Abstract
Soils around the world are degraded due to inappropriate management practices. There is thus the necessity to find more conservationist agricultural systems. Agroforestry system is an alternative system that helps prevent land degradation while allowing continuing use of land to produce crops and livestock on a sustainable basis. Agroforestry system is a form of sustainable land use that combines trees and shrubs with crops and livestock in ways that increase and diversify farm and forest production while also conserving natural resources. This system enhances organic carbon accumulation in soils by the inclusion of cover crops and permanent vegetation, which is expected to increase the soil microbial biomass. The use of microorganisms aims at improving nutrient availability for plants. Currently, there is an emerging demand to decrease the dependence on chemical fertilizers and achieve sustainable agriculture and agroforestry. Arbuscular mycorrhizal fungi, plant growth-promoting rhizobacteria, and the association of rhizobia with leguminous plants are mutualistic symbioses of high economic importance for increasing agricultural production. The biological nitrogen fixation (BNF) process is an economically attractive and ecologically sound method to reduce external nitrogen input and improve the quality and quantity of internal resources. BNF by associative diazotrophic bacteria is a spontaneous process where soil nitrogen is limited and adequate carbon sources are available. However, the ability of these bacteria to contribute to increased crop yields is only partly a result of BNF. The successful use of legumes is dependent upon appropriate attention to the formation of effective symbioses with root nodule bacteria. An essential component for increasing the use of legumes is the integration of plant breeding and cultivar development, with appropriate research leading to the selection of elite strains of root nodule bacteria. An expansion of the utility of inoculants is also necessary to develop a broad conceptual framework and methodology that is supported by scientific arguments; it is destined to impact assessment of the use of new biological products in agriculture.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Soil microbial biomass . . . . . . . . . . . . . . . . . . . . 2
3. Biological nitrogen fixation . . . . . . . . . . . . . . . . . . . . . 3
3.1. Improving the nodulation and nitrogen fixation ability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.2. The role of arbuscular mycorrhiza fungi in improving nodulation and rhizobial activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
3.3. Inoculation technology: a strategy for sustainable development . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
3.4. Rhizobial biodiversity and its importance for the inoculant industry . . . . . . . . . . . . . . . . . . . . . . . . . 6
4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
1 Introduction
Soil degradation can be attributed to unsuitable land use and inappropriate land management practices. Deforestation of fragile land, overcutting of vegetation, shifting cultivation, overgrazing, repetitive tillage, and unbalanced fertilizer use have resulted in progressive loss of soil quality (Miralles et al. 2009). Therefore, there is a need to develop sustainable agricultural systems that maintain soil biological processes and are less dependent on external inputs (i.e., fertilizers and herbicides) and mechanical cultivation to reduce impacts on the environment and conserve soils (Moonen and Bàrberi 2008). Agroforestry system (AFS) can be considered an alternative system that help prevent land degradation while allowing continuing use of land to produce crops and livestock on a sustainable basis (Cacho 2001; FAO 2005).
AFS is a form of multi-cropping which involves combining at least one woody-perennial species with a crop which results in ecological and economic interactions between the two components (Palma et al. 2007). Such systems are effective at improving and conserving soil quality by continuous deposition of plant biomass and turnover of leaf litter. This provides a continuous stream of organic material to the soil (Nair et al. 2008), especially because of the long roots of the forest component that go deep into the soil (Albrecht and Kandji 2003; Barreto et al. 2010), increasing soil organic matter stocks (Manley et al. 2007; Fontes et al. 2010) and the carbon sequestration potential (Roshetko et al. 2007; Sharrow and Ismail 2004; Kirby and Potvin 2007; Nair et al. 2009).
Biological properties can be also optimized in the soil under AFS (Yan et al., 2000; Udawatta et al. 2008; Yadav, et al. 2010). Several authors have reported that soil microbial biomass and microbial diversity are greater in the AFS due to the ameliorative effects of trees and organic matter inputs and the differences in litter quality and quantity and root exudates (Gomez et al. 2000; Myers et al. 2001; Mungai et al. 2005; Sørensen and Sessitsch 2007). The presence of a large and diverse soil microbial community is crucial to the productivity of any agroecosystem. Moreover, mixtures of plant species in AFS usually allow a larger diversity and/or abundance of mycorrhizal fungi than monocultures (Cardoso and Kuyper 2006) and becomes more efficient the nitrogen biological fixation, especially in tropical soils (Serraj 2004; Freitas et al. 2010).
Although several benefits of agroforestry practices to soil microorganisms are reported in the literature, more research is needed to fill key knowledge gaps for a comprehensive understanding of buffer effects on overall environmental quality (Lowrance et al. 2002; Loveall and Sullivan 2006).
2 Soil microbial biomass
The soil microbial biomass comprises all soil organisms with a volume less than approximately 5 × 103 μm3 (other than plant tissue) and can be considered as the living part of soil organic matter (Brookes 2001). The proportion present as living microbial cells (microbial biomass carbon in milligrams per kilogram of soil) typically comprises 1% to 5% (w/w) of the total organic carbon, and microbial nitrogen accounts for 1% to 6% (w/w) of the total organic nitrogen (Jenkinson and Ladd 1981).
The soil microbial biomass has important functions in the soil, including nutrient cycling and the degradation of pollutants (e.g., pesticides, urban and industrial waste) (Dick 1997; Haney et al. 2003; Watanabe and Hamamura 2003; Araújo et al. 2003; Araújo and Monteiro 2006). According to Powlson et al. (1987), the main function of microorganisms is to mediate soil processes and high rates of turnover, which is a sensitive indicator of changes in the soil organic matter.
The adoption of different management systems can have negative or positive effects on the soil properties. AFS are being increasingly recommended as a sustainable form of land use because they are believed to provide the optimum level of food production, a supply of firewood, and cash benefits, while maintaining soil fertility (Heuvelop et al. 1988). AFS generally enhance organic matter accumulation in soils through the inclusion of different crops and permanent vegetation cover, which would be expected to increase the soil microbial biomass. Additionally, AFS have been recognized as an alternative for the rehabilitation of degraded areas through the use of different tree species with crops. This management strategy improves the biological properties of degraded soils due the high quantity of sources of organic residues (Mendonça et al. 2001). These systems may restore soil biodiversity and other important functions of the soil community (Macdicken and Vergara 1990). Fisher (1995) suggested that trees might improve soil quality in several ways. Many tropical tree species can fix atmospheric nitrogen and may therefore increase the soil nitrogen content. The large root system of trees potentially accumulates nutrients from a large volume of soil, whereas fallen litter concentrates nutrients near the soil surface. Fallen litter and fine-root turnover may increase the soil organic matter concentration. Trees may also enhance the above- and belowground microclimate around plant roots and may alter the soil biological properties. In Kenya, Belsky et al. (1989) found 35% to 60% greater soil microbial biomass under Adansonia digitata and Acacia tortilis crowns than in the open grassland areas, due to a better microclimate for the soil microorganisms. Tangjang et al. (2009) noticed that plant residues, added organic matter, vegetation, plant species composition, and soil mineral nutrients altered the microbial population and their species composition under traditional AFS in Northeast, India. Instead of the effects of growing trees in combination with field crops on soil microbial biomass was evaluated by Chander et al. (1998) in soils under a 12-year-old AFS, and the soil microbial biomass was significantly affected by the AFS. Both the amount of microbial biomass carbon and the enzymatic activities were greater in soils under AFS than in conventional systems. According to the same authors, the greater microbial biomass reflected the response of the increased input of organic matter to the soil under the AFS. Previously, Tornquist et al. (1999) found that the soil microbial biomass carbon and nitrogen were not significantly different in pastures and AFS in Costa Rica. According to the authors, the soils evaluated had a high soil microbial biomass.
Kaur et al. (2000) investigated the effects of the monocropping of rice, forestry, and agroforestry on the soil microbial biomass in India. The authors observed that the soil microbial biomass was increased by 42% (microbial carbon) and 13% (microbial nitrogen) in AFS compared to monocropping. They attributed the higher soil microbial biomass to the high quantity of carbon released by the AFS. Their findings supported a study by Rao and Pathak (1996) that demonstrated an increase in the microbial carbon and nitrogen (10–60% and 17–43%, respectively) in AFS with a large carbon source than in conventional soil with low carbon.
It seems likely that litter quality regulated the level of soil microbial biomass in tree-based systems. The availability of carbonaceous materials and substrates such as sugars, amino acids, and organic acids to the soil from the roots is important for supplying energy for the microbial populations (Bowen and Rovira 1991). The importance of root exudates in maintaining a larger microbial biomass closer to the trees has also been reported by Browaldh (1997).
In a Brazilian ecosystem, Almeida et al. (1997) compared the influence of an AFS with coffee, native vegetation, or a conventional system on the soil microbial biomass. The author observed a decrease in the soil microbial biomass under the conventional system; however, the AFS was similar to the native vegetation. Furthermore, the AFS showed greater potential to cycle nutrients than the conventional system.
3 Biological nitrogen fixation
Biological nitrogen fixation (BNF) is known to occur to various degrees and in different environments, including soils, fresh and salt waters, and sediments; on or within the roots, stems, and leaves of certain higher plants; and within the digestive tracts of some animals. The potential for nitrogen fixation exists for any environment capable of supporting the growth of microorganisms. Biological systems that are capable of fixing nitrogen are historically classified as non-symbiotic or symbiotic, depending on the involvement of one or more organisms, respectively (Hubbell and Kidder 2003).
Over the last few years, studies examining the nodulation of legume tree species and the selection of highly efficient rhizobial strains for legume trees have received more attention. Species with potential use in different agrosystems, efficient nitrogen-fixing rhizobia, have been selected and are available for inoculant production (Faria 1995; Faria and Lima 1998; Chen et al. 2005; Balachandar et al. 2007). New species of rhizobia or bradyrhizobia have been described, and large collections of isolates are being developed. These rhizobia are of economic importance in low-input sustainable agriculture, agroforestry, and land reclamation (Balachandar et al. 2007).
Until recently, it has been generally accepted that legumes (and the non-legume genus Parasponia) are nodulated exclusively by members of the family Rhizobiaceae in the α-proteobacteria, which includes the genera Azorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium, and Sinorhizobium (Sprent 2001). Over the last few years, however, several other species of α-proteobacteria have been shown to nodulate legumes (Moulin et al. 2002). These include strains of Methylobacterium that nodulate Crotalaria and Lotononis (Jaftha et al. 2002; Sy et al. 2001a and b); Blastobacter denitrificans, which nodulates Aeschynomene indica (van Berkum and Eardly 2002); and Devosia strains that nodulate Neptunia natans (Rivas et al. 2002). More controversially, a few members of the β-proteobacteria, such as Burkholderia spp. (originally isolated from Aspalathus carnosa and Machaerium lunatum, Moulin et al. 2001) and Ralstonia taiwanensis (isolated from Mimosa pudica; Chen et al. 2001) have been discovered in nodules of tropical legumes. The terms α- and β-rhizobia have been proposed to distinguish the rhizobial α- and β-proteobacteria (Moulin et al. 2001). Phylogenetic analysis of the available nodA and nifH genes from α- and β-proteobacteria suggests that β-rhizobia evolved from diazotrophs through multiple lateral gene transfers (Chen et al. 2003).
All α-rhizobial genera belong to the Rhizobiales order, whereas β-rhizobial genera belong to the Burkholderiales order. A same genus or even species often contains both rhizobial and nonrhizobial strains, each Rhizobium has a defined host spectrum, but there is no strict correlation between legume and bacterium taxonomy, although some associations are favored (e.g., Azorhizobium—Sesbania and Burkholderia—Mimosa) (Masson-Boivin et al. 2009).
The taxonomic classification of rhizobia strains has undergone a transformation since 2001, with the reclassification of some species to the β-proteobacteria suborder, especially Burkholderia species (Moulin et al. 2001). Burkholderia species are effective symbionts of several plants species (Barrett and Parke 2005, 2006; Chen et al. 2005; Chen et al. 2003). Although some are important pathogens for humans and animals (e.g., Burkholderia cepacia, Burkholderia pseudomallei, and Burkholderia mallei), studies show that the symbiont species are phylogenetically distant of these (Bontemps et al. 2009).
According to Moulin et al. (2001), the characterization of the symbionts of the yet unexplored legumes may reveal the rhizobial nature of additional members of the beta-proteobacteria and possibly other taxonomic classes. Such a study may contribute significantly to the understanding of the origin, and the evolution of, the legume–rhizobia symbioses, and may open new perspectives for engineering beneficial associations.
Besides, a number of isolates have been reported from legume nodules, capable of nitrogen fixation but phylogenetically located outside the traditional groups of rhizobia in the alpha-proteobacteria. New lines that contain nitrogen-fixing legume symbionts include Methylobacterium, Devosia, Ochrobactrum, and Phyllobacterium in the alpha-proteobacteria and Burkholderia, Ralstonia, and Cupriavidus in the beta-proteobacteria. All these new nodulating bacteria are phylogenetically (16S rDNA) distinct from the rhizobia, but do carry nod genes similar to those of rhizobia. These genes encode for Nod factors, signal molecules in the bacterium–legume communication that accompanies nodulation (Willems 2006).
Recently, the presence of γ-proteobacteria of the genera Pseudomonas, Pantoea, Enterobacter, and Escherichia was described in the nodules of Hedysarum spp. (Benhizia et al. 2004; Muresu et al. 2008), suggesting potential synergistic interactions among various species and the existence of other unidentified mechanisms. Another species belonging to the Cohnella phaseoli suborder of γ-proteobacteria was recently isolated from the nodules of Phaseolus in Spain. However, this species was not detected in nodules from three species of this genus, and no reported Nod genes have been identified in this bacteria (García-Fraile et al. 2008).
Among the new genera capable of nodulating leguminous species, the association between plants of the genus Mimosa and bacteria should be emphasized. Burkholderia spp. is more competitive when co-inoculated with strains of Rhizobium tropici and Rhizobium etli (Elliott et al. 2009). Another interesting point is the inability of Mimosa spp. to form nodules when inoculated with Rhizobium sp. strain NGR234, which has a broad spectrum of hosts (over 250 plants including Parasponia sp.) (Pueppke and Broughton 1999).
Studies using native plant species in tropical regions have been conducted, and new rhizobia species have been described (Martinez-Romero et al. 1991; Vandamme et al. 2002; Chen et al. 2008), suggesting wide diversity for this bacteria group. The selection of partners (macro and microsymbionts) based on symbiotic specificity and the identification of those with greater efficiency is part of the strategy to optimize the BNF, especially given that nodulation in legumes does not occur equally among the three subfamilies. Hirsch et al. (2001) estimated that less than 25% of Caesalpinoidae are able to nodulate, whereas over 90% of the Mimosoidae and Papilionoidae subfamilies are capable of nodulation.
3.1 Improving the nodulation and nitrogen fixation ability
Microbial interactions, which are regulated by specific molecules/signals, are responsible for key environmental processes, such as the biogeochemical cycling of nutrients and matter and the maintenance of plant health and soil quality (Barea et al. 2004). Plant growth-promoting rhizobacteria (PGPR), in combination with efficient rhizobia, could improve growth and nitrogen fixation by inducing the occupancy of the introduced rhizobia in the nodules of the legume (Tilak et al. 2006). Some PGPR can improve nodulation and nitrogen fixation in legume plants (Zhang et al. 1996; Andrade et al. 1998; Lucas-Garcia et al. 2004). Studies carried out under field conditions (Bai et al. 2003), particularly those using 15N-based techniques (Dashti et al. 1998), have highlighted these beneficial co-operative effects between microbes. Research on the mechanisms by which PGPR enhance nodule formation has implicated their production of plant hormones in the co-inoculation benefits. For example, Chebotar et al. (2001) demonstrated that some Pseudomonas strains, but not all, increased the number of nodules and lowered the acetylene activity in soybean plants inoculated with Bradyrhizobium japonicum. Silva et al. (2006) verified that some Bacillus strains with effective Rhizobia resulted in enhanced nodulation in cowpeas (Vigna unguiculata L.), soybeans (Glycine max L.) (Araújo and Hungria 1999), and beans (Phaseolus vulgaris L.) (Figueiredo et al. 2008). Furthermore, Vessey and Buss (2002) demonstrated that the application of Bacillus species to seeds or roots caused variation in the composition of the rhizosphere, which resulted in increased growth and yield of different crops.
According to Saravana-Kumar and Samiyappan (2007), Bradyrhizobium prompted the nodulation and growth of legumes in combination with active 1-aminocyclopropane-1-carboxylate (ACC) deaminase-expressing PGPR. Moreover, certain rhizobacteria also possess the enzyme ACC deaminase, which hydrolyses ACC into ammonia and α-ketobutyrate (Mayak et al. 1999). ACC deaminase activity in PGPR plays an important role in the host nodulation response (Remans et al. 2007). PGPR expressing ACC deaminase could suppress accelerated endogenous ethylene synthesis and, therefore, may facilitate root elongation and nodulation, which in turn could improve the growth and yield of the plants (Zafar-ul-Hye 2008). In addition, the gene for ACC deaminase has also been found in some rhizobia, including Mesorhizobium loti, B. japonicum, and Rhizobium sp. ACC deaminase also facilitates symbiosis by decreasing the ethylene levels in the roots of the host (Okasaki et al. 2007).
Endophytes can also produce ACC deaminase. Whereas this enzyme has no function in bacteria, it cleaves ACC, the precursor of ethylene in plants, and therefore modulates the ethylene levels that promote plant growth (Sziderics et al. 2007; Sun et al. 2009). Plant growth is also promoted by the production of phytohormones, such as auxins, cytokinins, and gibberellins (Steenhoudt and Vanderleyden 2000). The most related phytohormone produced by endophytic bacteria is the auxin indole-3-acetic acid, which is produced by Gluconoacetobacter, Azospirillum, Herbaspirillum, Methylobacterium, Erwinia, Pantoea, and Pseudomonas (Kuklinsky-Sobral et al. 2004).
3.2 The role of arbuscular mycorrhiza fungi in improving nodulation and rhizobial activity
The widespread presence of symbiotic arbuscular mycorrhiza (AM) fungi in nodulated legumes and the role of AM fungi in improving nodulation and rhizobial activity within the nodules are both universally recognized processes (Barea et al. 2005). AM fungi and rhizobia are two of the most important plant symbionts; they play a key role in natural ecosystems and influence plant productivity, plant nutrition, and plant disease resistance (Demir and Akkopru 2007). Mycorrhizas benefit the host through the mobilization of phosphorus from non-labile sources, whereas Rhizobium fixes nitrogen (Scheublin and Van der Heijden 2006). The interactions between AM fungi and bacteria suggest a beneficial effect of the fungi on bacterial development and vice versa (De Boer et al. 2005). AM colonization has been shown to improve nodulation and nitrogen fixation, and the use of the isotope 15N has made it possible to ascertain and quantify both the amount of nitrogen that is fixed in a particular situation and the contribution of the AM symbiosis to nitrogen fixation (Barea et al. 2002). Studies examining the biochemical and physiological basis of the interactions between AM fungi and rhizobia that improve legume productivity have suggested that the main effect of AM fungi in enhancing rhizobia activity is through the generalized stimulation of host nutrition. However, it should be noted that some localized effects may also occur at the root or nodule level (Barea et al. 1992). Additional experiments have corroborated the positive effect of the interactions between AM fungi and rhizobia under drought conditions (Ruiz-Lozano et al. 2001). For example, inoculation with AM fungi protected soybean plants against the detrimental effects of drought and helped the plants tolerate the premature nodule senescence induced by drought stress (Porcel et al. 2003). Suitable combinations of AM fungi and rhizobia bacteria may increase plant growth and resistance to pathogens (Aysan and Demir 2009) and improve nodulation and nitrogen fixation (Barea et al. 2002).
The bacteria involved in the establishment of mycorrhiza and/or mycorrhiza function were therefore designated mycorrhiza helper bacteria (MHB) by Garbaye (1994) and are currently the most investigated group of bacteria that interact with mycorrhizas (Frey-Klett et al. 2007). The MHB strains that have been identified to date belong to many bacterial groups and genera, such as Gram-negative proteobacteria (Agrobacterium, Azospirillum, Azotobacter, Burkholderia, Bradyrhizobium, Enterobacter, Pseudomonas, Klebsiella, and Rhizobium), Gram-positive firmicutes (Bacillus, Brevibacillus, and Paenibacillus) and Gram-positive actinomycetes (Rhodococcus, Streptomyces, and Arthrobacter) (Frey-Klett et al. 2007). Some species are responsible for multiple helper effects because they influence both plants and the associated mycorrhizal fungi. The stimulating effect of MHB has been evaluated mostly when symbiotic associations are exposed to stresses ranging from drought to contamination with heavy metals (Vivas et al. 2003a, b). A classic example illustrating the helper effect is the rhizobia-producing ACC deaminase, which modulates plant ethylene levels, thereby increasing plant tolerance to environmental stress and stimulating nodulation (Ma et al. 2002). Changes in auxin and cytokinin levels have been implicated in the normal infection and nodulation processes of various species of legumes. However, rhizobial inoculation has been reported to both increase and decrease auxin levels in the roots (Ferguson and Mathesius 2003).
3.3 Inoculation technology: a strategy for sustainable development
The success of inoculation technology is a result of the knowledge accumulated over a century of research. The first inoculants containing Rhizobium were marketed in the United States. Today, the inoculants are marketed in most of the world and are mainly destined for the agribusiness cultures, and it has been estimated that some 2,000 t of rhizobial inoculants are produced worldwide every year (Ben et al. 2007). Nevertheless, its use is still restricted for other species of legumes, such as those of interest in AFS. In Brazil, this scenario does not reflect the potential use of biological resources in a country that has an estimated 15–20% of the planet’s biological diversity (Salati et al. 2006).
However, in addition to the selection of the strain, the inoculation vehicle is also part of the technology. Peat has been used for about a century as the principal support vehicle for inoculation of legumes. A number of practical issues, such as unevenness in the composition and difficulties in obtaining, handling, and the sterilization of peat, suggest new formulations need to be tested, developed, and adequately assessed in the field. Liquid formulations also have limitations, including difficulties in transportation and storage (because they often require refrigeration) and the difficulties in coating and homogeneous mixtures in the seeds. The proper formulation should be biodegradable and easy to handle and is even more critical when mixed inoculants are developed or when the inoculants contain additional plant growth-promoting bacteria (Dobbelaere et al. 2003; Deaker et al. 2004). In order to increase the inoculant quality and efficiency and to reduce costs and environmental impacts, alternative carrier materials have been studied (Ben et al. 2007; Albareda et al. 2008).
In an attempt to improve the inoculant quality in Brazil, different carrier blends, together with diazotrophs, were evaluated at room temperature, and their performance as an inoculant was compared to a peat-based inoculant carrier. Polymer blends functioned as an efficient carrier to rhizobial inoculants and show competitive advantages including biodegradability and being non-toxic and water soluble. These blends enabled the pre-inoculation of the seeds and the maintenance of the rhizobia numbers at room temperature that were comparable to that of traditional peat inoculants (Xavier et al. 2010). This product has been tested in association with Bradyrhizobium and cowpeas (Fernandes Júnior et al. 2009) and the inoculant for cane sugar (Gluconacetobacter diazotrophicus, Herbaspirillum seropedicae, Herbaspirillum rubrisubalbicans, Azospirillum amazonense, and Burkholderia tropica) (Silva et al. 2009).
The use of inoculant strains differs from traditional associations with rhizobia and legumes and is a promising alternative to agriculture. Over the next few years, there will be greater environmental awareness and sustainable use of natural resources, leading to a policy of increased demand for alternative sources of farm inputs and more efficient use of plants. With these conditions, there will be opportunities arising from the increased demand for more efficient plant uptake of nitrogen from the air.
However, quality control standards must be established, and few countries have identity standards and well-defined parameters for the inoculants. Since 2004, Brazil, through the Ministry of Agriculture and Livestock, has had legislation dealing with registration and the patterns and a catalog of authorized inoculants strains.
Expansion of the inoculants’ utility is also necessary to develop a broad conceptual framework and methodology. With regard to scientific arguments, it is destined to impact the assessment of new biological products in agriculture. Extensive discussions, with the participation of competent institutions responsible for the standardization of biosafety issues in the country, should be promoted, especially for the recommendation of new microbial species for use as inoculants.
To increase the efficiency of the product, the application of a mixture of strains with different characteristics to stimulate the synergy between the strains and adaptation to the environment should also be considered. However, these mixtures should be recommended cautiously because of the difficulties involved in the registration and quality control of these products.
Currently, BFN has also taken on a new meaning by the Brazilian government as it is among the four measures (in addition to the recovery of pasture, crop-livestock integration, and no-tillage on straw) to be adopted extensively in agriculture in order to voluntarily reduce greenhouse gas production. Therefore, BFN can also be viewed as a central part of the strategy for the integration of the other proposed actions.
3.4 Rhizobial biodiversity and its importance for the inoculant industry
Bacterial symbionts are extraordinarily diverse for some extremely beneficial traits, such as biological nitrogen fixation efficiency and rate, soil survival, and competitiveness for nodule formation (Brockman and Bezdicek 1989; Anyango et al. 1995; Doyle and Doyle 1998; Handley et al. 1998; Andronov et al. 1999; Caballero-Mellado and Martinez-Romero 1999; Collins et al. 2002; Galli-Terasawa et al. 2003; Fagerli and Svenning 2005; Grange and Hungria 2004; Jesus et al. 2005; Alexandre et al. 2006; Bala and Giller 2006; Duodu et al. 2006; Duodu et al. 2007; Langer et al. 2008; Alexandre et al. 2009).
This diversity is considered one of the most basic foundations of the inoculant industry, as it allows soil microbiology researchers to find, assess, and identify strains with higher nitrogen fixation potential, as well as other useful traits, that would allow a commercial rhizobial inoculant to increase the yield of legumes (Date 2000; Hungria and Vargas 2000; Aguilar et al. 2001; Lesueur et al. 2001; Faria 2002; Faria and Franco 2002; Mostasso et al. 2002; Martins et al. 2003; Howieson and Ballard 2004; Yates et al. 2005a; Yates et al. 2005b; Alberton et al. 2006; Silva et al. 2007).
On the other hand, this potential benefit can only be achieved by continuing research and evaluation of different bacterial strains (Daba and Haile 2000; Catroux et al. 2001), resulting in similarities between the inoculant and plant breeding industries. Both industries may be considered, from a pragmatic point of view, as essentially consisting of finding new genetic resources to achieve higher plant yields than currently possible with the use of the available genetic material.
This constant renewal leads to the development and evaluation of a continually increasing amount of new genetic material to maximize the probability of finding new genetic resources to achieve higher plant yields, be it via greater nutrient use efficiency, water use efficiency, drought tolerance etc., than currently available. It would seem to be a “Red Queen” phenomenon, in which the industry has to run harder to be able to outpace its own past successes. For example, the São Paulo state sugarcane breeding program evaluated 300,000 new progenies in 2001, of which only 17 were deemed desirable for performance testing (Bressiani 2001). On the other hand, most scientific papers detailing strain evaluation cite much lower evaluated strains numbers. Some examples are the selection of strains for red clover (Trifolium pratense) inoculation in northern Scandinavia based on 431 strains (Duodu et al. 2007), high temperature-resistant strains for soybean (G. max) in Iran based on 56 strains (Rhamani et al. 2009), salt-resistant common bean (P. vulgaris) in Tunisia based on 19 strains (Mnasri et al. 2007), and several Mediterranean legume shrubs and trees in Central Spain with an exceedingly narrow basis of only nine strains (Ruiz-Díez et al. 2009).
An approach more similar to that of the plant breeding can be seen on a 1997 paper describing selection of strains for a forage legume under evaluation in Australia, which evaluated 1,200 rhizobial isolates for Stylosanthes sp. Aff. Stylosanthes scabra (Stylosanthes seabrana). Of those strains, 18 were selected for field experimentation in four different areas, resulting in a 10% to 20% yield increase in areas without established compatible populations in the first year, followed by a 400% gain in the second year compared to the un-inoculated control (Date 1997).
Evaluated strain numbers may be underestimated in the scientific literature in comparison to works of a more technical nature, such as research reports or pamphlets such as those from EMBRAPA describing strain selection for Brazilian legume tree species (Faria et al. 1984; Faria 1997; 2000; 2002). Unfortunately, this kind of information is usually not available to research papers, basically for space limitations and the inability to include the entire bacteria collection with all of the relevant details.
While inoculant production, as well as crop breeding, centers on economically important legumes, biodiversity research efforts have focused on several legume species with limited economical importance today, but which show potentially important uses for reforestation, improved fallows, or AFS (Chikowo et al. 2006; Makatiani and Odee 2007; Manassila et al. 2007; Ceccon 2008; Chesney 2008; Daudin and Sierra 2008; Bashan et al. 2009; Jalonen et al. 2009; Nygren and Leblanc 2009; Freitas et al. 2010). For example, work has been conducted for several Mimosa species in Brazil (Bontemps et al. 2009), for Prosopis species in Morocco (Benata et al. 2008), and for several genera in Africa (Doignon-Bourcier et al. 1999; Bala et al. 2002; Odee et al. 2002; Bala et al. 2003a; Bala et al. 2003b; Wolde-meskel et al. 2004; Diabate et al. 2005; Diouf et al. 2007; Law et al. 2007).
4 Conclusion
AFS promote the permanent input of litter to increase the organic matter content of the soil and positively influence the soil microbial community by providing a large source of carbon and energy. The improvements in the soil microorganism status are important because microorganisms provide many functions in a soil ecosystem, including organic matter decomposition, nitrogen fixation, uptake of phosphorus by mycorrhiza, and the promotion of plant growth. The soil microbial populations are immersed in a framework of interactions known to affect plant fitness and soil quality. They are involved in fundamental activities that ensure the stability and productivity of both agricultural systems and natural ecosystems. Strategic and applied research has demonstrated that certain co-operative microbial activities can be exploited, as a low-input biotechnology, to help sustainable agriculture and agroforestry.
References
Aguilar OM, López MV, Riccillo PM (2001) The diversity of rhizobia nodulating beans in Northwest Argentina as a source of more efficient inoculant strains. J Biotech 91:181–188
Albareda M, Rodriguez-Navarro DN, Camacho M, Temprano FJ (2008) Alternatives to peat as a carrier for rhizobia inoculants: solid and liquid formulations. Soil Biol Biochem 40:2771–2779
Alberton O, Kaschuk G, Hungria M (2006) Sampling effects on the assessment of genetic diversity of rhizobia associated with soybean and common bean. Soil Biol Biochem 38:1298–1307
Albrecht A, Kandji ST (2003) Carbon sequestration in tropical agroforestry systems. Agric Ecosyst Environ 99:15–27
Alexandre A, Laranjo M, Oliveira S (2006) Natural populations of chickpea rhizobia evaluated by antibiotic resistance profiles and molecular methods. Microb Ecol 51:128–136
Alexandre A., Brígido C., Laranjo M., Rodrigues S., Oliveira S. (2009) Survey of Chickpea Rhizobia Diversity in Portugal Reveals the Predominance of Species Distinct from Mesorhizobium ciceri and Mesorhizobium mediterraneum. Microb Ecol 1–12. doi:10.1007/s00248-009-9536-6.
Almeida EF, Polizel RPH, Gomes LC, Xavier FA, Mendonça ES (1997) Biomassa microbiana em sistemas agroflorestais na zona da mata mineira. Rev Bras Agroecol 2:739–742
Andrade G, Mihara KL, Linderman RG, Bethlenfalvay GJ (1998) Soil aggregation status and rhizobacteria in the mycorrhizosphere. Plant Soil 202:89–96
Andronov EE, Roumyantseva ML, Sagoulenko VV, Simarov BV (1999) Effect of the host plant on the genetic diversity of a natural population of Sinorhizobium meliloti. Russian J Genet 35:1169–1176
Anyango B, Wilson KJ, Beynon JL, Giller KE (1995) Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. App Env Microb 61:4016–4021
Araújo ASF, Monteiro RTR (2006) Microbial biomass and activity in a Brazilian soil plus untreated and composted textile sludge. Chemosphere 64:1043–1046
Araújo ASF, Monteiro RTR, Abarkeli RB (2003) Effect of glyphosate on the microbial activity of two Brazilian soils. Chemosphere 52:799–804
Araújo FB, Hungria M (1999) Nodulação e rendimento de soja co-infectada com Bacillus subtilis e Bradyrhizobium japonicum/Bradyrhizobium elkanii. Pesq Agropec Bras 34:1633–1643
Aysan E, Demir S (2009) Using arbuscular mycorrhizal fungi and Rhizobium leguminosarum, Biovar Phaseoli Against Sclerotinia sclerotiorum (Lib.) de bary in the common bean Phaseolus vulgaris L. Plant Pathol J 8:74–78
Bai YM, Zhou XM, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1781
Bala A, Giller KE (2006) Relationships between rhizobial diversity and host legume nodulation and nitrogen fixation in tropical ecosystems. Nut Cycl Agroecosys 76:319–330
Bala A, Murphy P, Giller KE (2002) Occurrence and genetic diversity of rhizobia nodulating Sesbania sesban in African soils. Soil Biol Biochem 34:1759–1768
Bala A, Murphy P, Giller KE (2003a) Distribution and diversity of rhizobia nodulating agroforestry legumes in soils from three continents in the tropics. Mol Ecol 12:917–929
Bala A, Murphy PJ, Osunde AO, Giller KE (2003b) Nodulation of tree legumes and the ecology of their native rhizobial populations in tropical soils. App Soil Ecol 22:211–223
Balachandar D, Raja P, Kumar K, Sundaram SP (2007) Non-rhizobial nodulation in legumes. Biotech Mol Biol Rev 2:49–57
Barea JM, Azcon R, Azcon-Aguilar C (1992) Vesicular–arbuscular mycorrhizal fungi in nitrogen-fixing systems. In: Norris JR, Read DJ, Varma AK (eds) Methods in microbiology. Academic, London, pp 391–416
Barea JM, Azcon R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie van Leeuwenhoek Inter J Gen Mol Microbiol 81:343–351
Barea JM, Azcon R, Azcon-Aguilar C (2004) Mycorrhizal fungi and plant growth promoting rhizobacteria. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Heidelberg, pp 351–371
Barea JM, Werner D, Azcon-Aguilar C, Azcon R (2005) Interactions of arbuscular mycorrhiza and nitrogen fixing simbiosis in sustainable agriculture. In: Werner D, Newton WE (eds) Agriculture, forestry, ecology and the environment. Kluwer, The Netherlands
Barreto PAB, Gama-Rodrigues EF, Gama-Rodrigues AC, Fontes AG, Polidoro JC, Moço MKS, Machado RCR, Baligar VC (2010) Distribution of oxidizable organic C fractions in soils under cacao agroforestry systems in Southern Bahia, Brazil. Agrofor Sys doi:10.1007/s10457-010-9300-4
Barrett CF, Parke MA (2005) Prevalence of Burkholderia sp. nodule symbionts on four mimosoid legumes from Barro Colorado Island. Panama Syst App Microbiol 28:57–65
Barrett CF, Parke MA (2006) Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl Environ Microbiol 72:1198–1206
Bashan Y, Salazar B, Puente ME (2009) Responses of native legume desert trees used for reforestation in the Sonoran Desert to plant growth-promoting microorganisms in screen house. Biol Fert Soils 45:655–662
Belsky AJ, Amundson RG, Duxbury JM (1989) The effects of trees on their physical, chemical and biological environments in a semi-arid savanna in Kenya. J App Ecol 26:1005–1024
Ben RF, Prévost D, Yezza A, Tyagi RD (2007) Agro-industrial waste materials and wastewater sludge for rhizobium inoculant production: a review. Biores Tech 98:3535–3546
Benata H, Mohammed O, Noureddine B, Abdelbasset B, Abdelmoumen H, Muresu R, Squartini A, Idrissi MME (2008) Diversity of bacteria that nodulate Prosopis juliflora in the eastern area of Morocco. Syst App Microbiol 31:378–386
Benhizia Y, Benhizia H, Benguedouar A, Muresu R, Giacomini A, Squartir A (2004) Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst Appl Microbiol 27:462–468
Bontemps C, Elliott GN, Simon MF, Reis Júnior FB, Gross E, Lawton RC, Elias NN, Loureiro MF, De Faria SM, Sprent JI, James EK, Young JPW (2009) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19:44–52
Bowen GD, Rovira AD (1991) The rhizosphere. The hidden half of the hidden half. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 641–669
Bressiani JA (2001). Seleção sequencial em cana-de-açúcar Agronomy—Plant Breed. Genet. USP, Piracicaba, pp 159
Brockman FJ, Bezdicek DF (1989) Diversity within serogroups of Rhizobium leguminosarum biovar viceae in the Palouse region of eastern Washington as indicated by plasmid profiles, intrinsic antibiotic resistance, and topography. App Env Microb 55:109–115
Brookes PC (2001) The soil microbial biomass: concept, measurement and applications in soil ecosystem research. Microbes Environ 16:131–140
Browaldh M (1997) Change in soil mineral nitrogen and respiration following tree harvesting from an agrisilvicultural system in Sweden. Agrofor Sys 35:131–138
Caballero-Mellado J, Martinez-Romero E (1999) Soil fertilization limits the genetic diversity of Rhizobium in bean nodules. Symbiosis 26:111–121
Cacho O (2001) An analysis of externalities in agroforestry systems in the presence of land degradation. Ecol Econ 39:131–143
Cardoso MI, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agric Ecosys Environ 116:72–84
Catroux G, Hartmann A, Revellin C (2001) Trends in rhizobial inoculant production and use. Plant Soil 230:21–30
Ceccon E (2008) Production of bioenergy on small farms: a two-year agroforestry experiment using Eucalyptus urophylla intercropped with rice and beans in Minas Gerais, Brazil. New For 35:285–298
Chander K, Goyal S, Nandal DP, Kapoor KK (1998) Soil organic matter, microbial biomass and enzyme activities in a tropical agroforestry system. Biol Fertil Soils 27:168–172
Chebotar VK, Asis CA, Akao S (2001) Production of growthpromoting substances and high colonization ability of rhizobacteria enhance the nitrogen fixation of soybean when inoculated with Bradyrhizobium japonicum. Biol Fert Soils 34:427–432
Chen W, De Faria SM, Straliotto R, Pitard RM, Simões-Araújo JL, Chou J, Chou Y, Barrios E, Prescott AR, Elliott GN, Sprent JI, Young PW, James EK (2005) Proof that Burkholderia strains form effective symbioses with legumes: a study of novel mimosa-nodulating strains from South America. App Environ Microbiol 71:7461–7471
Chen W-M, Laevens S, Lee TM, Coenye T, de Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735
Chen WM, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by β-Proteobacteria is widespread in nature. J Bacteriol 185:7266–7272
Chen WM, Faria SM, Chou JH, James EK, Elliott GN, Sprent JI, Bontemps C, Young JPW, Vandamme P (2008) Burkholderia sabiae sp nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 58:2174–2179
Chesney P (2008) Nitrogen and fine root length dynamics in a tropical agroforestry system with periodically pruned Erythrina poeppigiana. Agrofor Sys 72:149–159
Chikowo R, Mapfumo P, Leffelaar PA, Giller KE (2006) Integrating legumes to improve N cycling on smallholder farms in sub-humid Zimbabwe: resource quality, biophysical and environmental limitations. Nut Cycl Agroecosys 76:219–231
Collins MT, Thies JE, Abbott LK (2002) Diversity and symbiotic effectiveness of Rhizobium leguminosarum bv. trifolii isolates from pasture soils in south-western Australia. Austr J Soil Res 40:1319–1329
Daba S, Haile M (2000) Effects of rhizobial inoculant and nitrogen fertilizer on yield and nodulation of common bean. J Pl Nut 23:581–591
Dashti N, Zhang F, Hynes R, 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 2:205–213
Date RA (1997) The contribution of R&D on root-nodule bacteria to future cultivars of tropical forage legumes. Trop Grass 31:350–354
Date RA (2000) Inoculated legumes in cropping systems of the tropics. Field Crops Res 65:123–136
Daudin D, Sierra J (2008) Spatial and temporal variation of below-ground N transfer from a leguminous tree to an associated grass in an agroforestry system. Agric Ecosys Environ 126:275–280
De Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811
Deaker R, Roughley RJ, Kennedy IR (2004) Legume seed inoculation technology—a review. Soil Biol Biochem 36:1275–1288
Demir S, Akkopru A (2007) Using of arbuscular mycorrhizal fungi (AMF) for biocontrol of soil-borne fungal plant pathogens. In: Chincholkar SB, Mukerji KG (eds) Biological control of plant diseases. Haworth Press, USA, pp 17–37
Diabate M, Munive A, Faria SM, Ba A, Dreyfus B, Galiana A (2005) Occurrence of nodulation in unexplored leguminous trees native to the West African tropical rainforest and inoculation response of native species useful in reforestation. New Phytol 166:231–239
Dick RP (1997) Soil enzymes activities as integrative indicator of soil health. In: Pankhurst C, Doube BM, Gupta VVSR (eds) Biological indicators of soil health. CAB International, Cambridge, pp 121–156
Diouf D, Samba-Mbaye R, Lesueur D, Ba AT, Dreyfus B, De Lajudie P, Neyra M (2007) Genetic diversity of Acacia seyal Del. rhizobial populations indigenous to senegalese soils in relation to salinity and pH of the sampling sites. Micro Ecol 54:553–566
Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149
Doignon-Bourcier F, Sy A, Willems A, Torck U, Dreyfus B, Gillis M, De Lajudie P (1999) Diversity of Bradyrhizobia from 27 tropical Leguminosae species native of Senegal. Syst App Microbiol 22:647–661
Doyle JJ, Doyle J (1998) Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3:473–478
Duodu S, Nsiah EK, Bhuvaneswari TV, Svenning MM (2006) Genetic diversity of a natural population of Rhizobium leguminosarum biovar trifolii analysed from field nodules and by a plant infection technique. Soil Biol Biochem 38:1162–1165
Duodu S, Carlsson G, Huss-Danell K, Svenning MM (2007) Large genotypic variation but small variation in N2 fixation among rhizobia nodulating red clover in soils of northern Scandinavia. J App Microbiol 102:1625–1635
Elliott GN, Chou J-H, Chen W-M, Bloemberg GV, Bontemps C, Martinez-Romero E, Velazquez E, Young JPW, Sprent JI, James EK (2009) Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol 11:762–778
Fagerli IL, Svenning MM (2005) Arctic and subarctic soil populations of Rhizobium leguminosarum biovar trifolii nodulating three different clover species: characterisation by diversity at chromosomal and symbiosis loci. Pl Soil 275:371–381
FAO (2005) The importance of soil organic matter. Key to drought-resistant soil and sustained food and production. Rome, p 78
Faria S.M. (1997) Obtenção de Estirpes de Rizóbio Eficientes na Fixação Biológica de Nitrogênio para Espécies Florestais. (Aproximação 1997). Embrapa Agrobiologia, Serop‚dica, p 4
Faria SM (2000) Obtenção de estirpes de rizóbio eficientes na fixação de nitrogênio para espécies florestais (aproximação 2000). Embrapa Agrobiologia, Seropédica, p 10
Faria SM (2002) Obtenção de estirpes de rizóbio eficientes na fixação de nitrogênio para espécies florestais (aproximação 2001). Embrapa Agrobiologia, Seropédica, p 16
Faria SM, Lima HC (1998) Additional studies of the nodulation status of legume species in Brazil. Plant Soil 200:185–192
Faria SM, Franco AA (2002) Identificação de bactérias eficientes na fixação biológica de nitrogênio para espécies leguminosas arbóreas. EMBRAPA-Agrobiologia, Seropédica, p 16
Faria SM, Moreira VCG, Franco AA (1984) Seleção de estirpes de Rhizobium para espécies leguminosas florestais. Pesq Agropec Bras 19:175–179
Faria, S.M. Ocurrence and rhizobial selection for legume trees adapted to acid soils (1995). In: Evans DO, Szott T (eds) Nitrogen fixing trees for acid soil. Nitrogen Fixing Tree Association. Morrilton, USA, pp 295–300
Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22:47–72
Fernandes Júnior PI, Rohr TG, Oliveira PJ, Xavier GR, Rumjanek NG (2009) Polymers as carriers for rhizobial inoculant formulations. Pesq Agropec Bras 44:184–1190
Figueiredo MVB, Martinez CR, Burity HA, Chanway CP (2008) Plant growth-promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean (Phaseolus vulgaris L.). World J. Microbiol Biotechnol 24:1187–1193
Fisher RF (1995) Amelioration of degraded rain forest soils by plantations of native trees. Soil Sci Soc Am J 59:544–549
Fontes SJ, Barrios E, Six J (2010) Earthworms, soil fertility and aggregate-associated soil organic matter dynamics in the Quesungual agroforestry system. Geoderma 155:320–328
Freitas ADS, Sampaio EVSB, Santos CERS, Fernandes AR (2010) Biological nitrogen fixation in tree legumes of the Brazilian semi-arid caatinga. J Arid Environ 74:344–349
Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36
Galli-Terasawa LV, Glienke-Blanco C, Hungria M (2003) Diversity of a soybean rhizobial population adapted to a Cerrados soil. World J Microb Biotech 19:933–939
Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210
García-Fraile P, Velázquez E, Mateos PF, Martínez-Molina E, Rivas R (2008) Cohnella phaseoli sp. nov., isolated from root nodules of Phaseolus coccineus in Spain, and emended description of the genus Cohnella. Int J Syst Evol Microbiol 58:1855–1859
Gomez E, Bisaro V, Conti M (2000) Potential C-source utilization patterns of bacterial communities as influenced by clearing and land use in a vertic soil of Argentina. Appl Soil Ecol 15:273–281
Grange L, Hungria M (2004) Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biol Biochem 36:1389–1398
Handley BA, Hedges AJ, Beringer JE (1998) Importance of host plants for detecting the population diversity of Rhizobium leguminosarum biovar Viciae in soil. Soil Biol Biochem 30:241–249
Haney RL, Senseman SA, Krutz LJ, Hons FM (2003) Soil carbon and nitrogen mineralization as affected by atrazine and glyphosate. Biol Fert Soils 35:35–40
Heuvelop J, Fassbender HW, Alpizar L, Enriquez G, Falster H (1988) Modelling agroforestry systems of cacao (Theobroma cacao) in Costa Rica. II. Cacao and wood production, litter production and decomposition. Agrofor Syst 6:37–48
Hirsch AM, Lum MR, Downie JA (2001) What makes the rhizobia-legume symbiosis so special? Plant Physiol 127:1484–1492
Howieson J, Ballard R (2004) Optimising the legume symbiosis in stressful and competitive environments within southern Australia—some contemporary thoughts. Soil Biol Biochem 36:1261–1273
Hubbell DH, Kidder G (2003) Biological nitrogen fixation. SL-16, soil and water science department, Florida cooperative extension service, institute of food and agricultural sciences. University of Florida, USA, pp 1–4
Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res 65:151–164
Jaftha JB, Strijdom BW, Steyn PL (2002) Characterization of pigmented methylotrophic bacteria which nodulate Lotononis bainesii. Syst Appl Microbiol 25:440–449
Jalonen R, Nygren P, Sierra J (2009) Transfer of nitrogen from a tropical legume tree to an associated fodder grass via root exudation and common mycelial networks. Plant Cell Environ 32:1366–1376
Jenkinson DS, Ladd JN (1981) Microbial biomass in soil: measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry. Dekker, New York, pp 415–471
Jesus EC, Moreira FMS, Florentino LA, Rodrigues MID, Oliveira MS (2005) Diversidade de bactérias que nodulam siratro em três sistemas de uso da terra da Amazônia Ocidental. Pesq Agropec Bras 40:769–776
Kaur B, Gupta SR, Singh G (2000) Soil carbon, microbial activity and nitrogen availability in agroforestry systems on moderately alkaline soils in northern India. App Soil Ecol 15:283–294
Kirby KR, Potvin C (2007) Variation in carbon storage among tree species: implications for the management of a small-scale carbon sink project. For Ecol Manage 246:208–221
Kuklinsky-Sobral J, Araujo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251
Langer H, Nandasena KG, Howieson JG, Jorquera M, Borie F (2008) Genetic diversity of Sinorhizobium meliloti associated with alfalfa in Chilean volcanic soils and their symbiotic effectiveness under acidic conditions. World J Microb Biot 24:301–308
Law IJ, Botha WF, Majaule UC, Phalane FL (2007) Symbiotic and genomic diversity of ‘cowpea’ bradyrhizobia from soils in Botswana and South Africa. Biol Fert Soils 43:653–663
Lesueur D, Ingleby K, Odee D, Chamberlain J, Wilson J, Manga TT, Sarrailh JM, Pottinger A (2001) Improvement of forage production in Calliandra calothyrsus: methodology for the identification of an effective inoculum containing Rhizobium strains and arbuscular mycorrhizal isolates. J Biotech 91:269–282
Loveall ST, Sullivan WC (2006) Environmental benefits of conservation buffers in the United States: evidence, promise, and open questions. Agric Ecosyst Environ 112:249–260
Lowrance R, Dabney S, Schultz R (2002) Improving water and soil quality with conservation buffers. J Soil Water Conserv 57:36–43
Lucas-Garcia JA, Probanza A, Ramos B, Colon-Flores JJ, Gutierrez-Mañero FJ (2004) Effects of plant growth promoting rhizobateria (PGPRs) on the biological nitrogen fixation, nodulation and growth of Lupinus albus I. cv. Multolupa. Eng Life Sci 4:71–77
Ma W, Penrose DM, Glick BR (2002) Strategies used by rhizobia to lower plant ethylene levels and increase nodulation. Can J Microbiol 48:947–954
Macdicken KG, Vergara NT (1990) Agroforestry: classification and management. Wiley, New York, p 382
Makatiani ET, Odee DW (2007) Response of Sesbania sesban (L.) Merr. to rhizobial inoculation in an N-deficient soil containing low numbers of effective indigenous rhizobia. Agrofor Sys 70:211–216
Manassila M, Nuntagij A, Kotepong S, Boonkerd N, Teaumroong N (2007) Characterization and monitoring of selected rhizobial strains isolated from tree legumes in Thailand. African J Biotech 6:1393–1402
Manley R, Feller C, Swift MJ (2007) Historical evolution of soil organic matter concepts and their relationships with the fertility and sustainability of cropping systems. Agric Ecosys Environ 119:217–233
Martinez-Romero E, Segovia L, Mercante FM, Franco AA, Graham P, Pardo MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Sys Bacteriol 41:417–426
Martins LMV, Xavier GR, Rangel FW, Ribeiro JRA, Neves MCP, Morgado LB, Rumjanek NG (2003) Contribution of biological nitrogen fixation to cowpea: a strategy for improving grain yield in the semi-arid region of Brazil. Biol Fert Soils 38:333–339
Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many Rhizobium recipes? Trends Microbiol 17:458–466
Mayak S, Tirosh T, Glick BR (1999) Effect of wild type and mutant plant growth promoting rhizobacteriaon the rooting of mung bean cuttings. J Plant Growth Regul 18:49–53
Mendonça ES, Leite LFC, Ferreira Neto PS (2001) Cultivo do café em sistema agroflorestal: uma opção para recuperação de solos degradados. Rev Arvore 25:375–383
Miralles I, Ortega R, Alemandros G, SancheZ-Maranon M, Soriano M (2009) Soil quality and organic carbon ratios in mountain agroecosystems of South-east Spain. Geoderma 150:32–40
Mnasri B, Mrabet M, Laguerre G, Aouani ME, Mhamdi R (2007) Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N 2 -fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch Microbiol 187:79–85
Moonen AC, Bàrberi P (2008) Functional biodiversity: an agroecosystem approach. Agric Ecosys Environ 127:7–21
Mostasso L, Mostasso FL, Dias BG, Vargas MAT, Hungria M (2002) Selection of bean (Phaseolus vulgaris L.) rhizobial strains for the Brazilian Cerrados. Field Crops Res 73:121–132
Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the β-subclass of Proteobacteria. Nature 411:948–950
Moulin L, Chen W-M, Béna G, Dreyfus B, Boivin-Masson C (2002) Rhizobia: the family is expanding. In: Finan T, O’Brian M, Layzell D, Vessey K, Newton W (eds) Nitrogen fixation: global perspectives. CAB International, Wallingford, pp 61–65
Mungai NW, Motavalli PP, Kremer RJ, Nelson KA (2005) Spatial variation of soil enzyme activities and microbial functional diversity in temperate alley cropping systems. Biol Fertil Soils 42:129–136
Muresu R, Polone E, Sulas L, Baldan B, Tondello A, Delogu G, Cappuccinelli P, Alberghini S, Benhizia Y, Benhizia H, Benguedouar A, Mori B, Calamassi R, Dazzo FB, Squartini A (2008) Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol Ecol 63:383–400
Myers RT, Zak DR, White DC, Peacock A (2001) Landscape-level patterns of microbial community composition and substrate use in upland forest ecosystems. Soil Sci Soc Am J 65:359–367
Nair PKR, Gordone AM, Mosquera-Losadac, MR (2008) Agroforestry. Elsevier, Netherland, pp. 101–110
Nair PKR, Kumar BM, Nair VD (2009) Agroforestry as a strategy for carbon sequestration. J Pl Nutrit Soil Sci 172:10–23
Nygren P, Leblanc HA (2009) Natural abundance of 15N in two cacao plantations with legume and non-legume shade trees. Agrofor Sys 76:303–315
Odee DW, Haukka K, McInroy SG, Sprent JI, Sutherland JM, Young JPW (2002) Genetic and symbiotic characterization of rhizobia isolated from tree and herbaceous legumes grown in soils from ecologically diverse sites in Kenya. Soil Biol Biochem 34:801–811
Okasaki S, Sugawara M, Yuhashi KI, Minamisawa K (2007) Rhizobitoxine-induced chlorosis occurs in coincidence with methionine deficiency in soybeans. Ann Botany 100:55–59
Palma JHN, Graves AR, Bunce RGH, Burgess PJ, Filippi R, Keesman K, van Keulen H, Liagre F, Mayus M, Moreno G, Reisner Y, Herzog F (2007) Modeling environmental benefits of silvoarable agroforestry in Europe. Agric Ecosyst Environ 119:320–334
Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143
Powlson DS, Brookes PC, Christensen BT (1987) Measurement of soil microbial biomass provides an early indication of changes in total organic matter due to straw incorporation. Soil Biol Biochem 19:159–164
Pueppke SG, Broughton WJ (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant-Microbe Interact 12:293–318
Rao DLN, Pathak H (1996) Ameliorative influence of organic matter on biological activity of salt affected soils. Arid Soil Res Rehab 10:311–319
Remans R, Croonenborghs A, Gutierrez RT, Michiels J, Vanderleyden J (2007) Effects of plant growth-promoting rhizobacteria on nodulation of Phaseolus vulgaris [L.] are dependent on plant P nutrition. Euro J Plant Pathol 119:341–351
Rhamani HA, Saleh-Rastin N, Khavazi K, Asgharzadeh A, Fewer D, Kiani S, Lindstrm K (2009) Selection of thermotolerant bradyrhizobial strains for nodulation of soybean (Glycine max L.) in semi-arid regions of Iran. World J Microb Biotech 25:591–600
Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E (2002) A new species of Devosia that forms a unique nitrogen-fixing rootnodule symbiosis with the aquatic legume Neptunia natans. Appl Environ Microbiol 68:5217–5222
Roshetko JM, Lasco RD, Delos Angeles MD (2007) Smallholder agroforestry systems for carbon storage. Mitigation Adapt Strategies Global Change 12:219–242
Ruiz-Díez B, Fajardo S, Puertas-Mejía MA, De Felipe MDR, Fernández-Pascual M (2009) Stress tolerance, genetic analysis and symbiotic properties of root-nodulating bacteria isolated from Mediterranean leguminous shrubs in Central Spain. Arch Microbiol 191:35–46
Ruiz-Lozano JM, Collados C, Barea JM, Azcon R (2001) Arbuscular mycorrhizal symbiosis can alleviate droughtinduced nodule senescence in soybean plants. New Phytol 151:493–502
Salati E, Santos AA, Klabin I (2006) Relevant environmental issues. Estudos Avançados 20:107–127
Saravana-Kumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbial 102:1283–1292
Scheublin TR, Van der Heijden MGA (2006) Arbuscular mycorrhizal fungi colonize nonfixing root nodules of several legume species. New Phytol 172:732–738
Serraj R (2004) Symbiotic nitrogen fixation: prospects for enhanced application in tropical agriculture. IBH, New Delhi, p 367
Sharrow SH, Ismail S (2004) Carbon and nitrogen storage in agroforests, tree plantations, and pastures in western Oregon, USA. Agroforest Syst 60:123–130
Silva MF, Oliveira PJ, Xavier GR, Rumjanek NG, Reis VM (2009) Inoculantes formulados com polímeros e bactérias endofíticas para a cultura da cana-de-açúcar. Pesq Agropec Bras 44:1437–1443
Silva VN, Silva LESF, Figueiredo MVB (2006) Atuação de rizóbios com rizobactérias promotora de crescimento em plantas na cultura do caupi (Vigna unguiculata L. Walp). Acta Sci Agron 28:407–412
Silva VN, Silva LESF, Figueiredo MVB, Carvalho FG, Silva MLRB, Silva AJN (2007) Caracterização e seleção de populações nativas de rizóbios de solo da região semi-árida de Pernambuco. Pesq Agropec Trop 37:16–21
Sørensen J, Sessitsch A (2007) Plant-associated bacterial-lifestyle and molecular interactions. In: Van Elsas JD, Jansson JK, Trevors JT (eds) Modern soil microbiology. CRC, New York, pp 221–236
Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, Kew, London
Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506
Sun Y, Cheng Z, Glick BR (2009) The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol Let 296:131–136
Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220
Sziderics AH, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J Microbiol 53:1195–1202
Tangjang S, Arunachalam K, Arunachalam A, Shukla AK (2009) Microbial population dynamics of soil under traditional agroforestry systems in Northeast India. Res J Soil Biol 1:1–7
Tilak KVBR, Rauganayaki N, Manoharachari C (2006) Synergistic effects of plant-growth promoting rhizobacteria and Rhizobium on nodulation and nitrogen fixation by pigeonpea (Cajanus cajan). Europ J Soil Sci 57:67–71
Tornquist CG, Hons FM, Feagley SE, Haggar J (1999) Agroforestry system effects on soil characteristics of the Sarapiquí region of Costa Rica. Agric Ecosys Environ 73:19–28
Udawatta RP, Kremer RJ, Adamson BW, Anderson SH (2008) Variations in soil aggregate stability and enzyme activities in a temperate agroforestry practice. App Soil Ecol 39:153–160
Van Berkum P, Eardly BD (2002) The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. In: Finan TM, O’Brian MR, Layzell DB, Vessey JK, Newton WE (eds) Nitrogen fixation: global perspectives. CAB International, New York, p 520
Vandamme P, Goris J, Chen WM, Vos P, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst App Microbiol 25:507–512
Vessey JK, Buss TJ (2002) Bacillus cereus UW85 inoculation effects on growth, nodulation, and N accumulation in grain legumes. Controlled-environment studies. Can J Plant Sci 82:282–290
Vivas A, Marulanda A, Ruiz-Lozano JM, Barea JM, Azcon R (2003a) Influence of a Bacillus sp. on physiological activities of two arbuscular mycorrhizal fungi and on plant responses to PEG-induced drought stress. Mycorrhiza 13:249–256
Vivas A, Azcon R, Biro B, Barea JM, Ruiz-Lozano JM (2003b) Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pretense L. under lead toxicity. Can J Microbiol 49:577–588
Watanabe K, Hamamura N (2003) Molecular and physiological approaches to understanding the ecology of pollutant degradation. App Soil Ecol 31:120–135
Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14
Wolde-Meskel E, Terefework Z, Lindström K, Frostegard A (2004) Rhizobia nodulating African Acacia spp. and Sesbania sesban trees in southern Ethiopian soils are metabolically and genomically diverse. Soil Biol Biochem 36:2013–2025
Xavier GR, Correia MEF, Aquino AM, Zilli JÉ, Rumjanek NG (2010) The structural and functional biodiversity of soil: an interdisciplinary vision for conservation agriculture in Brazil. In: Dion P (ed) Soil biol agric trop. Springer, Heidelberg, pp 65–80
Yadav RS, Yadav BL, Chhipa BR, Dhyani SK, Ram M (2010) Soil biological properties under different tree based traditional agroforestry systems in a semi-arid region of Rajasthan, India. Agroforest Syst 81:195–202
Yan F, McBratney AB, Copeland L (2000) Functional substrate biodiversity of cultivated and uncultivated a horizons of vertisols in NW New South Wales. Geoderma 96:321–343
Yates RJ, Howieson JG, Real D, Reeve WG, Vivas-Marfisi A, O’Hara GW (2005a) Evidence of selection for effective nodulation in the Trifolium spp. symbiosis with Rhizobium leguminosarum biovar trifolii. Aust J Experim Agric 45:189–198
Yates RJ, Howieson JG, Nandasena KG, O’Hara GW (2005b) Root-nodule bacteria from indigenous legumes in the north-west of Western Australia and their interaction with exotic legumes. Soil Biol Biochem 36:1319–1329
Zafar-ul-Hye M (2008) Improving nodulation in lentil through co-inoculation with rhizobia and ACC-deaminase containing plant growth promoting rhizobacteria, PhD Thesis, University of Agriculture, Faisalabad, Pakistan, p 198
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. Ann Botany 77:453–459
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Araujo, A.S.F., Leite, L.F.C., Iwata, B.F. et al. Microbiological process in agroforestry systems. A review. Agron. Sustain. Dev. 32, 215–226 (2012). https://doi.org/10.1007/s13593-011-0026-0
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13593-011-0026-0