial strains and there are chances of legume facilitated genetic interchange amongst rhizobia or genetic altercation between rhizobia and other types of rhizosphere bacteria (Osborn 2006). Kinkle et al. (1993) showed that exchange of plasmid among populations of R. leguminosarum bv. viciae and B. japonicum respectively, in non-sterile soil. Souza et al. (1994) provided indication that gene transfer was regular between native soil populations of R. etli. Because of genetic recombinations occurring in nature, rearrangements of genetic material between bacteria in soil occurs which ultimately results in evolution of new rhizobial populations dissimilar from that of inoculated one (Sullivan et al.1995; Vlassak et al.1996). Many times such genetic manipulations could develop greatly adaptable rhizobial population that will govern nodule development in succeeding years.
7.8.1.1 Transfer of Symbiotic Plasmid
Large number of Rhizobium strains own plasmids containing genes influencing nodulation (nod, nol and noe genes), nitrogen fixation (nif and fix genes) as well as additional cellular functions (Denarie et al.1992; Fischer 1994). Symbiotic (sym) plasmids of R. leguminosarum and R. meliloti differ in size from 140 kb to 1500 kb (Beynon et al.1980; Long 1989). Number and size of these plasmids differs between various strains. Transfer of sym plasmid of R. leguminosarum to other closely related rhizobia belonging to either bv. trifolii, bv. viciae or bv. phaseoli normally induce development of normal nitrogen-fixing nodules on host plants of donor strains (Beynon et al.1980; Brewin et al.1980) but when the sym plasmid of R. leguminosarum was transferred to distantly related species of R. meliloti, the transconjugants induce non-nitrogen fixing root nodules on pea and vetch (Kondorosi et al.1980; Young and Johnston 1989). Similarly, Kondorosi et al. (1982) also observed that transconjugants of Lotus rhizobia or tropical cowpea miscellany rhizobia, carrying the symbiotic megaplasmid pRme41b of R. meliloti strain 41, formed white non-nitrogen-fixing nodules on Medicago sativa. When the sym megaplasmid (pRme41b) of R. meliloti was mobilized into Agrobacterium tumefaciens by cloning a mob region into the sym megaplasmid (Kondorosi et al.1982), the transconjugants were capable to induce ineffective nodule like deformations on alfalfa roots. Introduction of R. leguminosarum or R. trifolii sym plasmid into Agrobacterium tumefaciens conferred the ability to nodulate pea and clover, respectively but the nodules formed were ineffective without formation of bacteroids (Hooykaas et al.1981, 1982). Djordjevic et al. (1983) showed that transfer of plasmid pBRIAN (encoding clover specific nodulation and nitrogen fixation functions) to A. tumefaciens strain ANU109 enabled the strain to nodulate white clovers, whereas the same strain carrying the plasmid pJB5JI (encoding pea-specific nodulation and nitrogen fixation) failed to nodulate peas.
Truchet et al. (1984) mobilized the sym megaplasmid of R. meliloti strain 2011 into A. tumefaciens with the help of plasmid RP4 or PGM142. The consequential transconjugants encouraged root distortions on homologous hosts Medicago sativa and Melilotus alba but not on the heterologous hosts Trifolium repens and T. pratense. Cytological interpretations showed that bacteria entered only in shallow layers of host tissue by an uncommon infection progression. Sindhu and Dadarwal (1993) constructed recombinant strains by protoplast fusion between R. sp. Vigna and R. sp. Cicer that formed effective nodules on green gram but ineffective pseudonodules on chickpea. These results indicated that infection and nodule commencement genes could be expressed in heterologous rhizobia which leads to expansion of host range but bacteroid formation and formation of efficient nitrogen fixing nodules is challenging to attain.
A cryptic plasmid, pRmeGR4b, reported to affect nodulation capacity and competitiveness in R. meliloti GR4 (Sanjuan and Olivares 1989). Mutations in the relevant locus, spanning 5 kb region, delayed nodule formation and also reduced nodulation competitiveness. Nucleotide sequence analysis revealed the occurrence of two neighboring genes, nfe1 and nfe2 (nodule development proficiency), preceded by a functional σ54 and a NifA-dependent promoter (Soto et al.1993). The nfe genes were not present in four other strains of R. meliloti and transfer of nfe genes by conjugation in these strains was found to increase nodulation efficiency in two of strains (Sanjuan and Olivares 1991a). Expression of both nfe1 and nfe2 is perhaps triggered in infection and nodule formation by alteration to microaerobic situations that trigger NifA synthesis. Adding of several replicas of nifA from Klebsiella pneumoniae correspondingly conferred improved nodulation effectiveness of constructed R. meliloti strains (Sanjuan and Olivares 1991b). However, Dillewijn et al. (1998) reported that this observed increase in nodulation was not reliant on plasmid-borne nifA activity however it was dependent on sensitivity of non-resistant strains to streptomycin carried over from growth cultures. Rogel et al. (2001) revealed that Ensifer adhaerens ATCC 33499, could not form nodules on Phaseolus vulgaris (bean) and Leucaena leucocephala. Transferring symbiotic plasmid of R. tropici CFN299 into E. adhaerens enables it to form nitrogen fixing nodules on both hosts. R. tropici was carefully chosen as donor as its sym plasmids deliberated nitrogen fixing nodule formation ability to A. tumefaciens on Phaseolus vulgaris and Leucaena leucocephala (Martinez et al.1987). The plasmids “a” and “b” were co-transferred from R. tropici CFN299 together with plasmid “c” (carrying nod-nif genes) into A. tumefaciens. A. tumefaciens recombinant strains comprising three plasmids showed better nodulation and nitrogen fixation as compared to recombinant with only plasmid “c”.
7.8.1.2 Transfer of Cloned Nodulation Genes
Rhizobia possess coordinately regulated operons containing nodulation genes either one on symbiotic plasmids (psym) or one on chromosome. Till date, above 60 diverse nodulation genes were described in various rhizobia (Sindhu and Dadarwal 2001a, b, c; Loh and Stacey 2003; Delamuta et al. 2017). Spaink et al. (1989) created chimeric nodD gene, containing 75% of nodD1 gene of R. meliloti at the 5′ end and 27% of nodD gene from R. leguminosarum bv. trifolii. Its expression in R. leguminosarum bv. trifolii and R. meliloti lead to expansion of host range for nodulation up to tropical legumes Macroptilium atropurpureum, Lablab purpureus and Leucaena leucocephala. Expression of chimeric nodD gene in R. leguminosarum bv. trifolii and R. leguminosarum bv. viciae similarly lead to substantial escalation of nitrogen fixation rates during symbiosis with Vicia sativa and Trifolium repens. Bender et al. (1988) moved nodD1 gene from Rhizobium strain NGR234 to a limited host range R. leguminosarum bv. trifolii strain and this exchange widened nodulation ability of beneficiaries to new hosts comprising non-legume Parasponia andersonii. Point mutations in nodD of R. leguminosarum bv. trifolii showed expansion of host range even to non-legume Parasponia (McIver et al.1989).
The transfer of a 14 kb HindIII fragment on recombinant plasmid pRt032 (carrying nodABC and nodD genes from sym plasmid of R. leguminosarum bv. trifolii strain ANU843) to other Rhizobium species or to A. tumefaciens provide capacity to nodulate clover by recipients (Schofield et al. 1984). The conjugative transfer of 14 kb HindIII fragment on plasmids pRt032 and pRKR9032, to R. fredii USDA192 strain, extended the host range of R. fredii even to clover (Yamato et al.1997). Transconjugant strain NA102 and YA101 produce non nitrogen fixing small and whitish nodules on clover. The Nod factors synthesized by the transconjugants in presence of apigenin and genistein flavonoids also varied from those of their receiver strains. Concurrent inoculation of Glycine max and Vigna unguiculata roots with NodNGR factors and nodABC mutants of strain NGR234 or B. japonicum USDA110 enabled bacteria to produce nitrogen fixing nodules on corresponding hosts (Relic et al.1994). NodNGR factors also enabled entrance of R. fredii USDA257 into the roots of non-host Calopogonium caeruleum (Relic et al.1994) and of nodABC mutant of NGR234 into Macroptilium atropurpureum (Relic et al.1993).
The allocation of the host-specific nodFEGHPQ genes of R. meliloti to strains of R. leguminosarum bv. trifolii or bv. viciae provided capacity of nodule formation on alfalfa (Putnoky and Kondorosi 1986) but intensely repressed nodulation on usual host plants, white clover and vetch, respectively (Debelle et al.1988; Faucher et al.1989). Mutations in the nodH gene of R. meliloti (involved in transfer of sulfate on lipo-oligosaccharide Nod factor) intensely repressed nodulation on common host Medicago sativa and directed to hindered nodulation on Melilotus alba but provided capacity to nodulate non-host plant, vetch (Faucher et al.1988; Roche et al.1991). Mutation in nodQ gene also expanded host range of R. meliloti to vetch (Schwedock and Long 1992). Transfer of R. meliloti nodHPQ genes into R. leguminosarum bv. trifolii or R. leguminosarum bv. viciae, none of which owns these genes, indicates production of sulphated Nod signals and prolonged the host range of these strains to alfalfa (Denarie et al.1996; Long 1996). Mutation of strain NGR234 noeE gene (involved in fucose-specific sulfotransferase) obstructed nodulation of Pachyrhizus tuberosus, while its overview into closely linked strain USDA257 prolonged host range of R. fredii to encompass Calopogonium caeruleum (Hanin et al.1997).
NodL gene is essential for accumulation of an O-acetyl residue at terminal non-reducing glucosamine remainder in R. meliloti Nod factors (Ardourel et al.1994). In strain NGR234, interruption of flavonoid-inducible nolL gene results in synthesis of NodNGR factors that lack 3-O- or 4-O- acetate group (Berck et al.1999). The transconjugants of R. fredii strain USDA257 comprising nolL of NGR234 formed acetylated Nod factors and nodulated non-hosts Calopogonium caeruleum, L. leucocephala and L. halophilus. Acetylation of Nod factors’ fucose of R. etli similarly deliberated effective nodulation on some P. vulgaris cultivars and on different host Vigna umbellata (Corvera et al.1999). NodZ gene, encodes a fucosyltransferase, which is essential for nodulation of legume siratro by B. japonicum, but alteration in nodZ of B. japonicum does not affect nodulation in soybeans considerably (Nieuwkoop et al.1987; Stacey et al.1994). NodZ− mutants of NGR234 vanished the ability to nodulate Pachyrhizus tuberosus (Quesada-Vincens et al.1997). Allocation of nodZ gene to R. leguminosarum bv. viciae lead to in synthesis of fucosylated Nod signals and widen host range to comprise Macroptillium (Lopez-Lara et al.1996). Inactivation of gene nodS, involved in methylation of Nod factors of A. caulinodans, NGR234 and R. tropici eliminated nodulation of Leucaena leucocephala and Phaseolus vulgaris (Lewin et al.1990; Waelkens et al.1995). Transfer of either nodS or nodU gene into R. fredii USDA257 expanded host range to include Leucaena spp. (Krishnan et al. 1992; Jabbouri et al. 1995). These outcomes shown that numerous replacements or alterations at reducing or non-reducing terminus of Nod factors could broaden the host range.
Castillo et al. (1999) utilized precise DNA amplification (SDA) approach to create S. meliloti strains CFNM101 and CFNM103, that demarcated 2.5 to 3 copies of symbiotic region (containing nodD1, nodABC and nifN of psym plasmid). Application of these strains to alfalfa created escalation in nodulation, nitrogen fixation and growth of alfalfa plants in environmentally controlled situations. Likewise, Mavingui et al. (1997) employed random DNA amplification (RDA) in symbiotic plasmid of R. tropici to get strains with improved competency for nodulation.
7.8.2 Improvement of Nitrogen Fixation
Structural or regulatory nif genes of the nitrogenase enzyme complex can be altered to enhance efficiency of nitrogen fixation. It was proposed that increasing NifA construction, which is the transcriptional activator of other nif genes, could improve expression of entire N2-fixing system (Szeto et al.1990). Initially greenhouse experiments showed that certain R. meliloti strains with higher nifA gene expression exhibited a 7–15% rise in alfalfa plant biomass in comparison to parents (Williams et al.1990). Meanwhile regulatory stage in nitrogen fixation appears to be process of attaching reduced dinitrogenase reductase (Fe-protein, the nifH gene product) to dinitrogenase (MoFe-protein) followed by one electron transfer. It was observed that increase in copy numbers of nifH gene and its products result in increase in throughput rate of nitrogenase which seems to be reason for occurrence of more than one copy of the nifH gene in certain diazotrophs such as A. vinelandii (Jacobson et al. 1986), Rhizobium phaseoli (Quinto et al. 1985) and A. sesbaniae (Norel and Elmerich 1987).
Alteration in expression of the C4- dicarboxylate transport (dct) genes could increase substrate transport which in turn increase nitrogen fixation efficiency (Ronson et al.1990). Root nodules contains photosynthetic energy and utilize roughly 10% of the plant’s net photosynthates for nitrogen fixation. Therefore, nitrogen fixation in the Rhizobium-legume symbiosis is supposed to be partial by amount of plant-derived photosynthetic outputs accessible to bacteroids (Hardy and Havelka 1975; Sindhu et al. 2003). Birkenhead et al. (1988) proposed that increasing efficiency of endosymbiont to use photosynthate in nodule may results in improved nitrogen fixation rates. Recombinant strains of R. meliloti and B. japonicum with better expression of dctA (structural gene for dicarboxylate transport) and nifA genes exhibited 15% escalation in nitrogen fixation rates (Ronson et al.1990).
Certain nitrogen fixing bacteria like Rhizobium, Azotobacter, Azospirillum etc. found to increase efficacy of nitrogen fixation by oxidizing hydrogen by means of hydrogenase enzyme, that concurrently formed and developed during nitrogen fixation (Sindhu et al.1994; Garg et al. 1985). This oxidation of hydrogen enhance ATP biosynthesis. Improved nitrogen fixation efficiency described in nodules and bacteroids of soybean, pea and Vigna group of hosts designed by application of Hup+ strains (Emerich et al.1979; Dadarwal et al.1985; Evans et al.1987). Improved hydrogenase activity in root nodule bacteroids showed increase in soybean yield by use of near isogenic strains of B. japonicum (Hanus et al.1981; Hungaria et al.1989). Second strategy to increase yields could be to increase the activity of the hydrogenase in bacterial strains that previously own it. Mutants of Hup+ B. japonicum strains (Merberg and Maier 1983) or Rhizobium sp. strains (Sindhu and Dadarwal 1992) were developed with enhanced hydrogenase activity. Inocualtion of mutants of Rhizobium sp. strains showed higher in dry matter yield of green gram and black gram. The hup genes, coding biosynthesis of uptake hydrogenase was cloned and utilized to transform Hup- strains. These Hup+ recombinants exhibited increased nitrogen fixation (Pau 1991).
7.8.3 Breeding for Enhanced Nodulation
Changing the genetic make-up of plants to influence both endophytic and external populations suggest likelihood of creating favorite rhizosphere communities (O’Connell et al.1996; Sindhu et al. 2018). Plant breeding strategy could be used to combine preference traits from several sources to generate plant genotypes capable of excluding nodulation by ineffective indigenous rhizobia. Hardarson et al. (1982) showed that the selection of alfalfa for physiological and morphological traits associated with nitrogen fixation capability altered the preference of the host plant for effective strains of R. meliloti. Nutman (1984) reported that red clover bred for improved nitrogen fixation maintained its superiority against a range of R. leguminosarum bv. trifolii strains. These studies illustrated the potential for developing broad-spectrum effectiveness for genetically diverse indigenous rhizobia in some legume species. Mytton et al. (1984) assessed genetic variation in nitrogen fixation in different cultivars of M. sativa inoculated with diverse strains of R. meliloti; one of these cultivars was found relatively insensitive to changes in Rhizobium genotype and maintained high average yield.
The specific compatibility between nodX of R. leguminosarum bv. viciae strain TOM and sym2 of Pisum sativum cv. Afghanistan could be utilized to avoid native rhizobia from nodulating and to permit inoculated strains to nodulate. The sym2 gene has already been crossed into a desirable pea cultivar (Trapper) and nodX was transferred in effective N2-fixing Rhizobium strain. Performance of these manipulated host cultivar and rhizobial strains appeared promising enough under field studies (Fobert et al.1991). A similar combined approach involving alteration of both soybean host and Bradyrhizobium strains has also been carried out to improve symbiotic N2 fixation in soybean-B. japonicum symbiosis (Cregan et al.1989; Sadowsky et al.1991). This strategy involves use of soybean genotypes that restrict the nodulation of indigenous competitive strains and allow nodulation only with desired added strains (Sadowsky et al.1995). In this way, improved strains produced by genetic engineering or other techniques can be targeted to specifically improve soybean varieties. Thus development of legume cultivars with broad-spectrum effectiveness for genetically diverse indigenous rhizobia could be an alternative beneficial plant breeding strategy to obviate the requirement for legume inoculation (Brockwell and Bottomley 1995). This requires an understanding of the genetics of host and rhizobia, and offers real promise for genetically well-defined systems such as alfalfa and soybean.
Alternative approach of improving number of nodules by alteration of host genome is also utilized to increase nitrogen fixation ability in symbiotic microbes. Proposed strategy is based on hypothesis that nodule formation in legume is suboptimal and obviously increase in nodule numbers results into increased rate of nitrogen fixation. Hypernodulating mutants of soybean developed 100 times more nodules as compared to parent plant (Carroll et al.1985; Betts and Herridge 1987). Scientists have isolated number of soybean mutants with the higher nodulation efficiency even in presence of nitrate (Carroll et al.1985) which can produce 3–40 times higher number of nodules as compared to parent crop and demonstrated improved nitrogen fixation capacity (Hansen et al. 1989). Unluckily, these mutants were found to be poor agronomic performers (Pracht et al. 1994) due to fact that plant used up large extent of energy in hosting root nodules and thereby restricting energy required for the nitrogen fixation (Kennedy et al.1997). Sato et al. (1999) altered source-sink association in hypernodulating soybeans by reducing infection dose so that nodulation is optimized to standard level and resolved that autoregulatory control may play crucial role in improving the number of nodules in soybeans and total nitrogen fixation activity.
7.8.4 Nodulation and Nitrogen Fixation in Nonlegume Hosts
Certain non-legume plants are able to establish nitrogen-fixing symbiosis. The Frankia are of great importance which nodulates woody angiosperms like Alnus or Casuarina. These nodules have simple, branched structures; indicative of solidified lateral roots, however their capability to fix nitrogen is comparable to that in legumes (Clawson et al.1998). Likewise, non-legume nodulation and nitrogen fixation was seen with Bradyrhizobium application in Parasponia (Trinick and Hadobas 1995; Webster et al.1995) with high capacity of nitrogen fixation and structurally related to actinorhizal nodules.
NodD gene of rhizobia proved to regulate the initial level of host specificity (Denarie et al.1992). Transfer of nodD1 gene from NGR234 into R. leguminosarum bv. trifolii expanded host range to nodulate non-legume Parasponia andersonii (Bender et al.1988). Plasmids containing nodDABC genes of R. leguminosarum bv. trifolii were reassigned to A. tumefaciens, P. aeruginosa, Lignobacter sp., A. brasilense, E. coli and different non-nodulating mutant rhizobia (owning sym plasmid deletions) which enabled them to perform root hair curling and alterations on clover and large number of other non-host legumes (Plazinski et al.1994), proposing manifestation of nodDABC genes in varied array of soil bacteria may spread or effect normal growth of plant root hairs of a varied kind of host and non-host legumes. Attempts to enhance nitrogen fixation by modification of macrosymbiont host plant have been done with leguminous crops such as soybean and alfalfa. In recent times, two model legumes Medicago truncatula and Lotus japonicus are identified for genetic examination of nodule formation and operational facts of root nodules, by which transgenics can usually be produced. These legumes will perform as tools for the identification and genetic characterization of plant genes engaged in nodule development as well as provides idea about mechanisms controlling root nodule formation.
Present studies to transfer the nitrogen fixation capability to nonleguminous plants showed nodule like structures could be formed on rice and wheat roots with Rhizobium strains in artificial conditions by means of hormones or cell wall degrading enzymes (Al-Mallah et al.1989; Cocking et al.1994). A precise investigation of these nodule-like structures shown accumulation of bacteria at the spot of lateral root formation and get enter through cracks. Rhizobium strains obtained from Aeschynomene indica (strain ORS310) and Sesbania rostrata (strain ORS571) were observed to produce nodule like structures on developing secondary roots of rice, wheat and maize (Cocking et al.1994) and displayed considerable nitrogen fixation activity. Wheat plants inoculated with A. caulinodans showed higher nitrogen fixation activity whereas uninoculated plants as well as those inoculated with nif - strain of A. caulinodans showed absence of nitrogen fixation (Sabry et al.1997). A. caulinodans strain ORS571 having lacZ reporter gene was found to be present in cracks of developing lateral roots in rice and wheat (Webster et al.1997). Sameway, lacZ containing A. caulinodans strain ORS571 could enter Arabidopsis thaliana roots through cracks developed during lateral root formation. The flavonoids, naringenin and diadzein at low concentration considerably roused incidence of lateral root cracks and intercellular colonization of A. thaliana roots by A. caulinodans.
Tchan and Kennedy (1989) reveled induction of ‘para nodules’ on wheat by application of 2, 4-dichlorophenoxyacetic acid (2, 4-D) or with auxins IAA and NAA (Naphthyl-acetic acid), along with inoculation of rhizobia or Azospirillum. Rolfe and Bender (1991) demonstrated formation of paranodules on rice roots by inoculation of Rhizobium having nodD allele whose gene product interacts with rice root exudate but could not display nitrogenase activity. It was discussed that transformation of rice may induce new genes and thereby provides great chance to examine the probability for nitrogen fixation in rice. In addition, certain early nodulin homologous genes in legumes were detected in rice genome which is yet to be studied in depth.
In depth research understanding about different physiological and genetic processes in legume plants and bacteria as well as detection of key characters for nodulation in legumes might provide opportunity to enable nonlegumes like rice and wheat to be engaged in symbiosis with nitrogen fixing bacteria (Kennedy and Tchan 1992). Consequently, widespread fundamental studies are required to realize relations between Rhizobium and cereal plants with specific weightage on signal exchange mechanisms. Additionally, these altered nodule like structures on lateral roots of cereals must develop microaerobic environment for protection of oxygen sensitive nitrogenase. To develop oxygen protection mechanism, plant could be engineered to accumulate polysaccharides or other O2 eliminating material within intercellular space upon infection. Plentiful efforts and management are needed in genetics, molecular biology and developmental biology to attain a comprehensive understanding of the Rhizobium legume symbiosis and to discover future opportunities for attaining final objective of expressing active nitrogenase in cereal crops (Dixon et al.1997; Shantharam and Mattoo 1997).
7.9 Rhizobium Based Commercially Available Inoculants
Strategies to improve crop production by inoculating plant growth promoting bacteria is accelerated as developing technology because of their environment friendly potentials. Bioinoculants like biofertilizers has been popularized since many years to get advantage positive effects of various soil microbes to boost plant growth and yields. Biofertilizers are microbial inoculants comprising of microbial strains having capacity of nitrogen fixation, phosphate solubilization/mineralization, phytohormone production and biocontrol activities. Rhizobial strains generally utilized as biofertilizers (singly or in mixture) contain a number of genera: Allorhizobium, Azorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium (Table 7.7). Prime focus points for development of rhizobial biofertilizer technology are development of appropriate formulation with suitable carrier and adoption of appropriate application methods. Rhizobia-based inoculants generally used for improvement of growth and yield of leguminous crops, whereas Azotobacter and Azospirillum for enhancement of cereal growth. On contrary Bacillus and Pseudomonas are utilized as biocontrol agents (as biopesticides) against plant diseases (Fravel 2005; Bravo et al. 2011). Table 7.7 displays certain selected commercially existing rhizobial inoculants with their producers/trade name. The development of mass production technology for commercial manufacturing of microbial inoculants like biofertilizers is the key point to be considered for spreading wide use of biofertilizers.
7.10 Performance and Limitations of Inoculant Strains
Rhizobial inoculation in soil have showed colonization of soil as well as plant roots to a extent adequately high for proposed aim. In majority of the cases expected effect of biofertilizers inoculation is not witnessed under field conditions in legume or cereal plants and frequently fails to increase crop yield (van Elsas and Heijnen 1990; Akkermans 1994). Regulating factors for performance of microbial strains under field conditions includes abiotic soil factors such as texture, pH, temperature, moisture content and substrate accessibility which should be determined crucially as they showed great influence on survival and activity of inoculated microorganisms (Hegazi et al.1979; Sindhu and Lakshminarayana 1982; van Veen et al.1997; Hansena et al. 2018). Efficiency of inoculated nitrogen fixing bacterial strain is determined by genetic and physiological efficiency of bacterial strain (Brockwell et al.1995). Insertion of genetic markers viz. antibiotic resistance genes or other metabolic markers could assist to mark out introduced strains, whether it is rhizobia, cyanobacteria, azotobacter or azospirilla (Wilson et al.1995).
A main factor limiting feat of rhizobial inoculants is its inability to survive under competitive stress with the native strains for nodulation (Sindhu and Dadarwal 2000; Sindhu et al. 2003). Rhizobia produces bacteriocins which can inhibit growth of and nodulation by the native ineffective strains (Goel et al.1999; Sindhu and Dadarwal 2000). Transfer and expression of genes involved in trifolitoxin synthesis i.e. tfx genes in rhizobia resulted in to constant synthesis of trifolitoxin and controlled nodulation by indigenous trifolitoxin-sensitive strains on many leguminous crops (Triplett 1988, 1990). Though, efforts to manipulate some rhizobial genes in particular legume rhizosphere places for improving competence failed to show notable results (Nambiar et al.1990; Sitrit et al.1993; Krishnan et al.1999).
Biotechnological methods for improving nitrogen fixation and crop production having narrow utility in field conditions. For example, recombinant strain of R. meliloti and B. japonicum showed higher expression of nifA and dctA genes indicating intensification in rate of N2 fixation but in field conditions, recombinant strains didn’t performed well for nitrogen fixation or yield enhancement (Ronson et al.1990). Alteration of nodulation genes to increase bacterial competence generally resulted in either no nodulation, delayed nodulation or inefficient nodulation (Devine and Kuykendall 1996). Mendoza et al. (1995) improved NH4 + assimilating enzymes in R. etli by adding an extra copy of glutamate dehydrogenase (GDH), ultimately showed retardation of nodulation on bean plants. Such inhibitory effect was minimized by NifA and thereby postponing the inception of GDH activity after nodule formation (Mendoza et al.1998). In the same way, efforts to manipulate hydrogen uptake (Hup+) ability by cloning hydrogenase genes into Hup- strains of Rhizobium showed success only in parts where soybeans are cultivated under restricted photosynthetic energy (Evans et al.1987). Efforts to construct self-fertilizing crops for nitrogen was also disappointment due to complex nature of nitrogenase enzyme system under unavailability of oxygen safeguard system in eukaryotes (Dixon et al.1997). Stimulation of nodule formation (pseudonodules) in wheat and rice crops by lytic enzyme of hormonal treatment displayed nitrogenase activity and nitrogen integration in plants. However, the activity expressed is >1% of the significance seen in legumes (Cocking et al.1994).
7.11 Conclusion
Biological nitrogen fixation provides nitrogen to leguminous crops and hence considered to be significant process for improving yield. Symbiotic nitrogen fixing systems like rhizobia and legumes can fix significant quantity of nitrogen by acclimatizing with varied ecological conditions. So that, influence of rhizobia on legumes cannot be ascertained exactly under harsh environment and there is need to isolate stress tolerant rhizobial strains to act under stress in soil ecosystem which in turn ensures survival and growth of inoculated legumes in challenging soil. We are enriched with the research about molecular mechanism of nitrogen fixation but it is yet to be involved in applied aspects under field studies. As a way out of issue regarding establishment of microbes after inoculation, diazotrophic inoculants should be chosen from native ecological boundaries and re-inoculated in similar environment for ensuring anticipated benefits. Forthcoming research should concentrate on unveiling in situ physiology of inoculant and means to manipulate the same. On applied side, idea development of mixed inoculum with ecologically different strains having same roles should be tested as an alternative of monoculture. The coinoculation of diazotrophic bacteria with rhizosphere bacteria or the inoculation of microbial consortia is preferable because these microorganisms might express beneficial functions more frequently in a soil or rhizosphere system, even under ecologically diverse and/or variable circumstances. Hence, both customary and biotechnological methodologies can be used to improve nitrogen fixation efficiency and crop production in sustainable agriculture.
In general, inoculative application of Rhizobium provide 10–15% yield increase in leguminous crops. On the other hand, anticipated effect of biofertilizer application on legumes is generally not attained in field conditions. Commercial inoculants generally fails under field condition because of incompetence to strive with the native, ineffective microbes, which offers a competitive obstruction to inoculated strains. Efforts to operate some rhizobial genes in particular legume rhizosphere environment to improve survival under competitive stress were not successful up to mark. This chapter emphasize potential of plant growth promoting rhizobia for sustainable agriculture as well as highlighted exceptional characteristics to cope up with various biotic and abiotic stresses on a various agricultural crops. Thus, development of broad knowledge on screening approaches and concentrated selection of superlative Rhizobium strains for rhizosphere competence and survival is required to improve field efficiency of applied strains. Characterization of such prospective rhizobial strains and evolving a strong technology for farmers is still in developing phase. Current developments of ‘omics’ technologies provided prospects to exploit genomic, transcriptomic, proteomic and metabolomic means to alter the characters of ‘biological designers’ to maximize their plant growth promotion proficiency. Bioengineering could possibly be used to operate the tolerance, accumulation and degradation potentials of plants and microbes against pollutants.
Change history
27 April 2019
The original version of this chapter was inadvertently published without the sources for Tables 6.1, 6.2 and 6.3.
References
Aamir M, Aslam A, Khan MY, Jamshaid MU, Ahmad M, Asghar HN, Zahir ZA (2013) Coinoculation with Rhizobium and plant growth promoting rhizobacteria (PGPR) for inducing salinity tolerance in mung bean under field condition of semi-arid climate. Asian J Agric Biol 1:17–22
Abd-Alla MH (1994a) Solubilization of rock phosphates by Rhizobium and Bradyrhizobium. Folia Microbiol 39:53–56
Abd-Alla MH (1994b) Use of organic phosphorus by Rhizobium leguminosarum biovar viciae phosphatases. Biol Fertil Soils 18:216–218
Abd-Alla MH, El-Enany AWE, Nafady NA, Khalaf DM, Morsy FM (2014) Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol Res 169:49–58
Ahemad M, Khan MS (2009a) Toxicity assessment of herbicides quizalafop-p-ethyl and clodinafop towards Rhizobium pea symbiosis. Bull Environ Contam Toxicol 82:761–766
Ahemad M, Khan MS (2009b) Effect of insecticide-tolerant and plant growth promoting Mesorhizobium on the performance of chickpea grown in insecticide stressed alluvial soils. J Crop Sci Biotech 12:217–226
Ahemad M, Khan MS (2011) Insecticide-tolerant and plant growth promoting Bradyrhizobium sp. (Vigna) improves the growth and yield of green gram [Vigna radiata (L.) Wilczek] in insecticide stressed soils. Symbiosis 54:17–27
Ahemad M, Khan MS (2012a) Ecological assessment of biotoxicity of pesticides towards plant growth promoting activities of pea (Pisum sativum)-specific Rhizobium sp. strain MRP1. Emirates J Food Agric 24:334–343
Ahemad M, Khan MS (2012b) Productivity of green gram in tebuconazole-stressed soil by using a tolerant and plant growth promoting Bradyrhizobium sp. MRM6 strain. Acta Physiol Plant 34:245–254
Ahemad M, Khan MS (2012c) Effects of pesticides on plant growth promoting traits of Mesorhizobium strain MRC4. J Saudi Soc Agric Sci 11:63–71
Ahmad D, Mehmannavaz R, Damaj M (1997) Isolation and characterization of symbiotic N2-fixing Rhizobium meliloti from soils contaminated with aromatic and chloroaromatic hydrocarbons: PAHs and PCBs. Int Biodeter Biodegr 39:33–43. https://doi.org/10.1016/S0964-8305(96)00065-0
Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181
Ahmad M, Zahir ZA, Asghar HN, Asghar M (2011) Inducing salt tolerance in mung bean through coinoculation with rhizobia and plant-growth-promoting rhizobacteria containing 1-aminocyclopropane-1- carboxylate-deaminase. Can J Microbiol 57:578–589
Ahmad M, Zahir ZA, Khalid M, Nazli F, Arshad M (2013) Efficacy of Rhizobium and Pseudomonas strains to improve physiology, ionic balance and quality of mung bean under salt-affected conditions on farmer’s fields. Plant Physiol Biochem 63:170–176
Akhtar N, Qureshi MA, Iqbal A, Ahmad MJ, Khan KH (2012) Influence of Azotobacter and IAA on symbiotic performance of Rhizobium and yield parameters of lentil. J Agric Res 50:361–372
Akkermans ADL (1994) Application of bacteria in soils: problems and pitfalls. FEMS Microbiol Rev 15:185–194
Alexandre A, Oliveira S (2011) Most heat-tolerant rhizobia show high induction of major chaperone genes upon stress. FEMS Microbiol Ecol 75:28–36
Al-Mallah MK, Davey MR, Cocking EC (1989) Formation of nodular structures on rice seedlings by rhizobia. J Expt Bot 40:473–478
Andrade G, De Leij FAAM, Lynch JM (1998) Plant mediated interactions between Pseudomonas fluorescens, Rhizobium leguminosarum and arbuscular mycorrhizae on pea. Lett Appl Microbiol 26:311–316
Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57–68
Appelbaum E (2018) The Rhizobium/Bradyrhizobium-legume symbiosis. In: Molecular biology of symbiotic nitrogen fixation. CRC Press, Boca Raton, pp 131–158
Ardourel M, Demont N, Debelle F, Maillet F, de Billy F, Prome JC, Denarie J, Truchet G (1994) Rhizobium meliloti lipo-oligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic development responses. Plant Cell 6:1357–1374
Arora NK, Kang SC, Maheshwari DK (2001) Isolation of siderophore producing strains of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr Sci 81:673–677
Arshad M, Shaharoona B, Mahmood T (2008) Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield and ripening of pea (Pisum sativum L.). Pedosphere 18:611–620
Ashraf M, Akram NA (2009) Improving salinity tolerance of plants through conventional breeding and improving salinity tolerance of plants through conventional breeding and genetic engineering: an analytical comparison. Biotechnol Adv 27:744–752
Awaya JD, Fox PM, Borthakur D (2005) pyd Genes of Rhizobium sp. strain TAL1145 are required for degradation of 3-hydroxy-4-pyridone, an aromatic intermediate in mimosine metabolism. J Bacteriol 187:4480–4487. https://doi.org/10.1128/JB.187.13.4480-4487.2005
Bai Y, Zhou X, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43(5):1774–1781
Bajguz A, Tretyn A (2003) The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62:1027–1046
Barbosa JA, Silva LP, Teles RC, Esteves GF, Azevedo RB, Ventura MM, de Freitas SM (2007) Crystal structure of the Bowman-Birk inhibitor from Vigna unguiculata seeds in complex with β-Trypsin at 1.55 Å resolution and its structural properties in association with proteinases. Biophysical J 92(5):1638–1650
Barbosa DD, Brito SL, Fernandes PD, Fernandes-Junior PI, Lima LM (2018) Can Bradyrhizobium strains inoculation reduce water deficit effects on peanuts? World J Microbiol Biotechnol 34:87. https://doi.org/10.1007/s11274-018-2474-z
Barrios S, Ouattara B, Strobl E (2008) The impact of climatic change on agricultural production: is it different for Africa? Food Policy 33(4):287–298
Bender GL, Nayudu M, Le Strange KK, Rolfe BG (1988) The nodDI gene of Rhizobium strain NGR234 is a key determinant in the extension of host range to non-legume Parasponia. Mol Plant Microbe Interact 1:254–256
Berck S, Perret X, Quesada-Vincens D, Prome JC, Broughten WJ, Jabbouri S (1999) NolL of Rhizobium sp. NGR234 is required for O-acetyltransferase activity. J Bacteriol 181:957–964
Bernard T, Pocard JA, Perroud B, Le Rudulier D (1986) Variations in the response of salt-stressed Rhizobium strains to betaines. Arch Microbiol 143:359–364
Berraho EL, Lesueur D, Diem HG, Sasson A (1997) Iron requirement and siderophore production in Rhizobium ciceri during growth on an iron-deficient medium. World J Microbiol Biotechnol 13:501–510
Betts JH, Herridge DF (1987) Isolation of soybean lines capable of nodulation and nitrogen fixation under high levels of nitrate supply. Crop Sci 27:1156–1161
Beynon JL, Beringer JE, Johnston AWB (1980) Plasmids and host range in Rhizobium leguminosarum and Rhizobium phaseoli. J Gen Microbiol 120:421–429
Bhagat D, Sharma P, Sirari A, Kumawat KC (2014) Screening of Mesorhizobium spp. for control of Fusarium wilt in chickpea in vitro conditions. Int J Curr Microbiol Appl Sci 3:923–930
Birkenhead K, Manian SS, O’Gara F (1988) Dicarboxylic acid transport in Bradyrhizobium japonicum: use of Rhizobium meliloti dct gene(s) to enhance nitrogen fixation. J Bacteriol 170:184–189
Biswas J, Ladha J, Dazzo F (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650
Bockman OC (1997) Fertilizers and biological nitrogen fixation as sources of plant nutrients: perspectives for future agriculture. Plant Soil 194:11–14
Bohlool BB, Ladha JK, Garrity DP, George T (1992) Biological nitrogen fixation for sustainable agriculture: a perspective. Plant Soil 141(1-2):1–11
Boiero L, Perrig D, Masciarelli O, Penna C, Cassán F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880
Bolton H Jr, Elliott LF, Turco RF, Kennedy AC (1990) Rhizoplane colonization of pea seedlings by Rhizobium leguminosarum and deleterious root colonizing Pseudomonas sp. and effects on plant growth. Plant Soil 123:121–124
Boncompagni E, Osterås M, Poggi MC, Le Rudulier D (1999) Occurrence of choline and glycine betaine uptake and metabolism in the family rhizobiaceae and their roles in osmoprotection. Appl Environ Microbiol 65:2072–2077
Bourion V, Heulin-Gotty K, Aubert V, Tisseyre P, Chabert-Martinello M, Pervent M, Delaitre C, Vile D, Siol M, Duc G, Brunel B (2017) Coinoculation of a pea core-collection with diverse rhizobial strains shows competitiveness for nodulation and efficiency of nitrogen fixation are distinct traits in the interaction. Front Plant Sci 8:2249
Bravo A, Likitvivatanavong S, Gill SS, Soberón M (2011) Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol 41(7):423–431
Brewin NJ (1991) Development of the legume root nodule. Annu Rev Cell Biol 7:191–226
Brewin NJ, Beringer JE, Johnston AWB (1980) Plasmid mediated transfer of host range specificity between two strains of Rhizobium leguminosarum. J Gen Microbiol 120:413–420
Brockwell J, Bottomley PJ (1995) Recent advances in inoculant technology and prospects for the future. Soil Biol Biochem 27:683–697
Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180
Broughten WJ, Perret X (1999) Geneology of legume-Rhizobium symbioses. Curr Opinion Plant Biol 2:305–311
Broughten WJ, Jabbouri S, Perret X (2000) Keys to symbiotic harmony. J Bacteriol 182:5641–5652
Burdman S, Kigel J, Okon Y (1997) Effects of Azospirillum brasilense on nodulation and growth of common bean (Phaseolus vulgaris L.). Soil Biol Biochem 29:923–929
Burns TA, Bishop PE, Israel DW (1981) Enhanced nodulation of leguminous plant roots by mixed cultures of Azotobacter vinelandii and Rhizobium. Plant Soil 62(3):399–412
Callaham DA, Torrey JG (1981) The structural basis for infection of root hairs of Trifolium repens by Rhizobium. Can J Bot 59:1647–1664
Camacho M, Santamaria C, Temprano F, Rodriguez-Navarro DN, Daza A (2001) Coinoculation with Bacillus sp. CECT 450 improves nodulation in Phaseolus vulgaris L. Can J Microbiol 47(11):1058–1062
Cao Y, Halane MK, Gassmann W, Stacey G (2017) The role of plant innate immunity in the legume-Rhizobium symbiosis. Annu Rev Plant Biol 68:535–561
Carroll BJ, McNeil DL, Gresshoff PM (1985) A supernodulation and nitrate tolerant symbiotic (nts) soybean mutant. Plant Physiol 78:34–40
Cassan F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35
Castillo M, Flores M, Mavingui P, Martinez-Romero E, Palacios R, Hernandez G (1999) Increase in alfalfa nodulation, nitrogen fixation and plant growth by specific DNA amplification in Sinorhizobium meliloti. Appl Environ Microbiol 65:2716–2722
Chaintreuil C, Giraud E, Prin Y, Lorguin J, Ba A, Gillis M, De laiudie P, Dreyfus B (2000) Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl Environ Microbiol 66:5437–5447
Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere competent Mesorhizobium loti MP6 induces root hair curling, inhibits Sclerotinia sclerotiorum and enhances growth of Indian mustard (Brassica campestris). Braz J Microbiol 38:128–130
Chanway CP, Hynes RK, Nelson LM (1989) Plant growth promoting rhizobacteria: effect on the growth and nitrogen fixation of lentils (Lens esculenta Moench) and pea (Pisum sativum L.). Soil Biol Biochem 21:511–512
Chen C, Zhu H (2013) Are common symbiosis genes required for endophytic rice-rhizobial interactions? Plant Signal Behav 8(9):e25453
Chen YS, Shiuan D, Chen SC, Chye SM, Chen YL (2003) Recombinant truncated flagellin of Burkholderia pseudomallei as a molecular probe for diagnosis of melioidosis. Clin Diagn Lab Immunol 10(3):423–425
Chen WM, de Faria SM, Chou JH, James EK, Elliott GN, Sprent JI, Bontemps C, Young JP, Vandamme P (2008) Burkholderia sabiae sp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 58(9):2174–2179
Choudhary SR, Sindhu SS (2015) Suppression of Rhizoctonia solani root rot disease of clusterbean (Cyamopsis tetragonoloba) and plant growth promotion by rhizosphere bacteria. Plant Pathol J 14:48–57
Choudhary D, Sindhu SS (2017) Amelioration of salt stress in chickpea (Cicer arietinum L.) by coinoculation of ACC deaminase containing rhizosphere bacteria with Mesorhizobium strains. Legume Res 40(1):80–86
Clawson ML, Carú M, Benson DR (1998) Diversity of Frankia strains in root nodules of plants from the families Elaeagnaceae and Rhamnaceae. Appl Environ Microbiol 64(9):3539–3543
Clune S, Crossin E, Verghese K (2017) Systematic review of greenhouse gas emissions for different fresh food categories. J Clean Prod 140:766–783
Cocking EC, Webster G, Batchelor CA, Davey MR (1994) Nodulation of non-legume crops: a new look. Agro-Industry Hi-Tech. 21–24
Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103(5):1355–1365
Corvera A, Prome D, Prome JC, Martinez-Romero E, Romero D (1999) The nolL gene from Rhizobium etli determines nodulation efficiency by mediating the acetylation of the fucosyl residue in the nodulation factor. Mol Plant Microbe Interact 12:236–246
Cregan PB, Keyser HH, Sadowsky MJ (1989) Host plant effect on nodulation and competitiveness of the Bradyrhizobium japonicum serotype strains constituting serocluster 123. Appl Environ Microbiol 55:2532–2536
Crook MB Jr (2013) Modulators of symbiotic outcome in Sinorhizobium meliloti. Brigham Young University
Crutzen PJ, Mosier AR, Smith KA, Winiwarter W (2007) N2O release from agro-biofuel production negates global warming reduction by replacing fossil fuels. Atmos Chem Phys Discus 7(4):11191–11205
Dadarwal KR, Sindhu SS, Batra R (1985) Ecology of Hup+ Rhizobium strains of cowpea miscellany: native frequency and competence. Arch Microbiol 141:255–259
Dahale SK, Prashanthi SK, Krishnaraj PU (2016) Rhizobium mutant deficient in mineral phosphate solubilization activity shows reduced nodulation and plant growth in green gram. Proc Natl Acad Sci India Sect B Biol Sci 86(3):723–734
Dardanelli MS, de Cordoba FJF, Espuny MR, Carvajal MAR, Díaz MES, Serrano AMG, Okon Y, Megias M (2008) Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biol Biochem 40:2713–2721
Dashti N, Zhang F, Hynes RK, Smith DL (1998) Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean [Glycine max (L.) Merr.] under short season conditions. Plant Soil 200:205–213
Datta B, Chakrabartty PK (2014) Siderophore biosynthesis genes of Rhizobium sp. isolated from Cicer arietinum L. 3 Biotech 4:391–401
David H, Ian R (2000) Breeding for enhanced nitrogen fixation in crop legumes. Field Crops Res 65:229–248
Dazzo FB, Yanni YG (2006) The natural Rhizobium-cereal crop association as an example of plant-bacteria interaction. Biological approaches to sustainable soil systems. CRC Press, Boca Raton, pp 109–127
Debelle F, Maillet F, Vasse J, Rosenberg C, de Billy F, Truchet G, Denarie J, Ausubel FM (1988) Interference between Rhizobium meliloti and Rhizobium trifolii nodulation genes: Genetic basis of R. meliloti dominance. J Bacteriol 170:5718–5727
Defez R, Andreozzi A, Dickinson M, Charlton A, Tadini L, Pesaresi P, Bianco C (2017) Improved drought stress response in alfalfa plants nodulated by an IAA over-producing Rhizobium strain. Front Microbiol 8:2466–2473
Delamuta JR, Menna P, Ribeiro RA, Hungria M (2017) Phylogenies of symbiotic genes of Bradyrhizobium symbionts of legumes of economic and environmental importance in Brazil support the definition of the new symbiovars pachyrhizi and sojae. Syst Appl Microbiol 40(5):254–265
Denarie J, Debelle F, Rosenberg C (1992) Signaling and host range variation in nodulation. Annu Rev Microbiol 46(1):497–531
Denarie J, Debelle F, Prome JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: Signalling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535
Deshwal VK, Dubey RC, Maheshwari DK (2003) Isolation of plant growth promoting strains of Bradyrhizobium (Arachis) sp. with biocontrol potential against Macrophomina phaseolina causing charcoal rot of peanut. Curr Sci 84:443–444
Devine TE, Kuykendall LD (1996) Host genetic control of symbiosis in soybean (Glycine max L.). Plant Soil 186:173–187
Di Benedetto NA, Corbo MR, Campaniello D, Cataldi MP, Bevilacqua A, Sinigaglia M, Flagella Z (2017) The role of plant growth promoting bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat. AIMS Microbiol 3(3):413–434
Dileep Kumar BS, Berggren I, Maartensson AM (2001) Potential for improving pea production by coinoculation with fluorescent Pseudomonas and Rhizobium. Plant Soil 229:25–34
Dillewijn P, Martinez-Abarca F, Toro N (1998) Multicopy vectors carrying the Klebsiella pneumoniae nifA gene do not enhance the nodulation competitiveness of Sinorhizobium meliloti on alfalfa. Mol Plant Microbe Interact 11:839–842
Dixon R, Cheng Q, Shen GF, Day A, Day MD (1997) nif genes and expression in chloroplasts: prospects and problems. Plant Soil 194:193–203
Djordjevic MA, Zurkowski W, Shine J, Rolfe BG (1983) Sym plasmid transfer to symbiotic mutants of Rhizobium trifolii, Rhizobium leguminosarum and Rhizobium meliloti. J Bacteriol 156:1035–1045
Djordjevic MA, Innes RW, Wijffelman CA, Schofield PR, Rolfe BG (1986) Nodulation of specific legumes is controlled by several distinct loci in Rhizobium trifolii. Plant Mol Biol 6:389–401
Djordjevic MA, Mohd-Radzman NA, Imin N (2015) Small peptide signals that control nodule number, development and symbiosis. J Expt Bot 66:5171–5181. https://doi.org/10.1007/s11104-015-2445-1
Downie JA (1994) Signalling strategies for nodulation of legumes by rhizobia. Trends Microbiol 2(9):318–324
Dudley ME, Jacob TH, Long SR (1987) Microscopic studies of cell divisions induced in alfalfa roots by Rhizobium meliloti. Planta 171:289–301
Duhan JS, Dudeja SS, Khurana AL (1998) Siderophore production in relation to N2 fixation and iron uptake in pigeon pea-Rhizobium symbiosis. Folia Microbiol 43(4):421–426
Eaglesham AR (1989) Nitrate inhibition of root-nodule symbiosis in doubly rooted soybean plants. Crop Sci 29(1):115–119
Echeverria M, Sannazzaro AI, Ruiz OA, Menéndez AB (2013) Modulatory effects of Mesorhizobium tianshanense and Glomus intraradices on plant proline and polyamine levels during early plant response of Lotus tenuis to salinity. Plant Soil 364:69–79
Egamberdieva D, Berg G, Lindström K, Räsänen LA (2013) Alleviation of salt stress of symbiotic Galega officinalis L. (goat’s rue) by coinoculation of Rhizobium with root-colonizing Pseudomonas. Plant Soil 369:453–465
Elkan GH (1992) Biological nitrogen fixation systems in tropical ecosystems: an overview. In: Mulongoy K, Gueye M, Spencer DSC (eds) Biological nitrogen fixation and sustainability of tropical agriculture. Wiley, Chichester, pp 27–40
Elkoca E, Kantar F, Sahin F (2007) Influence of nitrogen fixing and phosphorus solubilizing bacteria on the nodulation, plant growth and yield of chickpea. J Plant Nutr 31:157–171
Elsheikh EA (1998) Effects of salt on rhizobia and bradyrhizobia: a review. Annal Appl Biol 132(3):507–524
Emerich DW, Ruiz-Argüeso T, Evans HJ (1979) Hydrogen-dependent nitrogenase activity and ATP formation in Rhizobium japonicum bacteroids. J Bacteriol 137(1):153–160
Evans HJ, Harker AR, Papen H, Russell SA, Hanus FJ, Zuber M (1987) Physiology, biochemistry and genetics of the uptake hydrogenase in rhizobia. Annu Rev Microbiol 41:355–361
Faucher C, Maillet F, Vasse J, Rosenberg C, van Brussel AN, Truchet G, Denarie J (1988) Rhizobium meliloti host range nodH determines production of an alfalfa-specific extracellular signal. J Bacteriol 170:5489–5499
Faucher C, Camut S, Denarie J, Truchet G (1989) The nodH and nodQ host range genes of Rhizobium meliloti behave as virulence genes in R. leguminosarum bv. viciae and determine changes in the production of plant-specific extracellular signals. Mol Plant Microbe Interact 2:291–300
Ferguson L, Lessenger JE (2006) Plant growth regulators. In: Lessenger JE (ed) Agricultural medicine. Springer, New York, pp 156–166
Fernández LA, Zalba P, Gómez MA, Sagardoy MA (2007) Phosphate-solubilization activity of bacterial strains in soil and their effect on soybean growth under greenhouse conditions. Biol Fertil Soils 43(6):805–809
Ferreira PAA, Lopes G, Bomfeti CA, de Oliveira Longatti SM, de Sousa Soares CRF, Guilherme LRG, de Souza Moreira FM (2013) Leguminous plants nodulated by selected strains of Cupriavidus necator grow in heavy metal contaminated soils amended with calcium silicate. World J Microbiol Biotechnol 29:2055–2066
Figueiredo MVB, Burity HA, Martínez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by coinoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182–188
Fischer HM (1994) Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58:352–386
Fleury D, Jefferies S, Kuchel H, Langridge P (2010) Genetic and genomic tools to improve drought tolerance in wheat. J Expt Bot 61:3211–3222
Fobert PR, Roy N, Nash JH, Iyer VN (1991) Procedure for obtaining efficient root nodulation of a pea cultivar by a desired Rhizobium strain and preempting nodulation by other strains. Appl Environ Microbiol 57:1590–1594
Fox SL, O’Hara GW, Bräu L (2011) Enhanced nodulation and symbiotic effectiveness of Medicago truncatula when coinoculated with Pseudomonas fluorescens WSM3457 and Ensifer (Sinorhizobium) medicae WSM419. Plant Soil 348:245
Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321(1-2):35–59
Franzini VI, Azcon R, Mendes FL, Aroca R (2013) Different interaction among Glomus and Rhizobium species on Phaseolus vulgaris and Zea mays plant growth, physiology and symbiotic development under moderate drought stress conditions. Plant Growth Regul 70:265–273
Fravel DR (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 28(43):337–359
Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394–401
Frugier F, Kosuta S, Murray JD, Crespi M, Szczyglowski K (2008) Cytokinin: secret agent of symbiosis. Trends Plant Sci 13:115–120
Fujiata K, Ofosu-Budu KG, Ogata S (1992) Biological nitrogen fixation in mixed legume-cereal cropping systems. Plant Soil 141:155–175
Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300
Gal SW, Choi YJ (2003) Isolation and characterization of salt tolerance rhizobia from Acacia root nodules. Agric Chem Biotechnol 46:58–62
Gamas P, Brault M, Jardinaud MF, Frugier F (2017) Cytokinins in symbiotic nodulation: when, where, what for? Trends Plant Sci 22(9):792–802
Garg FC, Garg RP, Kukreja K, Sindhu SS, Tauro P (1985) Host-dependent expression of uptake hydrogenase in cowpea rhizobia. J Gen Microbiol 131(1):93–96
Ghosh PK, Kumar De T, Maiti TK (2015) Production and metabolism of indole acetic acid in root nodules and symbiont (Rhizobium undicola) isolated from root nodule of aquatic medicinal legume Neptunia oleracea Lour. J Bot 2015:1–11
Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G (2007) Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316(5829):1307–1312
Goel AK, Sindhu SS, Dadarwal KR (1999) Bacteriocin producing native rhizobia of green gram (Vigna radiata) having competitive advantage in nodule occupancy. Microbiol Res 154:43–48
Goel AK, Sindhu SS, Dadarwal KR (2000) Pigment diverse mutants of Pseudomonas sp.: Inhibition of fungal growth and stimulation of growth of Cicer arietinum. Biol Plant 43:563–569
Goel AK, Sindhu SS, Dadarwal KR (2002) Stimulation of nodulation and plant growth of chickpea (Cicer arietinum) by Pseudomonas spp. antagonistic to fungal pathogens. Biol Fertil Soils 36:391–396
Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech 5:355–377
Gough C, Vasse J, Galera C, Webster G, Cocking E, Denarie J (1997) Interactions between bacterial diazotrophs and non-legume dicots: Arabdiopsis thaliana as a model plant. Plant Soil 194:123–130
Graham PH (1992) Stress tolerance in Rhizobium and Bradyrhizobium and nodulation under adverse soil conditions. Can J Microbiol 38(6):475–484
Gresshoff PM (2003) Post-genomic insights into plant nodulation symbioses. Genome Biol 4:201. https://doi.org/10.1186/gb-2003-4-1-201
Grimes HD, Mount MS (1984) Influence of Pseudomonas putida on nodulation of Phaseolus vulgaris. Soil Biol Biochem 16:27–30
Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27(5):1231–1240
Guefrachi I, Rejili M, Mahdhi M, Mars M (2013) Assessing genotypic diversity and symbiotic efficiency of five rhizobial legume interactions under cadmium stress for soil phytoremediation. Int J Phytorem 15:938–951
Gully D, Teulet A, Busset N, Nouwen N, Fardoux J, Rouy Z, Vallenet D, Cruveiller S, Giraud E (2017) Complete genome sequence of Bradyrhizobium sp. ORS285, a photosynthetic strain able to establish Nod factor-dependent or Nod factor-independent symbiosis with Aeschynomene legumes. Genome Announc 5(30):e00421–e00417
Gusain YS, Singh US, Sharma AK (2015) Bacterial mediated amelioration of drought stress in drought tolerant and susceptible cultivars of rice (Oryza sativa L.). Afr J Biotechnol 14:764–773
Haggag WM, Abouziena HF, Abd-El-Kreem F, Habbasha S (2015) Agriculture biotechnology for management of multiple biotic and abiotic environmental stress in crops. J Chem Pharm 7(10):882–889
Halverson LJ, Handelsman J (1991) Enhancement of soybean nodulation by Bacillus cereus UW85 in the field and in a growth chamber. Appl Environ Microbiol 57:2767–2770
Hanin M, Jabbouri S, Quesada-Vincens D, Freiberg C, Perret X, Prome JC, Broughten WJ, Fallay R (1997) Sulphation of Rhizobium sp. NGR234 Nod factors is dependent on noeE, a new host specificity gene. Mol Biol 24:1119–1129
Hanin M, Jabbouri S, Broughten WJ, Fallay R, Quesada-Vincens D (1999) Molecular aspects of host specific nodulation. In: Stacey G, Keen NT (eds) Plant microbe interactions, vol 4. APS Press, St. Paul, pp 1–37
Hansen AP, Peoples MB, Gresshoff PM, Atkins CA, Pate JS, Carroll BJ (1989) Symbiotic performance of supernodulating soybean [Glycine max (L.) Merr.] mutants during development on different nitrogen regimes. J Expt Bot 40:715–724
Hansena JC, Schillingerb WF, Sullivanb TS, Paulitzc TC (2018) Rhizosphere microbial communities of canola and wheat at six paired field sites. Appl Soil Ecol. https://doi.org/10.1016/j.apsoil.2018.06.012
Hanus FJ, Albrecht SL, Zablotowicz RM, Emerich DW, Russell SA, Evans HJ (1981) Yield and N content of soybean seed as influenced by Rhizobium japonicum inoculants possessing the uptake hydrogenase characteristics. Agron J 73:368–372
Hara-Nishimura I, Hatsugai N, Nakaune S, Kuroyanagi M, Nishimura M (2005) Vacuolar processing enzyme: an executor of plant cell death. Curr Opin Plant Biol 8:404–408. https://doi.org/10.1016/j.pbi.2005.05.016
Hardarson G (1993) Methods for enhancing symbiotic nitrogen fixation. Plant Soil 152(1):1–7
Hardarson G, Heichel GH, Barnes DK, Vance CP (1982) Rhizobial strain preference of alfalfa populations selected for characteristics associated with N2 fixation. Crop Sci 22:55–58
Hardy RWF, Havelka UD (1975) Nitrogen fixation research: a key to world food? Science 188:633–643
Hegazi NA, Vlassak K, Monib M (1979) Effect of amendments, moisture and temperature on acetylene reduction in Nile Delta soil. Plant Soil 51:27–37
Hemissi I, Mabrouk Y, Mejri S, Saidi M, Sifi B (2013) Enhanced defence responses of chickpea plants against Rhizoctonia solani by pre-inoculation with rhizobia. J Phytopathol 161:412–418
Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311(1–2):1–8
Holl FB, Chanway CP, Turkington R, Radley RA (1988) Response of crested wheatgrass (Agrepyron cristatum L.), perennial ryegrass (Lolium perenne L.) and white clover (Trifolium repens L.) to inoculation with Bacillus polymyxa. Soil Biol Biochem 20:19–24
Hooykaas PJJ, van Brussel AAN, Den Dulk Ras H, van Slogteren GMS, Schilperoort RA (1981) Sym-plasmid of Rhizobium trifolii expressed in different rhizobial species and Agrobacterium tumefaciens. Nature 291:351–353
Hooykaas PJJ, Snijdewint FGM, Schilperoort RA (1982) Identification of the sym plasmid of Rhizobium leguminosarum strain 1001 and its transfer to and expression in other rhizobia and Agrobacterium tumefaciens. Plasmid 8:73–82
Hungaria M, Neves MCP, Dobreiner J (1989) Relative efficiency, ureide transport and harvest index in soybeans inoculated with isogenic Hup- mutants of Bradyrhizobium japonicum. Biol Fertil Soils 7:325–329
Hussain MB, Zahir ZA, Asghar HN (2014a) Can catalase and EPS producing rhizobia ameliorate drought in wheat? Int J Agric Biol 16:3–13
Hussain MB, Zahir ZA, Asghar HN, Mahmood S (2014b) Scrutinizing rhizobia to rescue maize growth under reduced water conditions. Soil Sci Soc Am J. https://doi.org/10.2136/sssaj2013.07.0315
Iqbal MA, Khalid M, Shahzad SM, Ahmad M, Soleman N, Akhtar N (2012) Integrated use of Rhizobium leguminosarum, plant growth promoting rhizobacteria and enriched compost for improving growth, nodulation and yield of lentil (Lens culinaris Medik.). Chil J Agric Res 72:104–110
Iruthayathas EE, Gunasekaran S, Vlassak K (1983) Effect of combined inoculation of Azospirillum and Rhizobium on nodulation and N2-fixation of winged bean and soybean. Scientia Horti 20(3):231–240
Ishizuka J (1992) Trends in biological nitrogen fixation research and application. Plant Soil 141:197–209
Islam MZ, Sattar MA, Ashrafuzzaman M, Berahim Z, Shamsuddoha ATM (2013) Evaluating some salinity tolerant rhizobacterial strains to lentil production under salinity stress. Int J Agric Biol 15:499–504
Itzigsohn R, Kapulnik Y, Okon Y, Dovrat A (1993) Physiological and morphological aspects of interaction between Rhizobium meliloti and alfalfa (Medicago sativa) in association with Azospirillum brasilense. Can J Microbiol 39:610–615
Jabbouri S, Fallay R, Telmont F, Kamalapriya P, Burger U, Relic B, Prome JC, Broughten WJ (1995) Involvement of nodS in N-methylation and nodU in 6-O-carbomylation of Rhizobium sp. NGR234 Nod factors. J Biol Chem 270:22968–22973
Jacobson MR, Premakumar R, Bishop PE (1986) Transcriptional regulation of nitrogen fixation by molybdenum in Azotobacter vinelandii. J Bacteriol 167:480–486
Jensen ES, Hauggaard-Nielsen H (2003) How can increased use of biological N2 fixation in agriculture benefit the environment? Plant Soil 252(1):177–186
Jensen ES, Peoples MB, Boddey RM, Gresshoff PM, Hauggaard-Nielsen H, Alves BJ, Morrison MJ (2012) Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries: a review. Agron Sustain Dev 32:329–364
Jeuffroy MH, Baranger E, Carrouée B, Chezelles ED, Gosme M, Hénault C (2013) Nitrous oxide emissions from crop rotations including wheat, oilseed rape and dry peas. Biogeosciences 10:1787–1797
Joseph B, Patra RR, Lawrence R (2007) Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.). Int J Plant Prod 2:141–152
Jangu OP, Sindhu SS (2011) Differential response of inoculation with acetic acid producing Pseudomonas sp. in green gram (Vigna radiata L.) and blck gram (Vigna mungo L.). Microbiol J 1:159–173
Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GED (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308:1786–1789
Kalra N, Suneja P, Mendiratta N, Gupta N (2013) Simulating the impact of climate change and its variability on growth and yield of crops. Clim Chang Environ Sustain 1(1):11–19
Karaman MR, Sahin S, Düzdemir O, Kandemir N (2013) Selection of chickpea cultivars with agronomic phosphorus (P) utilization characters as influenced by Rhizobium inoculation. Sci Res Essays 8:676–681
Karasu A, Dogan R (2009) The effect of bacterial inoculation and different nitrogen doses on yield and yield components of some chickpea genotypes (Cicer arietinum L.). Afr J Biotechnol 8(1):59–64
Karunakaran R, Ramachandran VK, Seaman JC, East AK, Mouhsine B, Prell J, Skeffington A, Poole PS (2009) Transcriptomic analysis of Rhizobium leguminosarum biovar viciae in symbiosis with host plants Pisum sativum and Vicia cracca. J Bacteriol 191:4002–4014. https://doi.org/10.1128/jb.00165-09
Kassaw T, Jr W, Frugoli J (2015) Multiple autoregulation of nodulation (AON) signals identified through split root analysis of Medicago truncatula sunn and rdn1 mutants. Plants 4(2):209–224
Kennedy IR, Tchan YT (1992) Biological nitrogen fixation in non-leguminous field crops: recent advances. Plant Soil 141:93–118
Kennedy IR, Pereg-Gerk LL, Wood C, Deaker R, Gilcrest K, Katupitia S (1997) Biological nitrogen fixation in non-leguminous field crops: facilitating the evolution of an effective association between Azospirillum and wheat. Plant Soil 194:65–79
Keum YS, Seo JS, Hu YT, Li QX (2006) Degradation pathways of phenanthrene by Sinorhizobium sp. C4. Appl Microbiol Biotechnol 71:935–941. https://doi.org/10.1007/s00253-005-0219-z
Khan MS, Zaidi A, Aamil M (2002) Biocontrol of fungal pathogens by the use of plant growth promoting rhizobacteria and nitrogen fixing microorganisms. Ind J Bot Soc 81:255–263
Khanna V, Sharma P (2011) Potential for enhancing lentil (Lens culinaris) productivity by co-inoculation with PSB, plant growth-promoting rhizobacteria and Rhizobium. Indian J Agric Sci 81(10):932–937
Khot GG, Tauro P, Dadarwal KR (1996) Rhizobacteria from chickpea (Cicer arietinum L.) rhizosphere effective in wilt control and promote nodulation. Ind J Microbiol 36:217–222
Kijne JW, Smith G, Diaz CL, Lugtenberg BJJ (1988) Lectin-enhanced accumulation of manganese-limited Rhizobium leguminosarum cells on pea root hair tips. J Bacteriol 170:2994–3000
Kim YC, Glick BR, Bashan Y, Ryu CM (2012) Enhancement of plant drought tolerance by microbes. In: Aroca R (ed) Springer, pp 383–413
Kinkle BK, Sadowsky MJ, Schmidt EL, Koskinen WC (1993) Plasmids pJP4 and R68.45 can be transferred between populations of bradyrhizobia in nonsterile soil. Appl Environ Microbiol 59:1762–1766
Knight TJ, Langston-Unkefer PJ (1988) Enhancement of symbiotic dinitrogen fixation by a toxin-releasing plant pathogen. Science 241:951–954
Kondorosi A, Vincze E, Johnston AWB, Beringer JE (1980) A comparison of three Rhizobium linkage maps. Mol Gen Genet 178:403–408
Kondorosi A, Kondorosi E, Pankhurst CE, Broughton WJ, Banfalvi Z (1982) Mobilization of Rhizobium meliloti megaplasmid carrying nodulation and nitrogen fixation genes in other rhizobia and Agrobacterium. Mol Gen Genet 188:433–439
Krishnan HB, Lewin A, Fallay R, Broughten WJ, Pueppke SG (1992) Differential expression of nodS accounts for the varied abilities of Rhizobium fredii USDA257 and Rhizobium sp. NGR234 to nodulate Leucaena spp. Mol Biol 6:3321–3330
Krishnan HB, Kim KY, Krishnan AH (1999) Expression of a Serratia marcescens chitinase gene in Sinorhizobium fredii USDA191 and Sinorhizobium meliloti RCR2011 impedes soybean and alfalfa nodulation. Mol Plant Microbe Interact 12:748–751
Kucey RM, Hynes MF (1989) Populations of Rhizobium leguminosarum biovars phaseoli and viceae in fields after bean or pea in rotation with nonlegumes. Can J Microbiol 35(6):661–667
Kulkarni S, Nautiyal CS (2000) Effects of salt and pH stress on temperature-tolerant Rhizobium sp. NBRI330 nodulating Prosopis juliflora. Curr Microbiol 40:221–226
Kumar G, Ram MR (2014) Phosphate solubilizing rhizobia isolated from Vigna trilobata. Am J Microbiol Res 2:105–109
Lahrouni M, Oufdou K, El Khalloufi F, Baz M, Lafuente A, Dary M, Pajuelo E, Oudra B (2013) Physiological and biochemical defense reactions of Vicia faba L.–Rhizobium symbiosis face to chronic exposure to cyanobacterial bloom extract containing microcystins. Environ Sci Pollut Res 20:5405–5415
Larrainzar E, Riely B, Kim SC, Carrasquilla-Garcia N, Yu HJ, Hwang HJ, Oh M, Kim GB, Surendrarao A, Chasman D, Siahpirani AF, Penmetsa RV, Lee GS, Kim N, Roy S, Mun JH, Cook DR (2015) Deep sequencing of the Medicago truncatula root transcriptome reveals a massive and early interaction between Nod factor and ethylene signals. Plant Physiol 169(1):233–265. https://doi.org/10.1104/pp.15.00350
Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, Denarie J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784
Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364
Lewin A, Cervantes E, Wong CH, Broughton WJ (1990) nodSU, two new nod genes of the broad host-range Rhizobium strain NGR234 encode host specific nodulation of the tropical tree Leucaena leucocephala. Mol Plant Microbe Interact 3:317–326
Li DM, Alexander M (1988) Coinoculation with antibiotic-producing bacteria to increase colonization and nodulation by rhizobia. Plant Soil 108:211–219
Li Y, Zhou L, Chen D, Tan X, Lei L, Zhou J (2008) A nodule-specific plant cysteine proteinase, AsNODF32, is involved in nodule senescence and nitrogen fixation activity of the green manure legume Astragalus sinicus. New Phytol 180:185–192. https://doi.org/10.1111/j.1469-8137.2008.02562.x
Lievens S, Goormachtig S, Den Herder J, Capoen W, Mathis R, Hedden P, Holsters M (2005) Gibberellins are involved in nodulation of Sesbania rostrata. Plant Physiol 139:1366–1379
Lim JH, Kim SD (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J 29:201–208
Lindström K, Kokko-Gonzales P, Terefework Z, Räsänen LA (2006) Differentiation of nitrogen-fixing legume root nodule bacteria (rhizobia). Molecular approaches soil, rhizosphere and plant microorganism analysis, p 236
Liu L, Kloepper JW, Tuzun S (1995a) Induction of systemic resistance in cucumber against bacterial angular leaf spot by plant growth-promoting rhizobacteria. Phytopathology 85(8):843–847
Liu L, Kloepper JW, Tuzun S (1995b) Induction of systemic resistance in cucumber against Fusarium wilt by plant growth-promoting rhizobacteria. Phytopathology 85(6):695–698
Loh J, Stacey G (2003) Nodulation gene regulation in Bradyrhizobium japonicum: a unique integration of global regulatory circuits. Appl Environ Microbiol 69:10–17
Long SR (1989) Rhizobium genetics. Annu Rev Genet 23:483–506
Long SR (1996) Rhizobium symbiosis: nod factors in perspective. Plant Cell 8:1885–1898
Loper J, Schroth M (1986) Influence of bacteria sources of indol-3-acetic acid on root elongation of sugar beet. Phytopathol 76:386–389
Lopez-Lara IM, Blok-Tip L, Quinto C, Garcia ML, Bloemberg GV, Lamers GEM, Kafetzopoulos D, Stacey G, Lugtenberg BJJ, Thomas-Oates JE, Spaink HP (1996) nodZ of Bradyrhizobium extends the nodulation host range of Rhizobium by adding a fucosyl residue to nodulation factors. Mol Microbiol 21:397–408
Lu YL, Chen WF, Wang ET, Guan SH, Yan XR, Chen WX (2009) Genetic diversity and biogeography of rhizobia associated with Caragana species in three ecological regions of China. Syst Appl Microbiol 32(5):351–361
Lynch JM (1983) Microorganisms and enzymes in the soil. In: Marumoto T, Watanabe I, Satoh K, Kanazawa S (eds) Soil biotechnology, microbiological factors in crop productivity. Blackwell Science Publications, London, p 185
Machado RG, de Sá EL, Bruxel M, Giongo A, da Silva Santos N, Nunes AS (2013) Indole acetic acid producing rhizobia promote growth of Tanzania grass (Panicum maximum) and Pensacola grass (Paspalum saurae). Int J Agric Biol 15:827–834
Martinez E, Palacios R, Sanchez F (1987) Nitrogen-fixing nodules induced by Agrobacterium tumefaciens harboring Rhizobium phaseoli plasmids. J Bacteriol 169:2828–2834
Mateos PF, Baker DL, Philip-Hollingsworth S, Sqartini A, Peruffo ADB, Nuti MP, Dazzo F (1995) Direct in situ identification of cellulose microfibrils associated with Rhizobium leguminosarum biovar trifolii attached to the root epidermis of white clover. Can J Microbiol 41:202–207
Mathews A, Carroll BJ (2018) Nitrate inhibition of nodulation in legumes. In: Molecular biology of symbiotic nitrogen fixation. CRC Press, Boca Raton, pp 159–180
Mavingui P, Flores M, Romero D, Martinez-Romero E, Palacios R (1997) Generation of Rhizobium strains with improved symbiotic properties by random DNA amplification (RDA). Nat Biotechnol 15:564–569
Mayak S, Tirosh T, Glick BR (2004a) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572
Mayak S, Tirosh T, Glick BR (2004b) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530
McIver J, Djordjevic MA, Weinman JJ, Bender GL, Rolfe BG (1989) Extension of host range of Rhizobium leguminosarum bv. trifolii caused by point mutations in nodD that result in alterations in regulatory function and recognition of inducer molecules. Mol Plant Microbe Interact 2:97–106
Mendoza A, Leija A, Martinez-Romero E, Hernandez G, Mora J (1995) The enhancement of ammonium assimilation in Rhizobium elti prevents nodulation of Phaseolus vulgaris. Mol Plant Microbe Interact 8:584–592
Mendoza A, Valderrama B, Leija A, Mora J (1998) NifA-dependent expression of glutamate dehydrogenase in Rhizobium etli modifies nitrogen partitioning during symbiosis. Mol Plant Microbe Interact 11:83–90
Menna P, Hungria M, Barcellos FG, Bangel EV, Hess PN, Martínez-Romero E (2006) Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Syst Appl Microbiol 29(4):315–332
Merberg D, Maier RJ (1983) Mutants of Rhizobium japonicum with increased hydrogenase activity. Science 220:1064–1065
Mfilinge A, Mtei K, Ndakidemi P (2014) Effect of Rhizobium inoculation and supplementation with phosphorus and potassium on growth and total leaf chlorophyll (Chl) content of bush bean Phaseolus vulgaris, L. Agri Sci 5:1413–1419
Mhadhbi H, Jebara M, Limam F, Aouani ME (2004) Rhizobial strain involvement in plant growth, nodule protein composition and antioxidant enzyme activities of chickpea–rhizobia symbioses: modulation by salt stress. Plant Physiol Biochem 42:717–722
Miller RH, May S (1991) Legume inoculation: successes and failures. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer, Dordrecht, pp 123–134
Miller-Williams M, Loewen PC, Oresnik IJ (2006) Isolation of salt-sensitive mutants of Sinorhizobium meliloti strain Rm1021. Microbiology 152(7):2049–2059
Miransari M, Smith D (2009) Rhizobial lipo-chitooligosaccharides and gibberellins enhance barley (Hordeum vulgare L.) seed germination. Biotechnology 8:270–275
Mishra NS, Tuteja R, Tuteja N (2006) Signaling through MAP kinase networks in plants. Arch Biochem Biophys 452(1):55–68
Mishra PK, Mishra S, Selvakumar G, Bisht JK, Kundu S, Gupta HS (2009) Coinoculation of Bacillus thuringiensis-KR1 with Rhizobium leguminosarum enhances plant growth and nodulation of pea (Pisum sativum L.) and lentil (Lens culinaris L.). World J Microbiol Biotechnol 25:753–761
Mishra PK, Bisht SC, Ruwari P, Joshi GK, Singh G, Bisht JK, Bhatt JC (2011) Bioassociative effect of cold tolerant Pseudomonas spp. and Rhizobium leguminosarum PR1 on iron acquisition, nutrient uptake and growth of lentil (Lens culinaris L.). Eur J Soil Biol 47:35–43
Miwa H, Sun J, Oldroyd GED, Allan Downie J (2006) Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 48:883–894
Mondal HK, Mehta S, Kaur H, Gera R (2017) Characterization of stress tolerant mungbean rhizobia as PGPR and plant growth promotion under abiotic stress. Indian J Microbiol 44(4):38–42
Morel MA, Braña V, Castro-Sowinski S (2012) Legume crops, importance and use of bacterial inoculation to increase production. InCrop Plant 2012. InTech
Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D’Haeseleer K, Holsters M, Goormachtig S (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153:222–237
Mortier V, De Wever E, Vuylsteke M, Holsters M, Goormachtig S (2012) Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. Plant J 70:367–376
Mytton LR, Brockwell J, Gibson AH (1984) The potential for breeding an improved legume-Rhizobium symbiosis: assessment of genetic variation. Euphytica 33:401–410
Malik DK, Sindhu SS (2008) Transposon derived mutants of Pseudomonas strains altered in indole acetic acid production: effect on nodulation and plant growth in green gram (Vigna radiata). Physiol Mol Biol Plants 14:315–320
Nambiar PT, Ma SW, Iyer VN (1990) Limiting an insect infestation of nitrogen-fixing root nodules of the pigeon pea (Cajanus cajan) by engineering the expression of an entomocidal gene in its root nodules. Appl Environ Microbiol 56(9):2866–2869
Nedumaran S, Abinaya P, Jyosthnaa P, Shraavya B, Rao P, Bantilan C (2015) Grain legumes production, consumption and trade trends in developing countries. ICRISAT Res Progr Mark Inst Polic Work Pap Ser 60:4–7
Newbould P (1989) The use of nitrogen fertilizer in agriculture: where do we go practically and ecologically? Plant Soil 115:297–311
Nieuwkoop AJ, Banfalvi Z, Deshmane N, Gerhold D, Schell MG, Sirotkin KM, Stacey G (1987) A locus encoding host range is linked to the common nodulation genes of Bradyrhizobium japonicum. J Bacteriol 169:2631–2638
Nishijima F, Evans WR, Vesper SJ (1988) Enhanced nodulation of soybean by Bradyrhizobium in the presence of Pseudomonas fluorescens. Plant Soil 111:149–150
Norel F, Elmerich C (1987) Nucleotide sequence and functional analysis of the two nifH copies of Rhizobium ORS571. J Gen Microbiol 133:1563–1576
Nutman PS (1984) Improving nitrogen fixation in legumes by plant breeding: The relevance of host selection experiments in red clover (Trifolium pretense L.) and subterraneum clover (T. subterraneum L.). Plant Soil 82:285–301
Nyoki D, Ndakidemi PA (2014) Effects of phosphorus and Bradyrhizobium japonicum on growth and chlorophyll content of cowpea (Vigna unguiculata (L) Walp). Am J Exp Agric 4:1120–1136
O’Connell KP, Goodman RM, Handelsman J (1996) Engineering the rhizosphere: a expressing a bias. Trends Biotechnol 14:83–86
Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546
Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Rev Microbiol 11(4):252
Osborn AM (2006) Horizontal gene transfer and its role in the emergence of new phenotypes. In: Logan NA, Lappin-Scott HM, Oyston PCF (eds) SGM sumposium 66: procaryotic diversity, mechanisms and significance. Cambridge University Press, Cambridge, pp 275–292
Oufdou K, Benidire L, Lyubenova L, Daoui K, Fatemi ZEA, Schröder P (2014) Enzymes of the glutathioneascorbate cycle in leaves and roots of rhizobia inoculated faba bean plants (Vicia faba L.) under salinity stress. Eur J Soil Biol 60:98–103
Papworth A, Maslin M, Randalls S (2015) Is climate change the greatest threat to global health? Geogr J 181:413–422
Parke D, Rivelli M, Ornston LN (1985) Chemotaxis to aromatic and hydroaromatic acids: comparison of Bradyrhizobium japonicum and Rhizobium trifolii. J Bacteriol 163:417–422
Passatore L, Rossetti S, Juwarkar AA, Massacci A (2014) Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): state of knowledge and research perspectives. J Hazard Mater 278:189–202. https://doi.org/10.1016/j.jhazmat.2014.05.051
Patriarca EJ, Tate R, Ioccarino M (2002) Key role of NH4 + metabolism in Rhizobium-plant symbiosis. Microbiol Mol Biol Rev 66:203–222. https://doi.org/10.1128/mmbr.66.2.203-222.2002
Pau AS (1991) Improvement of Rhizobium inoculants by mutation, genetic engineering and formulation. Biotechnol Adv 9:173–184
Peoples MB, Herridge DF (1990) Nitrogen fixation by legumes in tropical and subtropical agriculture. In: Advances in agronomy, vol 44. Academic, San Diego, pp 155–223
Peoples MB, Boyer EW, Goulding KW, Heffer P, Ochwoh VA, van Lauwe B, Wood S, Yagi K, van Cleemput O (2004) Pathways of nitrogen loss and their impacts on human health and the environment. Agriculture and the nitrogen cycle: assessing the impacts of fertilizer use on food production and the environment. Mosier AR, Sayers JR, Freney JR. SCOPE 65. Island Press, Washington, DC, 53–69
Peoples MB, Brockwell J, Herridge DF, Rochester IJ, Alves BJ, Urquiaga S, Boddey RM, Dakora FD, Bhattarai S, Maskey SL, Sampet C (2009) The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48(1-3):1–7
Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64(1):180–201
Pinto FGS, Hungaria M, Mercante FM (2007) Polyphasic characterization of Brazilian Rhizobium tropici strains effective in fixing N2 with common bean (Phaseolus vulgaris L.). Soil Biol Biochem 39:1851–1864
Pladys D, Dmitrijevic L, Rigaud J (1991) Localization of a protease in protoplast preparations in infected cells of French bean nodules. Plant Physiol 97:1174–1180
Plazinski J, Ridge RW, McKay IA, Djordjevic MA (1994) The nod ABC genes of Rhizobium leguminosarum biovar trifolii confer root-hair curling ability to a diverse range of soil bacteria and the ability to induce novel root swellings on beans. Aus J Plant Physiol 21:311–325
Podile AR (1995) Seed bacterization with Bacillus subtilis AF1 enhances seedling emergence, growth and nodulation of pigeonpea. Indian J Microbiol 35:199–204
Polcyn W, Luciński R (2003) Aerobic and anaerobic nitrate and nitrite reduction in free-living cells of Bradyrhizobium sp. (Lupinus). FEMS Microbiol Lett 226(2):331–337
Poonthrigpun S, Pattaragulwanit K, Paengthai S, Kriangkripipat T, Juntongjin K, Thaniyavarn S, Petsom A, Pinphanichakarn P (2006) Novel intermediates of acenaphthylene degradation by Rhizobium sp. strain CU-A1: evidence for naphthalene-1,8- dicarboxylic acid metabolism. Appl Environ Microbiol 72:6034–6039. https://doi.org/10.1128/AEM.00897-06
Prabha C, Maheshwari DK, Bajpai VK (2013) Diverse role of fast growing rhizobia in growth promotion and enhancement of psoralen content in Psoralea corylifolia L. Pharmacogn Mag 9:S57–S65
Pracht JE, Nickell CD, Harper JE, Bullock DG (1994) Agronomic evaluation of non-nodulating and hypernodulating mutants of soybean. Crop Sci 34:738–740
Prasad R, Kumar M, Varma A (2015) Role of PGPR in soil fertility and plant health. In: Plant-growth-promoting rhizobacteria (PGPR) and medicinal plants. Springer, Cham, pp 247–260
Probanza A, Lucas J, Acero N, Mañero FG (1996) The influence of native rhizobacteria on European alder (Alnus glutinosa (L.) Gaertn.) growth. Plant Soil 182:59–66
Putnoky P, Kondorosi A (1986) Two gene clusters of Rhizobium meliloti code for early essential nodulation functions and a third influences nodulation efficiency. J Bacteriol 167:881–887
Quain MD, Makgopa ME, Márquez-García B, Comadira G, Fernandez-Garcia N, Olmos E, Schnaubelt D, Kunert KJ, Foyer CH (2014) Ectopic phytocystatin expression leads to enhanced drought stress tolerance in soybean (Glycine max) and Arabidopsis thaliana through effects on strigolactone pathways and can also result in improved seed traits. Plant Biotechnol J 12:903–913. https://doi.org/10.1111/pbi.12193
Quain MD, Makgopa ME, Cooper JW, Kunert KJ, Foyer CH (2015) Ectopic phytocystatin expression increases nodule numbers and influences the responses of soybean (Glycine max) to nitrogen deficiency. Phytochemistry 112:179–187. https://doi.org/10.1016/j.phytochem.2014.12.027
Quesada-Vincens D, Fallay R, Nassim T, Viprey V, Burger U, Prome JC, Broughten WJ, Jabbouri S (1997) Rhizobium sp. NGR234 NodZ protein is a fucosyltransferase. J Bacteriol 179:5087–5093
Quinto C, de la Vega H, Flores M, Leemans J, Cevallos MA, Pardo MA, Azpiroz R, de Lourdes GM, Calva E, Palacois R (1985) Nitrogenase reductase: a functional multigene family in Rhizobium phaseoli. Proc Natl Acad Sci U S A 82:1170–1174
Quispel A (1988) Bacteria-plant interactions in symbiotic nitrogen fixation. Physiol Plant 74:783–790. https://doi.org/10.1111/j.1399-3054.1988.tb02052.x
Rahmani H, Saleh-Rastin N, Khavazi K, Asgharzadeh A, Fewer D, Kiani S, Lindstrom K (2009) Selection of thermotolerant bradyrhizobial strains for nodulation of soybean (Glycine max L.) in semi-arid regions of Iran. World J Microbiol Biotechnol 25:591–600
Rajendran G, Sing F, Desai AJ, Archana G (2008) Enhanced growth and nodulation of pigeon pea by coinoculation of Bacillus strains with Rhizobium spp. Bioresour Technol 99:4544–4550
Rajwar A, Sahgal M, Johri BN (2013) Legume-rhizobia symbiosis and interactions in agroecosystems. In: Arora NK (ed) Plant microbe symbiosis-fundamentals and advances. Springer, New Delhi, pp 233–265
Ramankutty N, Mehrabi Z, Waha K, Jarvis L, Kremen C, Herrero M, Rieseberg LH (2018) Trends in global agricultural land use: implications for environmental health and food security. Annu Rev Plant Biol 69:789–815
Rao SSR, Vardhini BV, Sujatha E, Anuradha S (2002) Brassinosteroids–a new class of phytohormones. Curr Sci 82:1239–1245
Raverkar KP, Konde BK (1988) Effect of Rhizobium and Azospirillum lipoferum inoculation on the nodulation, yield and nitrogen uptake of peanut cultivars. Plant Soil 106(2):249–252
Ravikumar R (2012) Growth effects of Rhizobium inoculation in some legume plants. Intern J Curr Sci 1:1–6
Reay DS, Davidson EA, Smith KA, Smith P, Melillo JM, Dentener F, Crutzen PJ (2012) Global agriculture and nitrous oxide emissions. Nat Clim Change 2:410–416
Reckling M, Hecker JM, Bergkvist G, Watson CA, Zander P, Schläfke N, Stoddard FL, Eory V, Topp CF, Maire J, Bachinger J (2016) A cropping system assessment framework–evaluating effects of introducing legumes into crop rotations. Eur J Agron 76:186–197
Rehman N, Ali M, Ahmad MZ, Liang G, Zhao J (2018) Strigolactones promote rhizobia interaction and increase nodulation in soybean (Glycine max). Microbiol Pathol 114:420–430
Reimann S, Hauschild R, Hildebrandt U, Sikora RA (2008) Interrelationships between Rhizobium etli G12 and Glomus intraradices and multitrophic effects in the biological control of the rootknot nematode Meloidogyne incognita on tomato. J Plant Dis Protect 115:108–113
Relic B, Talmont F, Kopcinska J, Golinowsky W, Prome JC, Broughten WJ (1993) Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptillium atropurpureum. Mol Plant Microbe Interact 6:764–774
Relic B, Perret X, Estrada-Garcia J, Kopcinska J, Golinowsky W, Krishnan HB, Pueppke SG, Broughten WJ (1994) Nod-factors of Rhizobium are a key to legume door. Mol Microbiol 13:171–178
Remans R, Croonenborghs A, Torres-Gutierrez R, Michiels J, Vanderleyden J (2007) Effects of plant growth promoting rhizobacteria on nodulation of Phaseolus vulgaris L. are dependent on plant nutrition. Eur J Plant Pathol 119:341–351
Remans R, Ramaekers L, Schalkens S, Hernandez G, Garcia A, Reyes JL, Mendez N, Toskano V, Mulling M, Galvez L, Vanderleyden J (2008) Effect of Rhizobium-Azospirillum coinoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in Cuba. Plant Soil 312:25–37
Roberts IN, Caputo C, Criado MV, Funk C (2012) Senescence-associated proteases in plants. Physiol Plant 145:130–139. https://doi.org/10.1111/j.1399-3054.2012.01574.x
Roche P, Debelle F, Maillet F, Lerouge P, Faucher C, Truchet G, Denarie J, Prome JC (1991) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67:1131–1143
Rochester IJ (2007) Nutrient uptake and export from an Australian cotton field. Nutr Cycl Agroecosyst 77(3):213–223
Rogel MA, Hernandez-Lucas I, Kuykendall D, Balkwill DL, Martinez-Romero E (2001) Nitrogen-fixing nodules with Ensifer adhaerens harboring Rhizobium tropici symbiotic plasmids. Appl Environ Microbiol 67:3264–3268
Rolfe BG, Bender GL (1991) Evolving a Rhizobium for non-legume nodulation. In: Gresshoff PM, Roth LE, Stacey G, Newton WE (eds) Nitrogen fixation: achievements and objectives. Chapman and Hall, New York, pp 779–780
Romdhane SB, Trabelsi M, Aouani ME, de Lajudie P, Mhamdi R (2009) The diversity of rhizobia nodulating chickpea (Cicer arietinum) under water deficiency as a source of more efficient inoculants. Soil Biol Biochem 41:2568–2572
Ronson CW, Bosworth A, Genova M, Gudbrandsen S, Hankinson T, Kwaitowski R, Ratcliffe H, Robie C, Sweeney P, Szeto W, Williams M, Zablotowicz R (1990) Field release of genetically engineered Rhizobium meliloti and Bradyrhizobium japonicum strains. In: Gresshoff PM, Roth LE, Stacey G, Newton WE (eds) Nitrogen fixation: achievements and objectives. Chapman and Hall, New York, pp 397–403
Roth LE, Stacey G (1989a) Bacterium release into host cells of nitrogen-fixing nodules: the symbiosome membrane comes from three sources. Eur J Cell Biol 49:13–23
Roth LE, Stacey G (1989b) Cytoplasmic membrane systems involved in bacterium release into soybean nodule cells as studied with two Bradyrhizobium japonicum mutant strains. Eur J Cell Biol 49:24–32
Russelle MP, Schepers JS, Raun WR (2008) Biological dinitrogen fixation in agriculture. Agronomy 49:281–359
Sabry SRS, Saleh SA, Batchelor CA, Davey MR (1997) In: Xanfu V, Kennedy IR, Tinagwei C (eds) Biological nitrogen fixation, novel association with nonleguminous crops. Qungdao Ocean University Press, China, p 59
Sadowsky MJ, Cregan PB, Gottfert M, Sharma A, Gerhold D, Rodriquez-Quinones F, Keyser HH, Hennecke H, Stacey G (1991) The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans. Proc Natl Acad Sci U S A 88:637–641
Sadowsky MJ, Kosslak RM, Madrzak CJ, Golinska B, Cregan PB (1995) Restriction of nodulation by Bradyrhizobium japonicum is mediated by factors present in the root of Glycine max. Appl Environ Microbiol 61:832–836
Sahasrabudhe MM (2011) Screening of rhizobia for indole acetic acid production. Ann Biol Res 2(4):460–468
Saıdi S, Chebil S, Gtari M, Mhamdi R (2013) Characterization of root-nodule bacteria isolated from Vicia faba and selection of plant growth promoting isolates. World J Microbiol Biotechnol 29:1099–1106
Saikia J, Sarma RK, Dhandia R, Yadav A, Bharali R, Gupta VK, Saikia R (2018) Alleviation of drought stress in pulse crops with ACC deaminase producing rhizobacteria isolated from acidic soil of Northeast India. Sci Rep 8:3560. https://doi.org/10.1038/s41598-018-21921-w
Saini P, Khanna V (2012) Evaluation of native rhizobacteria as promoters of plant growth for increased yield in lentil (Lens culinaris). Rec Res Sci Technol 4(4):5–9
Saini I, Sindhu SS, Dadarwal KR (1996) Uptake hydrogenase, nitrate Respiration, ex planta nitrogenase expression and symbiotic effectivity of Sesbania rhizobia. Indian J Microbiol 36:93–97
Sanjuan J, Olivares J (1989) Implication of nifA in regulation of genes located on a Rhizobium meliloti cryptic plasmid that affect nodulation efficiency. J Bacteriol 171:4154–4161
Sanjuan J, Olivares J (1991a) Multicopy plasmids carrying the Klebsiella pneumoniae nifA gene enhances Rhizobium meliloti nodulation competitiveness on alfalfa. Mol Plant Microbe Interact 4:365–369
Sanjuan J, Olivares J (1991b) NifA-NtrA regulatory system activates transcription of nfe, a gene locus involved in nodulation competitiveness of Rhizobium meliloti. Arch Microbiol 155:543–548
Sassi-Aydi S, Aydi S, Abdelly C (2012) Inoculation with the native Rhizobium gallicum 8a3 improves osmotic stress tolerance in common bean drought-sensitive cultivar. Acta Agric Scand Sect B Soil Plant Sci 62:179–187
Sato T, Yashima H, Ohtake N, Sueyoshi K, Akao S, Ohyama T (1999) Possible involvement of photosynthetic supply in changes of nodule characteristics of hypernodulating soybeans. Soil Sci Plant Nutr 45:187–196
Saur I, Oakes M, Djordjevic MA, Imin N (2011) Crosstalk between the nodulation signaling pathway and the autoregulation of nodulation in Medicago truncatula. New Phytol 190:865–874
Sawada H, Kuykendall LD, Young JM (2003) Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49:155–179
Schlindwein G, Vargas LK, Lisboa BB, Azambuja AC, Granada CE, Gabiatti NC, Prates F, Stumpf R (2008) Influence of rhizobial inoculation on seedling vigor and germination of lettuce. Ciencia Rural 38:658–664
Schmidt JE, Weese DJ, Lau JA (2017) Long-term agricultural management does not alter the evolution of a soybean–Rhizobium mutualism. Ecol Appl 27(8):2487–2496
Schofield PR, Ridge RW, Rolfe BG, Shine J, Watson JM (1984) Host-specific nodulation is encloded on a 14 kb fragment in Rhizobium trifolii. Plant Mol Biol 3:3–11
Schwedock J, Long SR (1992) Rhizobium meliloti genes involved in sulfate activation - The two copies of nod PQ and a new locus, saa. Genetics 132:899–909
Schwenke GD, Herridge DF, Scheer C, Rowlings DW, Haigh BM, McMullen KG (2015) Soil N2O emissions under N2-fixing legumes and N-fertilised canola: a reappraisal of emissions factor calculations. Agric Ecosyst Environ 202:232–242
Selvakumar G, Panneerselvam P, Ganeshamurthy AN (2012) Bacterial mediated alleviation of abiotic stress in crops. In: Bacteria in agrobiology: stress management. Springer, Berlin/Heidelberg, pp 205–224
Senbayram M, Wenthe C, Lingner A, Isselstein J, Steinmann H, Kaya C, Köbke S (2016) Legume-based mixed intercropping systems may lower agricultural born N2O emissions. Energy Sustain Soc 6:2
Sessitsch A, Howieson JG, Perret X, Antoun H (2002) Advances in Rhizobium research. Crit Rev Plant Sci 21:323–378. https://doi.org/10.1080/0735-260291044278
Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean. Lett Appl Microbiol 42:155–159
Shaharoona B, Jamro GM, Zahir ZA, Arshad M, Memon KS (2007) Effectiveness of various Pseudomonas spp. and Burkholderia caryophylli containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum I.). J Microbiol Biotechnol 17(8):1300
Shahzad SM, Khalid A, Arif MS, Riaz M, Ashraf M, Iqbal Z, Yasmeen T (2014) Coinoculation integrated with P-enriched compost improved nodulation and growth of chickpea (Cicer arietinum L.) under irrigated and rainfed farming systems. Biol Fertil Soils 50:1–12
Shantharam S, Mattoo AK (1997) Enhancing biological nitrogen fixation: an appraisal of current and alternative technologies for N input into plants. Plant Soil 194:205–216
Sharma R, Sindhu S, Sindhu SS (2018a) Bioinoculation of mustard (Brassica juncea L.) with beneficial rhizobacteria: a sustainable alternative to improve crop growth. Intern J Curr Microbiol Appl Sci 7(5):1375–1386
Sharma R, Sindhu S, Sindhu SS (2018b) Suppression of Alternaria blight disease and plant growth promotion of mustard (Brassica juncea L.) by antagonistic rhizosphere bacteria. Appl Soil Ecol 129:145–150
Shiri-Janagard M, Raei Y, Gasemi-Golezani K, Aliasgarzard N (2012) Influence of Bradyrhizobium japonicum and phosphate solubilizing bacteria on soybean yield at different levels of nitrogen and phosphorus. Int J Agron Plant Prod 3(11):544–449
Sindhu SS, Dadarwal KR (1986) Ex planta nitorgenase induction and uptake hydrogenase in Rhizobium sp. (cowpea miscellany). Soil Biol Biochem 18(3):291–295
Sindhu SS, Dadarwal KR (1988) Effect of temperature on nitrogenase and hydrogenase activity in cowpea miscellany hosts. Indian J Microbiol 28(3):178–183
Sindhu SS, Dadarwal KR (1992) Symbiotic effectivity of cowpea miscellany Rhizobium mutants having increased hydrogenase activity. Indian J Microbiol 32:411–416
Sindhu SS, Dadarwal KR (1993) Broadening of host range infectivity in cowpea miscellany Rhizobium by protoplast fusion. Indian J Expt Biol 31:521–528
Sindhu SS, Dadarwal KR (1995a) Hydrogen uptake-measurement of photosynthate limitation in nodules of cowpea miscellany hosts. Microbiol Res 150:213–217
Sindhu SS, Dadarwal KR (1995b) Molecular biology of nodule development and nitrogen fixation in Rhizobium-legume symbiosis. In: Srivastava HS, Singh RP (eds) Nitrogen nutrition in higher plants. Associated Publishing Company, New Delhi, pp 57–129
Sindhu SS, Dadarwal KR (2000) Competition for nodulation among rhizobia in legume-Rhizobium symbiosis. Indian J Microbiol 40(4):211–246
Sindhu SS, Dadarwal KR (2001a) Chitinolytic and cellulolytic Pseudomonas sp. antagonistic to fungal pathogens enhances nodulation by Mesorhizobium sp. Cicer in chickpea. Microbiol Res 156(4):353–358
Sindhu SS, Dadarwal KR (2001b) Genetic manipulation of rhizobia to improve nodulation and nitrogen fixation in legumes. In: Yadav AK, Motsara MR, Ray Choudhary S (eds) Recent advances in biofertilizer technology. Society for Promotion and Utilization of Resources and Technology, New Delhi, pp 1–97
Sindhu SS, Dadarwal KR (2001c) Symbiotic effectiveness of spontaneous antibiotic-resistant mutants of Rhizobium sp. Cicer nodulating chickpea (Cicer arietinum). Microbiol Res 155:325–329. http://www.urbanfischer.de/journals/microbiolres
Sindhu SS, Lakshminarayana K (1982) Survival and competitive ability of ammonia excreting and non-ammonia excreting Azotobacter chroococcum strains in sterile soil. Plant Soil 69:79–84
Sindhu SS, Lakshminarayana K, Singh D (1994) Expression of hydrogenase activity in Azotobacter chroococcum and its possible role in crop productivity. Indian J Expt Biol 32:423–426
Sindhu SS, Gupta SK, Dadarwal KR (1999a) Antagonistic effect of Pseudomonas spp. on pathogenic fungi and enhancement of growth of green gram (Vigna radiata). Biol Fertil Soils 29:62–68
Sindhu SS, Mor S, Dadarwal KR (1999b) Cell surface polysaccharides of Rhizobium and nodule development on legume roots: recent advances. In: Gakhar SK, Mishra SN (eds) Recent trends in developmental biology. Himalaya Publishing House, New Delhi, pp 204–240
Sindhu SS, Gupta SK, Suneja S, Dadarwal KR (2002a) Enhancement of green gram nodulation and plant growth by Bacillus species. Biol Plant 45:117–120
Sindhu SS, Suneja S, Goel AK, Parmar N, Dadarwal KR (2002b) Plant growth promoting effects of Pseudomonas sp. on coinoculation with Mesorhizobium sp. Cicer strain under sterile and “wilt sick” soil conditions. Appl Soil Ecol 19:57–64
Sindhu SS, Sharma HR, Dadarwal KR (2003) Competition among Bradyrhizobium strains for nodulation of green gram (Vigna radiata): use of dark-nodule strain. Folia Microbiol 48(1):83–90
Sindhu SS, Parmar P, Phour M (2014) Nutrient cycling: potassium solubilization by microorganisms and improvement of crop growth. In: Geomicrobiol biogeochem. Springer, Berlin/Heidelberg, pp 175–198
Sindhu SS, Sehrawat A, Sharma R, Dahiya A (2016) Biopesticides: use of rhizosphere bacteria for biological control of plant pathogens. Defence Life Sci J 1:135–148
Sindhu SS, Sehrawat A, Sharma R, Dahiya A, Khandelwal A (2017) Belowground microbial crosstalk and rhizosphere Biology. In: Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 695–752
Sindhu SS, Khandelwal A, Phour M, Sehrawat A (2018) Bioherbicidal potential of rhizosphere microorganisms for ecofriendly weed management. In: Role of rhizospheric microbes in soil. Springer, Singapore, pp 331–376
Singh G, Sekhon H, Sharma P (2011) Effect of irrigation and biofertilizer on water use, nodulation, growth and yield of chickpea (Cicer arietinum L.). Arch Agron Soil Sci 57:715–726
Sitrit Y, Barak Z, Kapulnik Y, Oppenheim AB, Chet I (1993) Expression of Serratia marcescens chitinase gene in Rhizobium meliloti during symbiosis on alfalfa roots. Mol Plant Microbe Interact 6:293–298
Sloger C, van Berkum P, Dutta SK (1992) Approaches for enhancing nitrogen fixation in cereal crops. Biological nitrogen fixation associated with rice production. In: Dutta SK, Sloger C (eds), pp 229–234
Smit G, Kijne JW, Lugtenberg BJJ (1987) Involvement of both cellulose fibrils and Ca2+ dependent adhesion in the attachment of Rhizobium leguminosarum to pea root hair tips. J Bacteriol 169:4294–4301
Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791
Smith SR, Giller KE (1992) Effective Rhizobium leguminosarum biovar trifolii present in five soils contaminated with heavy metals from long-term applications of sewage sludge or metal mine spoil. Soil Biol Biochem 24(8):781–788
So RB, Ladha JK, Young JP (1994) Photosynthetic symbionts of Aeschynomene spp. forms a cluster with bradyrhizobia on the basis of fatty acid and rRNA analyses. Int J Syst Evol Microbiol 44(3):392–403
Soedarjo M, Borthakur D (1998) Mimosine, a toxin produced by the tree-legume Leucaena provides a nodulation competition advantage to mimosine-degrading Rhizobium strains. Soil Biol Biochem 30:1605–1613. https://doi.org/10.1016/S0038-0717(97)00180-6
Soedarjo M, Hemscheidt TK, Borthakur D (1995) Mimosine, a toxin present in leguminous trees (Leucaena spp.), induces a mimosine-degrading enzyme activity in some strains of Rhizobium. Appl Environ Microbiol 60:4268–4272
Solano BR, Maicas JB, FJG M (2008) Physiological and molecular mechanisms of plant growth promoting rhizobacteria (PGPR). In: Ahmad I, Pichtel J, Hayat S (eds) Plant-bacteria interactions: Strategies and techniques to promote plant growth. Wiley, Weinheim, pp 41–52
Somasegaran P, Bohlool BB (1990) Single strain versus multistrain inoculation: Effect of soil mineral N availability on rhizobial strain effectiveness and competition for nodulation on chickpea, soybean and dry bean. Plant Soil 170:351–358
Soto MJ, Zorzano A, Mercado-Blanco J, Lepek V, Olivares J, Toro N (1993) Nucleotide sequence and characterization of Rhizobium meliloti nodulation competitiveness genes nfe. J Mol Biol 229:570–579
Sougoufara B, Diem HG, Dommergues YR (1989) Response of field grown Casuarina equisetifolia to inoculation with Frankia strain ORS021001 entraped in alginate beads. Plant Soil 118:133–137
Soussana J-F, Tallec T, Blanfort V (2010) Mitigating the greenhouse gas balance of ruminant production systems through carbon sequestration in grasslands. Animal 4(3):334–350
Souza V, Eguiarte L, Avila G, Cappello R, Gallardo C, Montoya J, Pinero D (1994) Genetic structure of Rhizobium etli biovar phaseoli associated with wild and cultivated bean plants (Phaseolus vulgaris and Phaseolus coccineus) in Morelos. Appl Environ Microbiol 60:1260–1268
Spaink HP (1996) Regulation of plant morphogenesis by lipo-chitinoligosaccharides. Crit Rev Plant Sci 15:559–582
Spaink HP, Okker RJH, Wijffelman CA, Tak T, Roo LG, Pees E, van Brussel AAN, Lugtenberg BJJ (1989) Symbiotic properties of rhizobia containing a flavonoid-independent hybrid nodD product. J Bacteriol 171:4045–4053
Sprent JI, Sprent P (1990) Nitrogen fixing organisms: pure and applied aspects. Chapman & Hall, London
Srinivasan M, Petersen DJ, Holl FB (1997) Nodulation of Phaseolus vulgaris by Rhizobium etli is enhanced in the presence of Bacillus. Can J Microbiol 43:1–8
Stacey G, Luka S, Sanjuan J, Banfalvi Z, Nieuwkoop AJ, Chun JY, Forsberg S, Carlson RW (1994) nodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. J Bacteriol 176:620–633
Stajkovic O, Delic D, Josic D, Kuzmanovic D, Rasulic N, Knezevic-Vukcevic J (2011) Improvement of common bean growth by coinoculation with Rhizobium and plant growth-promoting bacteria. Rom Biotechnol Lett 16:5919–5926
Stevenson FJ (1982) Origin and distribution of nitrogen in soil. In: Stevenson FJ (ed) Nitrogen in agricultural soils, agronomy No. 22. American Society of Agronomy, Madison, pp 1–42
Strange RN, Scott PR (2005) Plant disease: a threat to global food security. Ann Rev Phytopathol 43:1–36
Sturtevant DB, Taller BJ (1989) Cytokinin production by Bradyrhizobium japonicum. Plant Physiol 89:1247–1252
Suárez R, Wong A, Ramírez M, Barraza A, Orozco MC, Cevallos MA, Lara M, Hernández G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant Microbe Interact 21:958–966
Sullivan JT, Patrick HN, Lowther WL, Scott DB, Ronson CW (1995) Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci U S A 92:8985–8989
Suzuki A, Akune M, Kogiso M, Imagama Y, Osuki KI, Uchiumi T, Higashi S, Han SY, Yoshida S, Asami T, Abe M (2004) Control of nodule number by the phytohormone abscisic acid in the roots of two leguminous species. Plant Cell Physiol 45(7):914–922
Sy A, Giraud E, Samba R, Gillis M, Dreyfus B (2001) Nodulation of certain legumes of the genus Crotalaria by the new species Methylobacterium. Can J Microbiol 47(6):503–508
Szeto W, Kwiatkowski R, Cannon FC, Ronson CW (1990) The enhancement of symbiotic nitrogen fixation in Bradyrhizobium japonicum. In: Abstracts of fifth international symposium on the molecular genetics of plant-microbe interactions, Interlaken, Switzerland, p 152
Tairo EV, Ndakidemi PA (2013) Bradyrhizobium japonicum inoculation and phosphorus supplementation on growth and chlorophyll accumulation in soybean (Glycine max L.). Am J Plant Sci 4:2281–2289
Talano MA, Cejas RB, González PS, Agostini E (2013) Arsenic effect on the model crop symbiosis Bradyrhizobium-soybean. Plant Physiol Biochem 63:8–14
Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5:51–58
Tariq M, Hameed S, Yasmeen T, Ali A (2012) Non-rhizobial bacteria for improved nodulation and grain yield of mung bean [Vigna radiata (L.) Wilczek]. Afri J Biotechnol 11(84):15012–15019
Tate RL (1995) Soil microbiology (symbiotic nitrogen fixation). Wiley, New York
Tchan YT, Kennedy IR (1989) Possible nitrogen-fixing root nodules induced in non-legumes. Agric Sci 2:57–59
Tchebotar V, Kang U, Asis C Jr, Akao S (1998) The use of GUS-reporter gene to study the effect of Azospirillum-Rhizobium coinoculation on nodulation of white clover. Biol Fertil Soils 27:349–352
Tejera NA, Soussi M, Lluch C (2006) Physiological and nutritional indicators of tolerance to salinity in chickpea plants growing under symbiotic conditions. Environ Exp Bot 58:17–24
Thies JE, Singleton PW, Bohlool BB (1991) Influence of the size of indigenous rhizobial populations on establishment and symbiotic performance of introduced rhizobia on field-grown legumes. Appl Environ Microbiol 57(1):19–28
Timmers AC, Auriac MC, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126:3617–3628
Tominaga A, Nagata M, Futsuki K, Abe H, Uchiumi T, Abe M, Kucho KI, Hashiguchi M, Akashi R, Hirsch A, Arima S (2010) Effect of abscisic acid on symbiotic nitrogen fixation activity in the root nodules of Lotus japonicus. Plant Signal Behav 5(4):440–443
Trinick MJ, Hadobas PA (1995) Formation of nodular structures on the non-legumes Brassica napus, B. campestris, B. juncea and Arabdiopsis thaliana with Bradyrhizobium and Rhizobium isolated from Parasponia spp. or legumes grown in tropical soils. Plant Soil 172:207–219
Triplett EW (1988) Isolation of genes involved in nodulation competitiveness from Rhizobium leguminosarum bv. trifolii T24. Proc Natl Acad Sci U S A 85:3810–3814
Triplett EW (1990) Construction of a symbiotically effective strain of Rhizobium leguminosarum bv. trifolii with increased nodulation competitiveness. Appl Environ Microbiol 56:98–103
Truchet G, Rosenberg C, Vasse J, Julliot JS, Camut S, Denarie J (1984) Transfer of Rhizobium meliloti sym genes into Agrobacterium tumefaciens: host specific nodulation by a typical infection. J Bacteriol 157:134–142
Tu C, Teng Y, Luo Y, Li X, Sun X, Li Z, Liu W, Christie P (2011) Potential for biodegradation of polychlorinated biphenyls (PCBs) by Sinorhizobium meliloti. J Hazard Mater 186:1438–1444. https://doi.org/10.1016/j.jhazmat.2010.12.008
Turner JT, Backman PA (1991) Factors relating to peanut yield increased following Bacillus subtilis seed treatment. Plant Dis 75:347–353
Uma C, Sivagurunathan P, Sangeetha D (2013) Performance of bradyrhizobial isolates under drought conditions. Int J Curr Microbiol App Sci 2:228–232
Urban JE, Davis L, Brown SJ (1986) Rhizobium trifolii 0403 is capable of growth in the absence of combined nitrogen. Appl Environ Microbiol 52(5):1060–1067
Uribe AL, Winham DM, Wharton CM (2012) Community supported agriculture membership in Arizona. An exploratory study of food and sustainability behaviours. Appetite 59(2):431–436
van Elsas JD, Heijnen CE (1990) Methods for the introduction of bacteria into soil: a review. Biol Fertil Soils 10(2):127–133
van Veen JA, van Overbeek LS, van Elsas JD (1997) Fate and activity of microorganisms introduced into soil. Microbiol Mol Biol Rev 61:121–135
van Wyk SG, Du Plessis M, Cullis C, Kunert KJ, Vorster BJ (2014) Cysteine protease and cystatin expression and activity during soybean nodule development and senescence. BMC Plant Biol 14:294–307. https://doi.org/10.1186/s12870-014-0294-3
van Zeijl A, Op den Camp RH, Deinum EE, Charnikhova T, Franssen H, Op den Camp HJ, Bouwmeester H, Kohlen W, Bisseling T, Geurts R (2015) Rhizobium lipo-chitooligosaccharide signaling triggers accumulation of cytokinins in Medicago truncatula roots. Mol Plant 8:1213–1226
Valverde A, Araceli B, Tiziana F, Rivas R, Encarna R, Claudio V, Emilio R, Manual C, Jose-Mariano C (2006) Differential effects of inoculation with Pseudomonas jessenii PS06 and Mesorhizobium ciceri C-212 strain on the growth and seed yield of chickpea under greenhouse and field conditions. Plant Soil 287:43–50
Vande Velde W, Guerra JC, De Keyser A, De Rycke R, Rombauts S, Maunoury N, Mergaert P, Kondorosi E, Holsters M, Goormachtig S (2006) Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol 141:711–720. https://doi.org/10.1104/pp.106.078691
Vardhini BV, Ram Rao SS (1999) Effect of brassionosteriods on nodulation and nitrogenase activity in groundnut (Arachis hypogaea L.). Plant Growth Regul 28(3):165–167
Vargas LK, Lisboa BB, Schlindwein G, Granada CE, Giongo A, Beneduzi A, Passaglia LMP (2009) Occurrence of plant growth-promoting traits in clover-nodulating rhizobia strains isolated from different soils in Rio Grande do Sul state. R Bras Ci Solo 33:1227–1235
Varin S, Lemauviel-Lavenant S, Bernard-Cliquet J, Diquelou S, Padraic T, Mischaelson-Yeates T (2009) Functional plasticity of Trifolium repens L. in response to sulphur and nitrogen availability. Plant Soil 317:189–200. https://doi.org/10.1007/s11104-008-9800-4
Vasse J, de Billy F, Camut S, Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172:4295–4306
Velázquez E, Martínez-Romero E, Rodríguez-Navarro DM, Trujillo ME, Daza A, Mateos PE, MartínezMolina E, van Berkum P (2001) Characterization of rhizobial isolates of Phaseolus vulgaris by staircase electrophoresis of low-molecular weight RNA. Appl Environ Microbiol 67:1008–1010
Venkateshwaran M, Volkening JD, Sussman MR, Ané JM (2013) Symbiosis and the social network of higher plants. Curr Opin Plant Biol 16(1):118–127
Verma JP, Yadav J, Tiwari KN, Kumar A (2013) Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286
Verma JP, Yadav J, Tiwari KN, Jaiswal DK (2014) Evaluation of plant growth promoting activities of microbial strains and their effect on growth and yield of chickpea (Cicer arietinum L.) in India. Soil Biol Biochem 70:33–37
Vidor C, Miller RH (1980) Relative saprophytic competence of Rhizobium japonicum strains in soils as determined by the quantitative fluorescent antibody (FA) technique. Soil Biol Biochem 12(5):483–487
Vineusa P, Léon-Barrios M, Silva C, Willems A, JabaroLorenzo A, Pérez-Galdona R, Werner D, MartínezRomero E (2005) Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575
Vlassak KM, Vanderleyden J, Franco A (1996) Competition and persistence of Rhizobium tropici and R. etli in tropical soil during successive bean (Phaseolus vulgaris L.) cultures. Biol Fertil Soils 21:61–66
Vriezen JAC, de Bruijn FJ, Nusslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen and temperature. Appl Environ Microbiol 73:3451–3459
Waelkens F, Voets T, Vlassak K, Vanderleyden J, van Rhizn P (1995) The nodS gene of Rhizobium tropici CIAT899 is necessary for nodulation of Phaseolus vulgaris and Leucaena leucocephala. Mol Plant Microbe Interact 8:147–154
Walpola BC, Yoon M-H (2013) Isolation and characterization of phosphate solubilizing bacteria and their coinoculation efficiency on tomato plant growth and phosphorous uptake. Afr J Microbiol Res 7(3):266–275
Wang TL, Wood EA, Brewin NJ (1982) Growth regulators and nodulation in peas. The cytokinin content of a wild type and a Ti plasmid containing strain of R. leguminosarum. Planta 155:350–355
Wang ET, Rogel A, Santos AG, Martínez-Romero J, Cevallos MA, Martínez-Romero E (1999) Rhizobium etli bv mimosae, a novel biovar isolated from Mimosa affinis. Int J Syst Bacteriol 49:1479–1491
Wani PA, Khan MS (2013) Nickel detoxification and plant growth promotion by multi metal resistant plant growth promoting Rhizobium species RL9. Bull Environ Contam Toxicol 91:117–124
Wani SP, Rupela OP, Lee KK (1995) Sustainable agriculture in the semi-arid tropics through biological nitrogen fixation in grain legumes. Plant Soil 174:29–49
Wani PA, Khan MS, Zaidi A (2007a) Coinoculation of nitrogen fixing and phosphate solubilizing bacteria to promote growth, yield and nutrient uptake in chickpea. Acta Agron Hung 55:315–323
Wani PA, Khan MS, Zaidi A (2007b) Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (Vigna) on growth, symbiosis, seed yield and metal uptake by green gram plants. Chemosphere 70:36–45
Wani PA, Khan MS, Zaidi A (2007c) Synergistic effects of the inoculation with nitrogen fixing and phosphate solubilizing rhizobacteria on the performance of field grown chickpea. J Plant Nutr Soil Sci 170:283–287
Wani PA, Khan MS, Zaidi A (2008) Chromium-reducing and plant growth promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163
Webster G, Davey MR, Cocking EC (1995) Parasponia with rhizobia: a neglected non-legume nitrogen-fixing symbiosis. AgBiotech News Info 7:119N–124N
Webster G, Gough C, Vasse J, Batchelor CA, O’Callaghan KJ, Kothari SL, Davey MR (1997) Interactions of rhizobia with rice and wheat. Plant Soil 194:115–122
Werner D (2005) Production and biological nitrogen fixation of tropical legumes. In: Nitrogen fixation in agriculture, forestry, ecology and the environment. Springer, Dordrecht, pp 1–13
Williams MK, Beynon JL, Ronson CW, Cannon FC (1990) In: Abstracts of fifth international symposium on the molecular genetics of plant-microbe interactions. Interlaken, Switzerland, p 152
Wilson KJ, Peoples MB, Jefferson RA (1995) New techniques for studying competition by rhizobia and for assessing nitrogen fixation in the field. Plant Soil 174:241–253
Wittenberg JB, Wittenberg BA, Day DA, Udvardi MK, Appleby CA (1996) Siderophore bound iron in the peribacteroid space of soybean root nodules. Plant Soil 178:161–169
Woomer P, Singleton PW, Bohlool BB (1988) Ecological indicators of native rhizobia in tropical soils. Appl Environ Microbiol 54(5):1112–1116
Xiao TT, Schilderink S, Moling S, Deinum EE, Kondorosi E, Franssen H, Kulikova O, Niebel A, Bisseling T (2014) Fate map of Medicago truncatula root nodules. Development 141:3517–3528
Yadav A, Gaur I, Goel N, Mitra J, Saleem B, Goswami S, Paul PK, Upadhyaya KC (2015) Rhizospheric microbes are excellent plant growth promoters. Indian J Natur Sci 5(30):6584–6595
Yadegari M, Rahmani HA, Noormohammadi G, Ayneband A (2008) Evaluation of bean (Phaseolus vulgaris) seeds inoculation with Rhizobium phaseoli and plant growth promoting rhizobacteria on yield and yield components. Pak J Biol Sci PJBS 11(15):1935–1939
Yamato M, Nakayama Y, Yokoyama T, Ueno O, Akao S (1997) Nodulation of Rhizobium fredii USDA192 containing Rhizobium leguminosarum bv. trifolii ANU843 nod genes on homologous host soybean and heterologous host clover. Soil Sci Plant Nutr 43:51–61
Yang L, Tang R, Zhu J, Liu H, Mueller-Roeber B, Xia H, Zhang H (2008) Enhancement of stress tolerance in transgenic tobacco plants constitutively expressing AtIpk2β, an inositol polyphosphate 6-/3-kinase from Arabidopsis thaliana. Plant Mol Biol 66(4):329–343
Yang S, Tang F, Gao M, Krishnan HB, Zhu H (2010) R gene-controlled host specificity in the legume–rhizobia symbiosis. Proc Natl Acad Sci 107(43):18735–18740
Yasmeen T, Hameed S, Tariq M, Ali S (2012) Significance of arbuscular mycorrhizal and bacterial symbionts in a tripartite association with Vigna radiate. Acta Physiol Plant 34:1519–1528
Young JPW, Johnston AWB (1989) The evolution of specificity in the legume-Rhizobium symbiosis. Trends Ecol Evol 4:341–349
Yu X, Liu X, Zhu TH, Liu GH, Mao C (2012) Coinoculation with phosphate-solubilzing and nitrogen-fixing bacteria on solubilization of rock phosphate and their effect on growth promotion and nutrient uptake by walnut. Euro J Soil Biol 50:112–117
Zafar-ul-Hye M, Ahmad M, Shahzad SM (2013) Synergistic effect of rhizobia and plant growth promoting rhizobacteria on the growth and nodulation of lentil seedlings under axenic conditions. Soil Environ 32:79–86
Zahir ZA, Shah MK, Naveed M, Akhter MJ (2010) Substrate dependent auxin production by Rhizobium phaseoli improves the growth and yield of Vigna radiata L. under salt stress conditions. J Microbiol Biotechnol 20:1288–1294
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63(4):968–989
Zhang XP, Karsisto M, Harper R, Lindstrom K (1991) Diversity of Rhizobium bacteria isolated from the root nodules of leguminous trees. Int J Syst Bacteriol 41:104–113
Zhang F, Dashti N, Hynes RK, Smith DL (1996) Plant growth promoting rhizobacteria and soybean {Glycine max (L.) Merr.} nodulation and nitrogen fixation at suboptimal root zone temperatures. Annals Bot 77:453–459
Zhang YHP, Himmel ME, Mielenz JR (2006) Outlook for cellulase improvement: screening and selection strategies. Biotechnol Adv 24(5):452–481
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Sindhu, S.S., Sharma, R., Sindhu, S., Sehrawat, A. (2019). Soil Fertility Improvement by Symbiotic Rhizobia for Sustainable Agriculture. In: Panpatte, D., Jhala, Y. (eds) Soil Fertility Management for Sustainable Development. Springer, Singapore. https://doi.org/10.1007/978-981-13-5904-0_7
Download citation
DOI: https://doi.org/10.1007/978-981-13-5904-0_7
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-13-5903-3
Online ISBN: 978-981-13-5904-0
eBook Packages: Earth and Environmental ScienceEarth and Environmental Science (R0)