Abstract
The world has witnessed explosive population growth, which requires an efficient food supply. To this end, various efforts have been performed in agriculture among which the applying chemicals with anti-pest and fertilizing activity was a strategy of choice. However, implementation of such compounds has shown to have serious drawbacks, from the reduction of naturally occurring organisms which control the pests to the concerns arisen from environmental pollution. Therefore, the discovery and development of biological strategies have attracted much attention. Accordingly, there are well-known plant growth-promoting microorganisms (GPMs) with great potentials in improving the growth of plants via providing nutrition and alleviating biotic and abiotic stresses. Herein, a comprehensive study was performed to gather together the most updated knowledge on these mechanisms.
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14.1 Introduction
Different soil properties such as its texture, structure, and nutritional ingredients directly influence plant growth, among which, the latter property shows great importance. There are non-minerals (hydrogen, oxygen, and carbon), and minerals (macronutrients and micronutrients) obligatory for the growth and development of plants. Carbon dioxide and water provide non-minerals for the plant (Taiz 2010), while the latter is obtained from the soil. Since plants consume large amounts of some macronutrients such as nitrogen, phosphorus, and potassium, these components exist in very low quantity in nutrient-depleted soil, while other macronutrients like calcium and magnesium are found abundantly in the soil under normal conditions, especially whenever lime is applied to reduce soil acidity. Macronutrients, e.g., sulphur, and micronutrients including boron, copper, iron, chloride, manganese, molybdenum, and zinc are released by the slow procedure of organic matter decomposition (Hänsch and Mendel 2009; Yadav et al. 2021) (Fig. 14.1).
Bioavailability of these nutrients for plants is dependent on their amounts in the soil, the soil composition, as well as its physicochemical characteristics like nutrient and water retention, and oxygen content of the soil which are influenced by soil texture, the proportion of soil ingredients or components like sand, silt, clay and organic matter (Bronick and Lal 2005). High content of clay and organic matter leads to a considerable level of nutrient and water retention, and in some cases, it results in waterlogged soil and thus depletion of oxygen content. In this condition, aerobic respiration and nitrate production are ceased. On the other hand, nutrient uptake becomes difficult in soil containing a high level of sand, due to their leaching and entering to groundwater (Galloway et al. 2008). Soil structure, aggregation of soil particles, determines productivity; because it directly affects the movement of water and oxygen, availability of nutrient, and microbial activity within the rhizospheric regions of plants (Bronick and Lal 2005). Soil pH is also an influential factor in the bioavailability of nutrients. The macronutrients and micronutrients show less bioavailability at high and low pH levels. The slightly acidic pH range due to promoting root growth, nitrogen fixation, and sulfur conversion to sulfate, releasing minerals, and increasing carbonates, sulfates, and phosphates solubility, is suitable for plant growth (Taiz 2010). In sum, the soil contains essential elements, and its physical, chemical, and biological characteristics influence plant growth (Fig. 14.2).
14.2 Fertilizers as Plant Growth Boosters
It has been predicted that the world population will be undoubtedly increased to 10 billion around 2050, with an annual increase of 97 million (Conway 2012). Therefore, the inevitable increasing demand for food and the falling ratio of cultivable lands will be a serious challenge. According to FAO, an unacceptably high portion of people are undernourished (FAO 2010). To ameliorate this need, fertilizers and pesticides have been consumed to achieve enhanced productivity through promoting plant growth and preventing product loss due to pests.
14.2.1 Chemical Fertilizers
Chemical fertilizers, cost-effective formulation of nitrogen, phosphate, and potassium, have been widely used over centuries. These fertilizers provide nutrition in the form of bioavailable organic/inorganic salts, and their application appeared as a quick improvement in plant growth. In addition to nutrients including, phosphate, nitrate, ammonium, and potassium salts, heavy metals like Hg, Cd, As, Pb, Cu, Ni, and Cu; natural radionuclides like 238U, 232Th, and 210Po also exist in chemical fertilizers. Netherlands, Egypt, Japan, China, UK, Germany, France, USA, Italy, India, Greece, Indonesia, and Turkey are using 665.5, 624.8, 373.2, 301.5, 287.5, 205.4, 180.1, 160.8, 126.4, 121.4, 115.4,106.9, and 100.4 kg per hectare chemical fertilizer (N + P + K), respectively (Savci 2012).
Over time, it has been revealed that prolonged usage of chemical fertilizers has resulted in the gradual loss of their effectiveness and corresponding environmental problems were also emerging (Kumar et al. 2021; Sharma et al. 2021; Xiang et al. 2012). In this situation, more chemical fertilizers should be applied to achieve the same productivity. Also, the production process of chemical fertilizer results in the release of hazardous substances including sulfur oxides, nitric oxides, and fluorine compounds into the environment. Continuous application of chemical fertilizers can profoundly modify the salinity and pH of the soil, decline soil mineral and its water retention capacity, which can lead to gradual deterioration. It has been observed that extended or continuous supply of a considerable amount of nitrogen fertilizer can cause plant tissue softening, leading to increased sensitivity of plants to pests and diseases (Adesemoye et al. 2010; Chen 2006).
Whenever excessive amounts of chemical fertilizers are applied, and plants cannot assimilate them; several physical and chemical procedures are activated to decrease their concentrations in soil. Rinsing out, leaching, volatilization, immobilization, replacement, precipitation, and microbiological conversions are some of these strategies which may lead to the dispersion of hazardous chemicals into the air and aquatic ecosystems and cause long-lasting serious environmental problems, e.g., eutrophication of waters.
Considerable rate (50–70%) of nitrogenous contamination is due to nitrogenous fertilizer. Unabsorbed nitrogenous fertilizers are converted to nitrate through microbial nitrification. Generated soluble nitrate reaches the depth of soil and enter the groundwater due to its high solubility and negative charge. Leached nitrate, reactive nitrogen species, nitrites, and nitrosamines in ground and surface waters are some of the life-threatening compounds. High levels of nitrates, nitrites, and nitrosamines can aggregate in crops and adversely impose human and animal health. High-level nitrate (more than 50 mg NO3−/L) in drinking water cause inflammation of the digestive and urinary systems, methemoglobinemia, and some related diseases in infants and ruminant animals. Also, it increases the risk of metabolic diseases including cancers, respiratory disorders, cardiovascular ailments, goiter, congenital disabilities, digestive system disease, and the rate of infections with West Nile virus, malaria, and cholera (Galloway et al. 2008).
High buffering feature of soil has resulted in less obvious effects of chemical fertilizers on it; however, over time its deterioration occurs, and in turn, leads to decreased soil quality, normal structure, and composition due to losing its buffering potential. Also, the accumulation of toxic substances in the soil is lethal for living organisms, like microorganisms and earthworms. This biologically passive soil possesses negligible organic matter and less liberation of nutrients as much as biologically active soil, and because of this, interactions of living organisms are disrupted in this condition (Chandramohan et al. 2013). Prolonged consumption of nitrogen fertilizers like ammonium sulfate, which produces acid, dramatically reduces soil pH. Also, the diversity of microbial species in the rhizospheric regions are changed in acidic soil. In this condition, activities of plant growth-promoting microorganisms like decomposition of organic matter and symbiotic interaction with plants are reduced or inhibited. Ammonium sulfate fertilizer extremely acidifies the soil, and its extensive use will result in Mg deficiency (Fageria et al. 2010).
One of the most problematic matters during applying chemical fertilizers is groundwater contamination (Galloway et al. 2008). Nitrates are generated from the breakdown of nitrogen fertilizers, and because of their water-solubility feature, they easily move within the soil and can persist in that position for a long time leading to ecosystem deterioration (3).
Besides detrimental effects on human and animal life, terrestrial and aquatic ecosystems are affected by the extensive use of chemical fertilizers. For instance, large fractions of nitrogen fertilizers are oxidized, and nitrogen monoxides and nitric oxides are generated through denitrification process, which results in the depletion of the ozone layer and increases the probability of skin cancer. Also, nitric acid can be created after using urea and ammonium salt, the most current forms of ammonium, and in combination with sulphuric acid leading to the generation of acid rains which adversely affects ecosystems and results in erosion and depletion of the soil. High levels of water-soluble potassium impose an adverse effect on the soil pH and structure as well as seed germination. In this condition, uptake of other minerals and nutrients is ceased and the quality of the crop is declined (Savci 2012).
Rampant fertilization using phosphorous fertilizers disrupts its balance and leads to the accumulation of phosphorous in sites of application. Applied ammonium phosphates and superphosphates containing calcium phosphate, readily relocate under acidic conditions and plants could consume them as the phosphorous source. While in alkaline conditions, phosphorous compounds are potently attached in the phosphorus retarded reactions between soluble phosphates, and aluminum, iron, manganese, and calcium ions. The result of these reactions (including phosphate sorption, adsorption, retention, precipitation, or immobilization) is the production of insoluble and unleachable salts. Therefore, they cannot travel within the soil tissue. Therefore, these processes profoundly decrease the availability of plants to phosphorous. This process makes the continuous application of phosphate fertilizers inevitable. Excessive and accumulated phosphates accelerate eutrophication in terrestrial and aquatic ecosystems, which can impose lethal effects on their inhabitants.
Eutrophication creates an oxygen-free environment that is not suitable for drinking and profoundly reduce living species in the marine ecosystems as well as causes proliferation of unwanted species and unfavorable odor (Chislock et al. 2013). In addition, trace amounts of cadmium, chromium, lead, uranium, and radium exist in phosphate fertilizers. The prolonged application of this fertilizer can enhance the concentrations of these pollutants. These hazardous compounds pollute the soil and water, and whenever they enter the surface water or are absorbed by plants, can, in turn, enter into the human body through the food chain and create life-threatening problems (Fig. 14.3) (Khan et al. 2018).
Although extensive usage of chemical fertilizers has adverse effects on human and animal health and ecosystems, the inevitable need for chemical fertilizers by the agriculture industry is obvious. Lack of their use can lead to insufficient nutrients for the world population. Therefore, there is a pivotal need for alternative fertilizers which sustainably and eco-friendly flourish agricultural yield.
14.2.2 Organic Fertilizers
Conventional agriculture via chemical fertilizers and devastating agricultural imposes adverse effects on human and animal health, microbial habitats, and beneficial insects. It leads to the deterioration of soil and terrestrial ecosystems, and ozone layers. Also, it has been proven that its efficiency is unsustainable (Fricke and Vogtmann 1993; Mäder et al. 2002). Therefore, alternate farming methods are being applied to recover soil quality and ameliorate environmental degradation. One of these new eco-friendly approaches with self-sustainability features is organic agriculture. FAO/WHO has defined organic agriculture as a comprehensive production management system which uses it, the health of agro-ecosystem that is characterized by improved biodiversity, balanced biogeochemical cycles, and enhanced animal and microbial activities in soils. In organic agriculture, sustainable management practices in all aspects of farm management by considering regional conditions and applying locally adapted systems such as agronomic, biological, and mechanical methods should be implemented (FAO/WHO 2015).
In this regard, natural means like growing cover crops, mainly leguminous species, are applied. Organic fertilizers like composts and manure act in a different way in comparison to chemical fertilizers, e.g., they supply nutrients in a lower concentration (like potassium) (Fricke and Vogtmann 1993; Hernández et al. 2010) and slower release rate (like nitrogen because of low rate of mineralization) (Hernández et al. 2010). In sustainable agriculture, maximum yield cannot be achieved by solely relying on organic fertilizers. Therefore, through the combined usage of chemical–organic fertilizer along with biofertilizers, production yield can be maximized in a sustainable approach (Qin et al. 2015; Shafi et al. 2012; Song et al. 2015). The advantages and disadvantages of organic fertilizers are presented in (Fig. 14.4).
14.2.3 Biofertilizers
Applying manure, crop rotation with legumes, and water managing to increase soil’s nutrient content through their naturally occurring microorganisms are some of the ancient strategies to improve the fertility of lands (Franche et al. 2009; Morrison and Cozatl-Manzano 2003; Suthar et al. 2017). Microbial fertilizers were developed and commercialized in the late nineteenth century for the first time (Bashan 1998; Kilian et al. 2000) to ameliorate the unfavorable aspects of excessive usage of chemical fertilizers. Applying biofertilizer results in a reduced application of chemical fertilizer (Singh and Adholeya 2003).
Biofertilizers and green manure, intercrop, or organic supplemented chemical fertilizers are not the same concepts (Bhattacharyya and Jha 2012; Halpern et al. 2015). They are formulated with different types of beneficial microorganisms or their latent forms, which once applied, colonize the rhizospheric region or the inner parts of the plant and perform agriculturally-important activities including conversion of nutritionally critical nutrients from unavailable to bioavailable form (nitrogen and phosphate), mineralization of sulphur, zinc, potassium, and iron, producing degrading enzymes, antibiotics and phytohormones, induction of resistant mechanisms in the plants, secretion of growth hormones through which enhance crop yield up to 10–40% (Ahemad and Kibret 2014; Bhardwaj et al. 2014; Bhattacharjee and Dey 2014; Gaur 2010; Kour et al. 2019b, 2021; Lugtenberg and Kamilova 2009; Mishra et al. 2013a; Owen et al. 2015). Since the biofertilizers have low cost and renewable properties, they can be supplied along with chemical fertilizers to cut down their use, intensify their beneficial activities, and reduce their deteriorating activity on the ecosystem. Biofertilizer provides various inorganic substances with low bio-availability. Therefore, this strategy is more cost-effective for farmers than synthetic fertilizers (Kour et al. 2020). Co-application of phosphate solubilizing bacteria and bacteria with potassium solubilizing activity along with rocks containing low soluble phosphate and potassium enhanced yield and assimilation of nitrogen, phosphate, and potassium by various plants in phosphate and potassium limiting conditions (Han and Lee 2005; Han et al. 2006; Vassilev et al. 2006a). There are several types of biofertilizers, including microorganisms with the ability of nitrogen fixation, phosphate solubilization, phosphate mobilization, and promotion of plant growth (Mondal et al. 2020; Yadav 2021). It is proven that combined application of chemical, organic, and biofertilizers can meet the increasing need of enhancing world population to foods at a time when agriculture-based industries are facing various environmental concerns (Suthar et al. 2017).
However, despite the tremendous application of biofertilizers, their application is limited due to many factors such as the unpredictability of results, difficult identification, and traceability of microbial strains in the field, limited knowledge about interactions among microbial cells and plants, and the technical process of large scale production (Bashan et al. 2014; Lucy et al. 2004; Owen et al. 2015). In addition to bacterial grazers, especially naked amoeba, nematodes can also modify the effectiveness of microbial inoculum (Malusa et al. 2010). One of the important obstacles in applying biofertilizers is that behavioral characteristics of microorganisms are changed in a microbial community compared to a situation that they exist in pure culture. These constraints are encouraging reasons to conduct extensive and comprehensive studies on biofertilizers (Fig. 14.5).
14.2.3.1 Major Constituents of Biofertilizers
Each type of biofertilizer contains various beneficial microorganisms, including plant growth-promoting rhizobacteria, fungal strains like mycorrhiza and cyanobacteria (Table 14.1). These microorganisms can suppress the adverse effects of phytopathogenic organisms and abiotic stresses on plant growth and development via various strategies such as facilitating nitrogen, phosphate, iron, zinc, and potassium acquisition, modifying phytohormone levels, which, in turn, can flourish agriculture in an eco-friendly manner (Kour et al. 2019a; Singh et al. 2020; Thakur et al. 2020; Tiwari et al. 2020, 2021). According to the mechanisms by which biofertilizers augment plant growth, they are divided into various groups including biofertilizers containing microorganisms with nitrogen fixation ability (Rhizobium, Bradyrhizobium, Azospirillum, and Azotobacter), phosphate mobilization ability (Mycorrhiza), growth promotion activity (Pseudomonas), phosphorous solubilization capability (Bacillus, Pseudomonas, Aspergillus, Penicillium, Fusarium, Trichoderma, Mucor, Ovularopsis, Tritirachium, and Candida), and biofertilizers with compost enriching activities (Humicola fuscoatra, Aspergillus flavus, Aspergillus nidulans, Aspergillus niger, Aspergillus ochraceus, Fusarium solani, and F. oxysporum).
Biological fertilizers can be made either by a single microorganism or a mixture of them. Results would be better if applying single microorganism which shows simultaneous mechanisms to promote plant growth, e.g., simultaneous capability of phosphate solubilization and biological control of filamentous fungi (Vassilev et al. 2006a), simultaneous ability to solubilize phosphate and biological control of Trichoderma strains (Altomare et al. 1999), simultaneous assimilation of both inorganic and organic nitrogen along with phosphate or other micro- and macro-elements by arbuscular mycorrhiza fungi (AMF) (Hawkins et al. 2000; Smith and Read 2008) have been reported. On the other hand, biofertilizers containing mixed microbial inoculum can promote plant growth through various strategies. These microbial strains are produced in individual fermentation processes and then mixed with each other (De Roy et al. 2014). For instance, the co-application of Penicillium spp. and AMF, Penicillium and Rhizobium spp., AMF with rhizobia, Rhizobium and phosphate solubilizing bacteria, AMF/Rhizobium/phosphate solubilizing fungus can be named, which leads to enhanced growth of cereals (Babana and Antoun 2006; Kucey 1988) and legumes, respectively (Alagawadi and Gaur 1988; Downey and Van Kessel 1990; Rice et al. 2000; Wang et al. 2011).
In some cases, the yield of fertilized plants by biofertilizer containing arbuscular mycorrhiza fungi and free-living bacteria with nitrogen fixing ability or various PGPR was equal to plants which were fertilized with chemicals (Adesemoye et al. 2008; Malusa et al. 2007; Wu et al. 2005; Xavier and Germida 2003). Biofertilizers with several plant growth-promoting mechanisms can obtain more acceptance from farmers and markets who prefer to use multifunctional products and present a product for several purposes, respectively (Vassilev et al. 2006b).
Plant Growth-Promoting Rhizobacteria (PGPR)
Rhizospheric bacteria are divided into three groups according to their interaction with plants, including commensal, parasite, and beneficial association (Rai et al. 2020). In commensalism, bacteria harmlessly colonize on the root surface (Verma et al. 2017). No observable effect is imposed on the physicochemical properties of plants (Beattie 2007). Phytopathogenic rhizobacteria establish a parasitism interaction with host plants through producing phytotoxic substances which adversely affect the physicochemical properties of plants. Beneficial rhizobacteria are considered an available part of the rhizospheric reign. They grow in the vicinity of host plants and stimulate their growth through multifaceted activities like solubilizing the nutrients, fixing atmospheric nitrogen, producing phytohormones and lytic enzymes, stimulating the growth of beneficial microorganisms like mycorrhizae, limiting phytopathogens, acting as biocontrol agents (Franco-Correa et al. 2010), removing phytotoxic substances or alleviating salinity, drought, and flooding stresses (Bashan and De-Bashan 2010; Khalid et al. 2004), thus they are identified as plant growth-promoting rhizobacteria (PGPR).
A few of their characteristics like high adaptability to various environmental conditions, fast growth rate, and considerable ability to degrade an extended spectrum of natural and xenobiotic compounds lead to their successful competition with autochthonous, and especially phytopathogenic microorganisms. Rhizobacteria with aggressive root colonization potential, ability to stimulate plant growth, and biocontrol activities can be considered as PGPR (Vessey 2003).
According to their association with root cells of the plants, PGPR are divided into extracellular plant growth-promoting rhizobacteria (ePGPR) and intracellular plant growth-promoting rhizobacteria (iPGPR) (Martínez-Viveros et al. 2010). ePGPR frequently exist within the rhizoplane or in the spaces between the cells of the root cortex, while iPGPR are exclusively present within the specialized nodular structures of root cells. ePGPR belong to Agrobacterium, Arthrobacter, Azotobacter, Azospirillum, Bacillus, Burkholderia, Caulobacter, Chromobacterium, Erwinia, Flavobacterium, Micrococcus, Pseudomonas, and Serratia genera (Gray and Smith 2005), while iPGPR belong to Frankia, Allorhizobium, Azorhizobium (Azorhizobium caulinodans) (Dreyfus et al. 1988), Bradyrhizobium (Bradyrhizobium japonicum) (Guerinot and Chelm 1984), Mesorhizobium (Mesorhizobium chacoense (Velázquez et al. 2001), Mesorhizobium pluriforium (de Lajudie et al. 1998), Sinorhizobium (Sinorhizobium arboris (Nick et al. 1999), Sinorhizobium fredii (Chen et al. 1988), and Sinorhizobium medicae (Rome et al. 1996)), and Rhizobium (Rhizobium cicero (Nour et al. 1994), Rhizobium etli (Segovia et al. 1993), Rhizobium fredii (Scholla and Elkan 1984), Rhizobium galegae (Lindström 1989), Rhizobium gallicum (Amarger et al. 1997), Rhizobium giardinii (Amarger et al. 1997)) genera.
Fungi
Fungal biofertilizers comprise a single fungus or mixture of fungal strains and through direct or indirect mechanisms improve the growth of plants and yield of crops (Devi et al. 2020). Mycorrhizal hyphae extend into the soil through infecting plants growing in their vicinity and impose their improving effect on plant growth by penetrating nutrient depletion zone and increasing bioavailability or mobility of elements (Chiariello et al. 1982).
A mycorrhiza, a fungal distinct morphological structure, generates mutualistic association with roots of host plants like herbs, shrubs, trees, aquatic, xerophytes, epiphytes, hydrophytes, many crops, and forest tree species (Rai et al. 2013). In this association, roots of host plants are intracellularly or extracellularly colonized, either by endomycorrhizal fungi or ectomycorrhizal fungi, respectively. Applying biofertilizers containing mycorrhizal fungi probably results in carbon storage in soil via altering kinetic properties of the root, improving its ability to uptake nutrients which consequently leads to improved quality of soil organic matter to support more agricultural productivity (Smith and Smith 1997).
They are various endomycorrhiza, they are categorized into arbuscular, ericoid, arbutoid, monotropoid, and orchid mycorrhizae. Arbuscular mycorrhizal (AM) fungi are frequent in the terrestrial ecosystem from the arctic to the tropics (Gerdemann 1968). Studies have shown their high occurrence in symbiotic association. They possess high diversity due to the diversity of plant species, soil characteristics, and seasonal conditions (Smith and Smith 2012). They belong to the Glomeromycota phylum (Schuessler et al. 2001). Gerdemannia, Acaulospora, Scutellospora, Entrophospora, Gigaspora, Glomus, Archaeospora, Geosiphon, Paraglomus, and Sclerocystisare AM forming genera. After arbuscular mycorrhiza colonization on the root cortex, highly branched structures like arbuscules are formed inside the cells where nutrient exchange occurs between plant and fungus (Balestrini et al. 2015).
Fungi alleviate biotic stresses like parasitic fungi and nematodes (Duchesne et al. 1989) and abiotic stresses due to drought, salinity, and flooding and enhance the resistance of plants against heavy metals, promote plant productivity and agricultural productivity mainly in low-nutrient and stressful conditions through mobilizing P, supplying macro and micronutrients like P, Ca, Zn, S, N which are inaccessible to plant roots (Augé et al. 2015; Meier et al. 2015; Porcel et al. 2012; Rana et al. 2019a; Sharma et al. 2019). It has been revealed that AM symbiosis induces the expression of Pi transporters in plants (Walder and van der Heijden 2015; Xie et al. 2013). Fungal hyphae have a higher penetration ability than plant roots which able them to obtain nutrients which are away from plant roots. In turn, plants supply carbohydrates for AM fungi (Allen 2011).
Trees with ectomycorrhizal (ECM) fungi inoculated roots due to rapid absorbing and accumulating nitrogen, phosphorus, potassium, and calcium show better growth parameters than nonmycorrhizal plants. These fungi accelerate the degradation of the complicated minerals and organic matter in the soil and their transmission to the tree. Also, they enhance the tolerance of trees to biotic and abiotic stress including, drought, high temperatures, extreme pH of the soil, and toxins. Pisolithus tinctorius and Piriformospora indica are ECM fungi with multifaceted plant growth-promoting activities (Schwartz et al. 2006). There are many fungal biofertilizers such as fungal species which exert their plant growth improving effects through solubilizing phosphorous (Aspergillus spp., A. tubingensis, Penicillium spp., Fusarium spp., Trichoderma spp., Mucor spp., Tritirachium spp., and Candida spp.), solubilizing potassium (Aspergillusfumigates, A. niger, A. terreus, and ectomycorrhizal fungi), solubilizing zinc (Saccharomyces spp., Oidiodendron maius and Aspergillus niger, Penicillium simplicissimum), mobilizing phosphate (ectomycorrhiza and Arbuscular mycorrhiza), and enriching compost (Trichoderma spp., Penicillium spp., Aspergillus spp., Pleurotus spp., Chaetomium spp., Humicola fuscoatra, and Fusarium spp.) (Lian et al. 2008; Whitelaw 2000; Raj 2007).
Cyanobacteria
Biofertilizers containing microalgae, especially cyanobacteria promote plant growth and soil condition via various strategies. They improve the nutrient quantity of soil through secreting phytohormones like auxin (Nostoc, Hapalosiphon), gibberellin, vitamins like vitamin B12 (Cylindrospermum sp. Tolypothrix tenuis, Nostoc muscorum, and Hapalosiphon fontinalis), amino acids (Rodríguez et al. 2006a, 2006b; Roger and Pierre-Adrien 1982), fixing nitrogen and releasing nutrients after their death and decomposition. Anabaena azollae with lignolysis ability release phenolic compounds once applyied as biofertilizer. Nostoc linkia, Anabaena variabilis, Aulosira fertilisima, Calothrix sp., Tolypothrix sp., and Scytonema sp. are nitrogen-fixing cyanobacteria, which can be utilized for rice cultivation (Prasad and Prasad 2001). Anabaena fixes nitrogen (up to 60 kg/ha/season) in association with water fern Azolla and enhances organic matter content in the soils (Moore 1969).
Cyanobacteria contain considerable amounts of macro and micronutrients, as well as amino acids. They can be considered as a suitable alternative for chemical fertilizers to alleviate their environmental polluting effects (MM 2001). Algae via producing organic acids can increase the bioavailability of soil phosphate. The physicochemical properties of soil can be improved via algal biofertilizers. They enhance water holding capacity and aeration of soils through their jelly structure and filamentous structure, respectively. Soil salinity is reduced after their application. They can act as viable biocontrol agents by preventing the growth of weeds. Since cyanobacteria are capable of degrading various kinds of pollutants and possess simple growth requirements, they can be applied to rehabilitate deteriorated ecosystems (Subramanian 1996).
14.2.3.2 Biofertilizer’s Mechanism of Action
As mentioned, microbial cells in biofertilizers improve plant growth via various mechanisms which will be discussed hereafter (Tables 14.2, 14.3, and 14.4) and (Fig. 14.6) also summarized these mechanisms.
14.3 Making Nutrient Available for Plants
Biofertilizers augment plant growth through enhancing the bioavailability of nutrients in the rhizospheric regions gradually. They increase nutrient availability and prevent nutrient leaching out via fixing nitrogen, solubilizing phosphate, potassium, and zinc and producing siderophores as well as decompose organic material (Prasad et al. 2021).
14.3.1 Fixation of Nitrogen
Nitrogen is a critical macronutrient for plant growth and productivity, which plants require to construct macromolecules like proteins and nucleic acid. Most portion of nitrogen (78%) exists in the atmosphere as N2 which is an unavailable form for plant assimilation. N2 should be converted to bioavailable organic form (ammonia) to compensate the loss of N from soils or ecosystems by a well-known process known as biological nitrogen fixation (Tairo and Ndakidemi 2013). This process, exclusively, can be performed by nitrogen-fixing organisms, also known as diazotrophs, including bacteria and cyanobacteria through an oxygen-sensitive enzymatic complex known as nitrogenase system (Rana et al. 2020; Smith and Newton 2013). A considerable amount of ammonia (2.5 × 1011 kg) is annually produced through this system (Schlesinger and Bernhardt 2013). The amount of biologically fixed nitrogen can be affected by environmental conditions or different plant-microbe combinations. Biological fixation of nitrogen tremendously declines volatilization, leaching, and denitrification process. Biological nitrogen fixation can be done via free-living and symbiotic microorganisms. Some nitrogen-fixing microorganisms possess intimate endophytic associations with host plants and some nitrogen fixers, who live in close association in the rhizospheric region, and do not form intimate endophytic symbioses.
The nitrogen fixing ability of Rhizobia species like Rhizobium, Allorhizobium Sinorhizobium, Bradyrhizobium, Azorhizobium, and Mesorhizobium), as endophytes of leguminous plants, have been extensively studied (Gopalakrishnan et al. 2015; Laranjo and Oliveira 2014; Rana et al. 2019b). N2-fixing endophytes are highly found in the legume class, but are not restricted to this class (Carvalho et al. 2014). Recently, many investigates have reported the isolation of endophytes from various non-leguminous plants. Restriction of a specific compartment has not been observed in the endophytes of non-legumes. It has been observed that they colonize in various parts of plants, including, roots, stems, and leaves. The obligative or facultative association among these microorganisms and host plants can be created. The stomata or cracks at the site of lateral root emergence are sites through which these microorganisms can enter into various tissues of plants (Glick 2015; Gaiero et al. 2013). Entering endophytes into the plant's tissues caused a more favorable environment for the plant in the rhizospheric region (Reinhold-Hurek 2011). Since, they easily access to nutritional elements and low concentration of oxygen needed for nitrogenase activity. In return, the endophytes encourage the productivity of the host plants by fixing nitrogen and supplying compounds with growth-promoting activity. In recent years, the number of identified endophytic diazotrophs has been significantly enhanced. Various bacteria belonging to different genera, such as Pseudomonas, Azospirillum, Azotobacter, Klebsiella, Enterobacter, Alcaligenes, Arthrobacter, Burkholderia, Bacillus, and Serratia, have been reported to augment the growth of plants via various strategies (Glick 2015)
Nitrogen-fixing microorganisms can be either symbiotic or non-symbiotic. Symbiotic microorganisms (Rhizobium, Frankia, and Azolla) form a symbiotic relationship with leguminous and non-leguminous plants (Ahemad 2010; Glick 2015), while asymbiotic nitrogen fixers are free-living (Azotobacter, Beijerinckia) or endophytic (Gluconacetobacter, Azospirillum, and Herbaspirillum) microorganisms (Bhattacharyya and Jha 2012). There are many nitrogen-fixing microorganisms including Achromobacter, Alcaligenes, Arthrobacter, Acetobacter, Azomonas, Beijerinckia, Bacillus, Clostridium, Enterobacter, Erwinia, Derxia, Desulfovibrio, Corynebacterium, Campylobacter, Herbaspirillum, Klebsiella, Lignobacter, Mycobacterium, Rhodospirillum, Rhodopseudomonas, Xanthobacter, Mycobacterium, and Methylosinus which are associated with non-legumes(Wani 1990).
Some symbiotic bacteria with nitrogen fixing ability have been extensively studied, which includes Rhizobia, Bradyrhizobium, and Frankia. A large portion (70–80%) of biological fixation of nitrogen is performed by symbiotic microorganisms (Ishizuka 1992). Below are the descriptions of some symbiotic nitrogen fixers.
14.3.1.1 Rhizobium
Rhizobium is the best-known group of microorganisms which via symbiotic relationship with legume crops fixes nitrogen (50–100 kg/ha) and belongs to Rhizobiaceae family which consists of Allorhizobium, Azorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium, Sinorhizobium, Devosia, Methylobacterium, Ochrobactrum, and Phyllobacterium, Burkholderia, and Cupriavidus genera. Commercial rhizobial fertilizers, for legume crops, were first introduced in the 1890s. Rhizobium is an aerobic, non-sporulating, Gram-negative, rod-shaped, and fast-growing bacterium which forms nodules in the leguminous plant (Allito and Alemneh 2014; Lindström et al. 2006; Lindström and Martinez-Romero 2007).
Plant roots attract the rhizobia via their exudates. They colonize the roots of leguminous plants. An infection thread passes the root cortex toward a cluster of dividing cells that will become a plant root primordium. In this symbiotic relationship, the plant produces flavonoids that induce rhizobial nod genes and subsequently signal nodulation through the expression of nod, nol, and noe genes, leading to nodule formation, wherein nitrogen is biologically fixed. Besides N2-fixing activity, rhizobia augment plant growth through mobilizing inorganic and organic P. In selecting biofertilizers, the high ability of their strains to fix nitrogen and compete with phytopathogens microorganisms should be considered. Under unfavorable conditions (acidic or basic soil) in which the population of symbiotic rhizobia is low (100 rhizobia per gram of soil), inoculation with compatible rhizobia is likely to prove highly advantageous. While in the presence of high densities of the rhizobial population, the inoculation is likely to be unnecessary, and investment in inoculation practice might be wasted (Abdel-Lateif et al. 2013; Abiala et al. 2013).
14.3.1.2 Bradyrhizobium
One important group of the symbiotic nitrogen fixers is Bradyrhizobium. They are slow-growing soil-dwelling microorganisms which fix nitrogen, and in turn, use carbohydrate derived from plants in a symbiotic association. It has been shown that nodule formation and availability of nutrients in the soil can be enhanced once the application of inoculum consists of Bradyrhizobium and certain PGPRs probably due to auxins and siderophores production which consequently promote plant growth and increase its tolerance to the phytopathogens (Youssef and Eissa 2014).
14.3.1.3 Frankia
Many commercial drugs are derived from these bacteria. Recent investigations have revealed the significant importance of actinobacteria in producing medically (Salimi et al. 2018a, b, 2019), industrially (Imanparast et al. 2018), and agriculturally important compounds or enzymes (Hamedi and Mohammadipanah 2015). One of these outstanding genera is Frankia. Frankia, a N2-fixing actinobacteria, fix nitrogen via nodulation of actinorhizal plants (more than 280 species of woody plants) including the Elaeagnaceae, Casuarinaceae, Datisticaceae, Coriariaceae, and Myricaceae families, whereas nodulation occurs occasionally in Betulaceae, Rhamnaceae, and Rosaceae (Benson and Clawson 2000). These plants are woody trees or shrubs except for Datisca and can impose a pivotal role in agroforestry and land reclamation. The Frankia genus belongs to the family Frankiaceae. These bacteria produce differentiated structures, vesicles, where nitrogen is biologically fixed. Some parameters like the age of the microbial inoculum, its concentration, and preservation strategy may greatly affect inoculum efficiency.
Plant survival and performance can be improved through inoculation and nodulation before seedling transplanting (Prat 1992). They infect host plants through two various strategies: intracellular and intercellular root invasion (Wall and Berry 2007). Earlier occurs via the signal exchange between Frankia and the host plant which results in root curling and invagination of Frankia growing filaments into them and their subsequent encapsulation by a cell wall deposit. Besides nitrogen fixation, Frankia via releasing plant growth regulators, hydrogen cyanide, siderophores or increasing availability of phosphate improves plant growth. Frankia inoculum can be preserved as lyophilized or frozen in glycerol (Fontaine et al. 1986; Franche et al. 2009).
14.3.1.4 Gluconoacetobacter Diazotrophicus
Gluconoacetobacter diazotrophicus also known as Acetobacter diazotrophicus, fixes nitrogen in a symbiotic association with sugarcane as the host plant. It belongs to the Acetobacteriaceae family. Its inoculation leads to cut off chemical N fertilizer usage for at least two successive years (Muthukumarasamy et al. 2002).
14.3.1.5 Cyanobacteria and Azolla
Nitrogen can be fixed in plant roots via associate interaction by heterocystous cyanobacteria, including Nostoc and Anabaena. A significant amount of nitrogen (36% of global N2 fixation) is symbiotically fixed via an aquatic cyanobacterium, Trichodesmium (Gallon 2001). Cyanobacterial nitrogen fixation in heterocysts fulfills the nitrogen requirement of plants, and in turn, the plant supply carbohydrates derived from their photosynthetic activity. Asymbiotic association can be generated among cyanobacteria and fungi, liverworts, ferns, as well as flowering plants (Roychowdhury et al. 2014). Until the end of the 1970s, symbiosis of Azolla–Anabaena was the crucial nitrogen source to cultivate rice in China. Also, it can serve as an applicable source of nitrogen. It imposes its growth-promoting on plants via producing phytohormones like auxin, indole acetic acid, and gibberellic acid and providing a considerable level of iron, zinc, phosphorus, potassium, molybdenum, and other micronutrients. It has been reported inhibitory effects of three cyanobacteria including Anabaena oryzae, Nostoc calcicola, and Spirulina sp. on galls and egg masses (Al Abboud and Alawlaqi 2014; Mishra et al. 2013).
The effect of microorganisms, that non-symbiotically fix nitrogen, on agricultural productivity and yield is tremendous. Non-symbiotic nitrogen fixers compensate their access to plant derived nutrients decreasing their distance from the host (rhizoplane) or entering into the plants (endophytes). Azotobacter sp., Azospirillum, Azoarcus sp., Gluconacetobacter diazotrophicus, Herbaspirillium sp., Achromobacter, Acetobacter, Alcaligenes, Arthrobacter, Azospirillum, Azomonas, Bacillus, Beijerinckia, Clostridium, Corynebacterium, Derxia, Enterobacter, Klebsiella, Pseudomonas, Rhodospirillum, Rhodopseudomonas, and Xanthobacter are non-symbiotic nitrogen fixers (Saxena and Tilak 1998). In the following, some of these non-symbiotic nitrogen fixers are presented in detail.
14.3.1.6 Azotobacter
Free-living microorganisms like Azotobacter, Clostridium, Rhodospirillum, and Klebsiella which are known as asymbiotic nitrogen fixers are present in the rhizospheric region. Azotobacter, as a well-known asymbiotic nitrogen fixer belongs to the family Azotobacteriaceae, establishes a mutual relationship with plants in which they fix nitrogen and absorb organic compounds from plant exudate. It has been reported that Azotobacter through producing and releasing vitamin B and various plant hormones like gibberellins, naphthalene acetic acid (NAA), promotes root growth and minerals uptake and simultaneously inhibits root pathogens (Mathivanan et al. 2015). The Azotobacter has been found in the rhizospheric region of some crop plants like vegetables, sugarcane, rice, maize, bajra, and plantation crops. A.chroococcum, via multiple mechanisms other than nitrogen fixation like production of vitamin, growth substance, antifungals, and siderophore (Martinez-Toledo et al. 1988), promotes plant growth. Azotobacter indicum through producing a lot of antifungal compounds inhibits some pathogenic fungi in the rhizosphere hence considerably decreases the seedling mortality (Martin et al. 2011). Occurrence of Azotobacters has been reported in soils with neutral or alkaline pH. A. chroococcum is a common species in arid soils. Other reported species include A. vinelandii, A. beijerinckii, A. insignis, and A. macrocytogenes. A sizable proportion of root colonized Azotobacter penetrates the root tissues and lives in an associate relationship with the host plants. However, any visible nodules or outgrowth on root tissue is not created (Bhat et al. 2015).
14.3.1.7 Azospirillum
Azospirillum with ten species including A. lipoferum, A. brasilense, A. amazonense, A. halopraeferens, A. irakense, A. largimobile, A. doebereinerae, A. oryzae, and A. melinis is one of the non-symbiont nitrogen-fixing bacterial genus (20–40 kg/ha) (non-nodule forming bacteria), belong to the Spirilaceae family and colonizes a great variety of annual and perennial plants (Mehnaz 2015). In these microorganisms, nitrogen fixation occurs under microaerophilic conditions. These bacteria have an interrelationship with roots of corn, wheat, sorghum, and other grasses (Montañez et al. 2012) especially plant with C4 dicarboxylic pathway of photosynthesis which their growth and nitrogen fixation occurs in the presence of the aspartic and malic acid as well as the organic salts (Mishra and Dash 2014). It seems that Azospirillum is not limited to a specific plant and can be considered as a general root colonizer; therefore, they are suitable for pearl millet, sorghum, maize, sugarcane, etc. Azospirillum can increase the growth of different crops including, sunflower, carrot, oak, sugarbeet, tomato, eggplant, pepper, cotton, wheat, and rice due to fixing nitrogen, as well as producing growth-promoting compounds including, IAA, gibberellins, and cytokinin by which development of root and nutrient (N, P, and K) uptake are enhanced. It has been shown that maize inoculation with A. brasilense sp. 245 enhanced the production of various phytohormones which had been led to a substantial enhancement of maize growth. It has been shown that commercial production and field application of Azospirillumis simple. Its inoculum can be cost effectively produced and applied as peat formulation (Steenhoudt and Vanderleyden 2000).
14.3.1.8 Nitrogen-Fixing Endophytes
There is increasing evidence which proves the presence of endophytic nitrogen-fixing bacteria (108 CFU per g of dry weight). They cause no disease and damage. Nitrogen-fixing endophytes are bacteria belonging to Azoarcus, Gluconacetobacter, and Herbaspirillum genera. These bacteria successfully multiply and spread within plant tissues (Rana et al. 2019c). They colonize on the root cortex of host plants like rhizospheric bacteria. Then, using hydrolytic enzymes, they penetrate endodermis to colonize the steel, from which they may be subsequently translocated to the aerial parts, and in turn, will systemically spread in xylem vessels and shoots. Endophytic diazotrophs colonize the apoplast, like the intercellular spaces, the xylem vessels, and lignified xylem parenchyma, as well as dead cells, such as those comprising lysigenous aerenchyma in rice and kallar grass. G.diazotrophicus and H. frisingense are some examples of endophytic nitrogen-fixing bacteria in sugar cane and C4- gramineous plant Miscanthus sinensis, respectively (Franche et al. 2009). Azoarcus, is also an endophytic nitrogen fixer, which can enter into the host plant (Leptochloa fusca L Kunth) and live endophytically. Biofertilizer containing Azoarcus can efficiently be used under salinity stress in soils with low fertility.
14.3.2 Phosphate Solubilizing Activity
Phosphate is the second indispensable macronutrient for growing plants. The low frequency of its soluble form limits the growth of terrestrial plants that require phosphate to synthesize macromolecules and perform the transfer of energy, respiration, photosynthesis, and signal transduction (Hesham et al. 2021; Khan et al. 2010; Subrahmanyam et al. 2020). Phosphate abundance is 400–1200 mg kg−1 of soil. Phosphate application can deeply affect crop yield due to its fundamental role in the growth and reproduction processes of plants. In general, chemical phosphatic fertilizers are applied to supply phosphates to the soil. Studies have shown that a low portion of phosphatic fertilizers (30–35%) is utilized by the plants, while its significant portion (65–70%) is turned into insoluble, immobilized, or precipitated forms and consequently unavailable to the plants. Therefore, available phosphate is less than plant requirement (Angus 2012). Aluminum and iron phosphates, as well as calcium phosphates, are most of the insoluble phosphate forms in acidic and alkaline soils, respectively. The insoluble forms are found as inorganic material like apatite or organic forms such as phosphomonoesters, phosphotriesters, and inositol phosphate (Mahdi et al. 2012). The abundance of phosphate in soluble form is usually very negligible (1 ppm) (Goldstein 1994).
Monobasic phosphoric acid (HPO42−)] and dibasic [dihydrogen phosphate (H2PO4−)] are less frequent, soluble, and bioavailable forms of phosphate in the soil. Insoluble phosphate compounds (both organic and inorganic) should be converted to bioavailable form to avoid continuous usage of phosphate chemical fertilizer and its degrading effect on the ecosystem and also to elevate agricultural yields in soils with less bioavailable phosphorous. This crucial requirement can be provided using a biofertilizer containing phosphate solubilizing microorganisms (Rodríguez et al. 2006a, 2006b). Acidification of soil via producing low molecular weight organic acids like glycolic acid, citric acids, gluconic acid, 2-ketogluconic acid, malonic acid, oxalic acid, succinic acid, and propionic acid which make inorganic phosphorus into their soluble form occur by the activity of these bacteria. They play a crucial role in providing phosphorus to the plants. Hydroxyl and carboxyl groups are existing organic acids with low molecular weight. They can chelate the cations bound to phosphate and convert insoluble phosphorous to its bioavailable form (Glick 2012).
Phosphate solubilizing bacteria belong to various genera including, Pseudomonas, Bacillus, Rhizobium, Burkholderia, Achromobacter, Agrobacterium, Micrococcus, Acetobacter, Flavobacterium, Arthrobacter, Enterobacter, Beijerinckia, Microbacterium, Rhizobium, Mesorhizobium, Flavobacterium, Rhodococcus, Serratia, Phyllobacterium, and Erwiniacansolubilize insoluble and inorganic phosphate compounds such as rock phosphate, dicalcium phosphate, tricalcium phosphate, hydroxyl apatite (Goldstein 1986; Otieno et al. 2015; Rodriguez and Fraga 1999a). Higher frequency of bacteria with phosphate solubilizing activity is commonly found in the rhizospheric regions in comparison with nonrhizosphere soil due to a higher amount of organic substrates in rhizospheres which attract phosphate solubilizing bacteria (PSB) (Youssef and Eissa 2014). In addition, PSB augment the growth of plants via inducing biological nitrogen fixation by nitrogen-fixing microbial cells (Mohammadi and Sohrabi 2012).
Also, various P containing organic substances can be applied as a promising P resource for requirements of plants after mineralization process where organic P is hydrolyzed to its inorganic form by means of enzymes like phosphatase (phosphohydrolases) (Rodriguez and Fraga 1999), phytase (Richardson 1997), phosphonoacetate hydrolase (McGrath et al. 1998), d-α-glycerophosphatase (Skraly and Cameron 1998), and C-P lyase (Ohtake et al. 1998). A considerable level of acid phosphatases is created by rhizospheric microorganisms like bacteria belong to Rhizobium (Abd-Alla 1994), Enterobacter, Serratia, Citrobacter, Proteus, and Klebsiella (Thaller et al. 1995), as well as Pseudomonas (Gügi et al. 1991) and Bacillus genera (McComb et al. 2013).
14.3.3 Potassium Solubilizing Activity
Potassium (K) is the third essential element necessary for the growth of plants. Orthoclase, mica, illite, and muscovite are the insoluble source of K in soil. Soluble potassium exists in very low concentration in the soil (Parmar and Sindhu 2013; Yadav et al. 2020b). In soluble-potassium limiting conditions, plant growth and production rate significantly declined. To enhance the bioavailability of potassium to plants, a combination of high K containing clay mineral with K solubilizing bacteria can be applied to meet the K requirement of plants in the agricultural industry (Shrivastava et al. 2016). These microorganisms via producing organic substances solubilize potassium, thus enhance the concentration of soluble K in soil solution. Frateuria aurantia, Bacillus edaphicus, Paenibacillus glucanolyticus, Bacillus mucilaginosus, Acidothiobacillus sp., Pseudomonas sp., Burkholderia sp., and Paenibacillus sp. are well-known as potassium mobilizing microorganisms (Prakash and Verma 2016; Priyadharsini and Muthukumar 2016; Raghavendra et al. 2016; Rawat et al. 2016). Also, these microorganisms produce diverse amino acids, compounds with plant growth-promoting activity (IAA and gibberellic acid), and vitamins, by them plant growth and productivity are increased (Dotaniya et al. 2016)
14.3.4 Zinc Solubilization
Zn is one of the crucial elements which is required in low amount. Deficiency of zinc declines the growth and yield of crops. Hence, Zn containing fertilizers, with soluble zinc sulfate (ZnSO4), are currently used. On this matter, applying Zn solubilizers extremely affect the reproduction and quality of crops. The reaction of used zinc fertilizers with soil constituents converts them into bioavailable. Several events, including cation exchange of acidic soil, chemisorption in alkaline soil (Zn-CaCO3) or making a complex with organic ligands immobilize the zinc in soil and decline its abundance in soil. Most well-known biofertilizers contain microorganisms which supply significant macronutrients like nitrogen, phosphate, and potassium, while the unmet need to micronutrient like Zn also negatively affects plant growth, development, and productivity. Therefore, biofertilizers containing Zn solubilizing microorganisms like B. subtilis, Thiobacillus thiooxidans, and Saccharomyces sp. are severely required. It has been shown that better responses can be achieved through co-application of these strains with Zn fertilizers or Zn containing oxides (Zinc oxide, Zinc carbonate, and Zinc sulfide) (Samoon et al. 2010).
14.3.5 Iron Sequestration
Iron is one of the pivotal growth elements for nearly all living organisms, including animals plants, bacteria, and fungi (Rajkumar et al. 2010). In the presence of oxygen, iron mainly presents as ferric iron (Fe3+) and probably generate insoluble hydroxides and oxyhydroxides. Therefore, a large amount of the iron is not in bioavailable form for plant and bacterial assimilation (Rajkumar et al. 2010). The low abundance of bioavailable iron in terrestrial ecosystems creates an extreme competition. Plants frequently produce and excrete water-soluble organic compounds (siderophores) with low molecular weight, that chelate Fe3+ and maintain it in solution. The root surface receives Fe3+ from siderophores and reduces it to Fe2+ and consequently absorbs it. Also, bacteria produce and release siderophores, high-affinity iron chelator, to scavenge iron by the formation of soluble Fe3+complexes. They can be considered as agents with iron solubilizing activity from minerals or organic compounds in iron-limiting conditions (Ahemad and Khan 2011; Rajkumar et al. 2010). They can be categorized into two types including extracellular and intracellular iron chelators. Enterobactin is one of the strongest siderophores (Hider and Kong 2010).
Microbially derived siderophores also can be applied by plants; hence they can augment the growth of plants under iron limited condition. Plants can assimilate iron provided by microbial siderophores via diverse strategies like chelating and releasing iron, direct uptake of siderophores-Fe complexes, or ligand exchange reaction (Thomine and Lanquar 2011). Several isolates belonging to Pseudomonas, Enterobacter, Bacillus, and Rhodococcus genera are siderophore producing microorganisms. Siderophores producing Phyllobacterium strain, Pseudomonas fluorescens C7, and Chryseobacterium sp C138 promote the growth and quality of strawberries and Arabidopsis thaliana, respectively (Parray et al. 2016). More importantly, biofertilizer containing siderophore producing microorganisms like Pseudomonas, Bacillus sp. and Streptomyces can be applied as biological agents for biocontrol. They limit the reproduction and activity of phytopathogens via producing high iron affinity siderophores. Through this mechanism, phytopathogens like Fusarium oxysporum cannot meet their iron requirement, and therefore, their reproduction will be limited (Bashan and De-Bashan 2005; Saraf et al. 2014).
14.3.6 Production of Volatile Organic Compounds
Producing volatile organic compounds (VOCs) is one of the interesting strategies which is applied by biofertilizers to promote plant growth and its resistance towards fungal pathogen and pathogenic nematodes as well as abiotic stresses. Acetoin, 2,3-butanediol cyclohexane, 2-(benzyloxy) ethanamine, benzene, methyl-decane-1-(N-phenylcarbamyl)-2-morpholinocyclohexene, dodecane, benzene(1-methylnonadecyl), 1-chlorooctadecane, tetradecane, 2,6,10-trimethyl, dotriacontane, and 11-decyldocosane are some of these compounds (Effmert et al. 2012; Kanchiswamy et al. 2015; Ryu et al. 2003).
Rhizobacterially-produced VOCs act as signaling molecules to trigger the plant responses and form plant–microbe interactions and elicitor agents of induced systemic resistance (Ryu et al. 2003; Sharifi and Ryu 2016). Reported VOC producing microorganisms are Bacillus subtilis GB03, B. amyloliquefaciens IN937a, Pseudomonas, Serratia, Arthrobacter, and Stenotrophomonas and Enterobacter cloacae JM22. It has been reported that some of these VOC producing microorganisms can promote the growth of Arabidopsis thaliana (Choudhary et al. 2016).
Some rhizospheric microorganisms including Rhizobium, Pseudomonas, Bacillus, and Aeromonas genera can produce hydrogen cyanide (HCN), a bioactive compounds with an adverse effect on the reproduction of phytopathogens or weeds whose usage will protect the host plants (Ahmad et al. 2008; Das et al. 2017; Flury et al. 2017; Nandi et al. 2015; Sivakumar et al. 2012; Zachow et al. 2017). It has been found that HCN production is common in Pseudomonas (88.89%) and Bacillus (50%) genera (Ahmad et al. 2008). Since, produced HCN has no adverse effect on host plants, HCN producing microorganisms can act as biocontrol agents. In most cases, these microorganisms also produce compounds with antibiotic activity or cell wall degrading enzymes which along with HCN can synergistically suppress the growth of phytopathogens. On the other hand, low level of HCN cannot effectively prevent the proliferation of most fungal phytopathogens (Ramette et al. 2006) but can prevent phytopathogens to become resistant (Olanrewaju et al. 2017). HCN impose its toxicity effect due to the inhibitory effect on cytochrome c oxidase and other critical metalloenzymes (Nandi et al. 2017). Recently, it has been revealed that promoting the activity of HCN on the growth of plants is mostly related to its role in increasing the bioavailability of phosphate for the pioneer plants (like French sorrel) living in oligotrophic alpine environments (like granite-based substrate) (Rijavec and Lapanje 2016).
14.3.7 Production of Hydrolytic Enzymes
Many microorganisms can improve plant growth by suppressing the growth of their pathogens. Production of hydrolytic enzymes such as chitinase, glucanase, protease, and cellulase (Suyal et al. 2021; Yadav et al. 2016). Producing hydrolytic enzymes are one of the critical strategies by which microorganisms control pathogen growth (Jadhav and Sayyed 2016; Jadhav et al. 2017). A wide range of polymeric compounds like chitin, proteins, cellulose, and hemicellulose in the cell wall of the targeted phytopathogens can be hydrolyzed via these enzymes (Mabood et al. 2014).
14.3.7.1 Chitinase Production
Chitin is an insoluble unbranched β-1,4-β-linked polymer of N-acetyl-d-glucosamine (C8 H13O5N)n and is the second most plentiful naturally occurring polymer (Huang et al. 2005). Chitinase producing microorganisms can be considered as promising biological control agents and prevent fungal related plant diseases. Chitinase producing fluorescent Pseudomonas and Streptomyces sp. isolates can control ragi blast disease and sheath blight disease in rice, respectively (Chaiharn et al. 2018; Negi et al. 2017). Chitinasescategorized into three classes according to their mode action: β-1,4-N-acetyl-glucosaminidases, endochitinases, and exochitinases. Chitin degradation can be achieved through endochitinases via randomly cleaving at internal sites of chitin micro-fibril orexochitinases via progressive release of diacetylchitobiose in a stepwise manner without releasing monosaccharide or oligosaccharides (Harman et al. 1993; Manocha and Balasubramanian 1994).
14.3.7.2 Glucanase Production
β-1,3-Glucanases-producing microorganisms like Paenibacillus terrae NK3-4 can efficiently degrade another important cell wall component of fungi and yeasts, β-1,3(1,6)-Glucans (Simmons 1994; Yu et al. 2019). This polysaccharide consists of a β-1,3-linked backbone with some branches via β-1,6-linkages. They are classified into two groups, according to their mode of action: sequent removing of glucose residues from non-reducing end or randomly breakdown of linkage at random sites and releasing smaller oligosaccharides can be conducted via exo- or endo-β-1,3-glucanases, respectively. (Jadhav and Sayyed 2016).
14.3.7.3 Cellulase Production
Bacillus cereus, Bacillus subtilis, Bacillus thuringiensis, and Streptomyces sp. can impose their biocontrol activity via degrading the 1,4-β-d-glucosidic bonds in cellulose (Patagundi et al. 2014; Sadeghi et al. 2017). Cellulose consists of β-d-glucose units which are bonded via 1,4-β-linkages. These microorganisms also play a pivotal role in nature through the recycling of this abundant polymer. The rigid, insoluble, crystalline cellulosic microfibrils are formed via abundant intra- and inter-molecular hydrogen bonds. Various hydrolytic enzymes including endoglucanases, exo-glucanases, and β-glucosidases are involved to completely degrade cellulose into β-glucose (Lynd et al. 2002).
14.3.7.4 Protease Production
Protease or proteinase plays a crucial role in degrading the cell wall of phytopathogenic fungi. This enzyme degrades the protein matrix where chitin and/or fibrils of β-glucan (major components of the cell walls) are present. The polymer is hydrolyzed to peptide chains and/or their amino acids by this enzyme. Also, several proteases via inactivating extracellular enzymes of phytopathogenic fungi, suppress their growth (Al-Askar et al. 2015; Jadhav and Sayyed 2016).
14.3.8 Production of Hormones
Phytohormones, plant hormones, are organic substances that affect physiological, biochemical, and morphological characteristics in plants including growth, differentiation, and development of cells, tissues, and organs (Damam et al. 2016; Peleg and Blumwald 2011). These compounds can be considered as chemical signals to communicate cellular activities in higher plants (Voß et al. 2014), and their synthesis is tightly regulated. Some well-known examples are auxins, ethylene, gibberellins, abscisic acid (ABA), and cytokinins, which play a critical role at very low concentrations (<1 mM). They are active in plants in a short period of time and are mainly produced in special parts of the plant and transferred to another part. Since these chemical compounds affect the growth of the plant, they are also recognized as regulators of plant growth. Under stress conditions, plants or their rhizospheric microorganisms produce or modulate phytohormone levels to coordinate various signal transduction pathways and consequently ameliorate the adverse effects of environmental stresses (Kazan 2015).
Microbial produced phytohormones are known as exogenous phytohormones. Microbial production of plant hormones such as auxin and cytokinins are reported by a lot of rhizospheric microorganisms (Ahemad and Khan 2011). Also, phytohormones improve defense response of plants through stimulating cell division, extension, differentiation, photosynthesis, and pigment formation, inducing seed and tuber germination, increasing the development rate of xylem and root (Gupta et al. 2015; Ljung 2013; Spaepen and Vanderleyden 2011). Azospirillum is a well-known plant growth-promoting bacterium with the ability to excrete phytohormones including gibberellins, cytokinins, and auxins (Tien et al. 1979).
Root surface area and its length can be enhanced by microbial IAA, which enables the plant to achieve more nutrients from the soil (Ahemad and Khan 2012b). The plant cell wall is affected by rhizobacterial IAA and its loosening lead to facilitated exudation of plant exudates, which assure sufficient bacterial growth (Ahemad and Khan 2012a). Inoculating auxin-synthesizing Bacillus spp. positively affects the growth of Solanum tuberosum (Ahmed 2010). Seed germination, floral induction, development of flower and fruit, and growth of leaf and steam are affected by another pivotal phytohormone, gibberellin. Gibberellin-producing Sphingomonas sp. LK11 positively affects plant growth characters (Khan et al. 2014). It has been reported that cytokinin-producing Bacillus subtilis strains caused draught resistance of inoculated plants. It has been shown that Bacillus amyloliquefaciens RWL-1, an endophyte, synthesize ABA. Hence, it has the ability to enhance the salinity tolerance of Oryza sativa. Biofertilizers containing phytohormone producing or modulating microorganisms can offer economic and ecological advantages to boost agricultural production (Shahzad et al. 2017).
Ethylene is a significant phytohormone that affects the ripening of fruits and the abscission of leaves (Reid 1981). Elevated level of aminocyclopropane-1-carboxylate (ACC) synthesis, that is, the precursor of ethylene, is observed in plants under stress conditions like low temperature, drought, flooding, infections with pathogens, and the presence of heavy metals which creates physical or chemical perturbation in various tissues of plants (Li and Glick 2005), and for this reason, wounding hormone is its other name (Salisbury 1992). Increased level of ethylene halts the growth of stem and root, fixation of nitrogen in legumes, and causes premature senescence and consequently decreases the yield. In this regard, there are some rhizospheric microorganisms which produce aminocyclopropane-1-carboxylate deaminase, a pyridoxal phosphate-dependent enzyme. This enzyme can hydrolyze the precursor of ethylene, ACC, to ammonia and α-ketobutyrate then use them as nitrogen and carbon sources. Therefore, ACC deaminase producing microorganisms via reducing the level of ethylene precursor, ACC, improve the growth of plants in the presence of biotic and abiotic stresses (Glick 2014). So, plant growth-promoting microorganism’s ability to hydrolyze ACC possesses profound significance in declining the adverse effect of environmental stressors.
Synthesis of this enzyme is induced in the presence of ACC. ACC deaminase is encoded by AcdS gene which is found in Actinobacteria, Deinococcus-Thermus, three classes of α, β, and γ Proteobacteria, various fungi belonging to Ascomycota and Basidiomycota, and in some Stramenopiles (Nascimento et al. 2014). Of possessing microorganisms, different bacteria (Alcaligenes sp., Bacillus pumilus, Pseudomonas sp., and Variovorax paradoxus, as well as Azoarcus, Azorhizobium caulinodans, Azospirillum spp., Gluconacetobacter diazotrophicus, Herbaspirillum spp., Burkholderia vietnamiensis.) and some yeast (Hansenula saturnus and Issatchenkia occidentalis) (Minami et al. 1998; Palmer et al. 2007), as well as fungi (Penicillium citrinum, Trichoderma asperellum, and Phytophthora sojae) (Jia et al. 1999; Singh and Kashyap 2012; Viterbo et al. 2010) and archaea like Pyrococcus horikoshii (Fujino et al. 2004; Singh et al. 2015) can be considered. Also, it has been known that even certain plants like Arabidopsis thaliana (McDonnell et al. 2009) are ACC deaminase producing organisms.
These ACC deaminase producing microorganisms efficiently augment the growth rate, physiological characteristics, and quality of plants, especially in presence of salinity stress. ACC deaminase synthesizing Pseudomonas putida UW4 reduced post-submergence ethylene production. Therefore, it has been concluded that plant response to environmental stressors can be modified by rhizospheric bacteria (Ravanbakhsh et al. 2017). According to other studies, a salt-tolerant bacterium with ACC deaminase activity, Enterobacter sp., was isolated from the rice field and was reported to promote rice seedling growth in salinity stress (Sarkar et al. 2018). In another study, ACC producing endophyte, Pseudomonas migulae 8R6, limited phytoplasma-induced damages, and consequently Flavescence dorée disease in periwinkle (Gamalero et al. 2017).
It has been revealed that a salt-tolerant endophyte SMR20 with the capability to produce ACC deaminase, Brachybacterium paraconglomeratum, isolated from Chlorophytum borivilianum reduced salt stress-induced damage in the host plant and delayed chlorosis and senescence and improved yield. In addition, this bacterium modifies the levels of indole-3-acetic acid and abscisic acid in plants (Barnawal et al. 2016).
14.4 Environmental Stress Relief
Various biotic (bacterial and fungal phytopathogens, pests, and herbivores) and abiotic stresses (hostile conditions of ecosystem like drought, water logging, extreme temperatures, salt stress, oxidative stress, air pollution, heavy metals, pesticides, and unfavorable soil pH) affect plant growth and its productivity during their growth and development which lead to a reduction of agricultural yield (Rastegari et al. 2020a, 2020b; Suman et al. 2016; Yadav et al. 2020a). Reactive oxygen species (ROS) including H2O2, O2−, and OH− radicals are generated in stress conditions and their elevated level created oxidative stress, which consequently imposes its deleterious effect on plants (CH 2018). They can alleviate this oxidative stress through various strategies like producing and accumulating poly-sugars, proline, glycine-betaine, abscisic acid, and up-regulating enzymatic and nonenzymatic antioxidants, like superoxide dismutase, catalase, ascorbate peroxidase, glutathione reductase, ascorbic acid, α-tocopherol, and glutathione (Agami et al. 2016).
In these conditions, plant inoculation by biofertilizers can provide more protection against these stresses through microbial activities, including the release of substances that can improve soil structure, inhibiting the causative agents of biotic stress via modulating phytohormones and inducing systemic resistance (Yang et al. 2009). In addition, beneficial microorganisms can ameliorate the toxic effect of heavy metal on plants through various strategies like binding mechanisms. It has been reported that Pseudomonas putida and Pseudomonas fluorescens alleviate the toxic effect of cadmium contamination on barley plants through their ability to scavenge cadmium ions from soil (Baharlouei et al. 2011).
Microbial induced modifications lead to increased survival and productivity of plants. Some examples have validated the protective effect of biofertilizers, e.g., Azospirillum inoculation enhanced the growth of wheat and faba beans under saline stress. One group of microbial substances which alters the structure of soil, and imposes an improving effect on the growth of plants in the presence of water stress is a microbial polysaccharide. For example, inoculation of sunflower and wheat plants with exopolysaccharide producing Rhizobium sp. and Pantoea agglomerans resulted in better growth parameters in comparison with uninoculated plants. It has been reported that Pseudomonas strains via enhancing the assimilation of Mg2+, K+, and Ca2+, declining uptake of Na+, and enhancing the synthesis of endogenous indole acetic acid have improved asparagus seedling growth and seed germination in presence of water and salt stresses. Several reactive oxygen species generated during water stress cause injury to the photosynthetic mechanisms of the plant (Heidari and Golpayegani 2012). In this regard, biofertilizer containing Pseudomonades, Bacillus lentus, and Azospirillum brasilense through increasing expression of enzymatic antioxidants and enhancing the amount of chlorophyll in leaves ameliorate this stress. Therefore, biological fertilizer can augment the photosynthetic activity of the plant, and improve its physiological properties in presence of unfavorable conditions (Heidari and Golpayegani 2012).
Improving leaf water status, especially in the presence of salt and drought stresses, is another strategy to improve plant growth (Ahmad et al. 2013; Naveed et al. 2014). Biofertilizers via improving stomatal conductance of plant leaf enhance its ability in utilizing water and surviving under drought conditions. Pseudomonas aeruginosa has improved the growth of Vigna radiata plant in drought conditions (Naveed et al. 2014; Sarma and Saikia 2014). It has been demonstrated that Bacillus megaterium and Pantoea agglomerans enhanced the ability of maize roots to absorb water under salinity stress (Gond et al. 2015; Marulanda et al. 2010). Azospirillum brasilense also has enhanced the salt resistance of the jojoba plant rooting (Ahmad et al. 2013; Gonzalez et al. 2015; Naveed et al. 2014)
Biotic stresses impose their deleterious effect on co-evolution, dynamics of population, nutrient cycling in the ecosystem, ecology of natural habitat, and health of horticultural plant (Gusain et al. 2015). Bacillus spp. (like Paenibacillus polymyxa strains B2, B3, and B4, Bacillus amyloliquefaciens strain HYD-B17, B. licheniformis strain HYTAPB18, B. thuringiensis strain HYDGRFB19, P. favisporus strain BKB30, and B. subtilis strain RMPB44) and Pseudomonas sp. Decrease the growth and activity of phytopathogens by their antimicrobial metabolites or competition.
Pseudomonas sp. and rhizobacteria produce antimicrobial compounds and proteins with toxic properties against Gaeumannomyces graminis var. tritici (inducing wheat take-all) and crop insect pests, respectively (Strange and Scott 2005).
Phenazines, phenazine-1-carboxylic acid, phenazine-1-carboxamide, pyrrolnitrin, pyoluteorin, 2,4diacetylphloroglucinol, rhamnolipids, oomycin A, cepaciamide A, ecomycins, viscosinamide, butyrolactones, N-butylbenzene sulfonamide, pyocyanin are antifungal agents produced by Pseudomonas strains also produce antibacterial compounds (pseudomonic acid and azomycin), antitumor antibiotics (cepafungins and FR901463). Karalicine is an antiviral derived from Pseudomonas (Ramadan et al. 2016). Surfactin, iturins, and bacillomycin are antibacterial compounds derived from Bacillus sp. (Wang et al. 2015).
B. cereus UW85 and B. thuringiensis subsp. kurstaki HD-1 can be applied as biological agents to control the damping-off of alfalfa and gypsy moth, respectively (Broderick et al. 2000; Handelsman et al. 1990). Photorhabdus and Xenorhabdus inhibit harmful insects. Pseudomonas sp. and Bacillus subtilis produce siderophores that can be considered as biocontrol agents, which limit fungal pathogens like Fusarium wilt that is produced by Fusarium oxysporum in potato (Haggag et al. 2015).
Tolerance of plants to the attack of herbivores can be elevated by symbiosis with rhizobacteria. It is likely that these bacteria via supplying additional nitrogen make synthesizing cyanogenic defense compounds possible. These synthesized compounds repel leaf-chewing herbivores (Godschalx 2017). Also, chitinases and β-glucanases-producing microorganisms like Sinorhizobium fredii KCC5, Pseudomonas fluorescens LPK2, and Pseudomonas spp. via degrading chitin and β-1,4-N-N-acetylglucosamine inhibit Fusarium udum (causative agent of fusarium wilt), Rhizoctoniasolani, and Phytophthoracapsici (destructive crop pathogens), respectively (Ramadan et al. 2016).
14.5 Factors Influencing the Efficiency of Biofertilizers
One of the considerable properties which has resulted in limited application of biofertilizers is their unpredictable function under different agro-environmental conditions, which may seriously reduce their plant growth promotion potential. There are some less investigated factors including the production process of biofertilizers, interaction of host plant and microbial strains, competition condition of the soil, which involved in this phenomenon (Bashan 1998; Owen et al. 2015). Reducing the unfavorable properties of the biofertilizers and improving the influential factors on biofertilizer efficiency can encourage the farmers to use them. Biofertilization program by selecting strains according to their high root colonization, abundant sporulation, or growth augmentation in pot experiments without considering affecting factors like field conditions can lead to non-conclusive results.
14.5.1 Effect of the Plants on the Efficacy of Biofertilizers
One of the determinant factors on biofertilizer efficiency is the interaction of microbial biofertilizers with plants. Crop species and environmental conditions of the field are two main factors that govern the interaction between microorganisms and plants (Dodd and Ruiz-Lozano 2012). Promoting and inhibitory effects of plants are significantly depending on their phenological growth phase and physiological and nutritional status. These situations directly affect the release of compounds from the roots. These compounds in plant exudates impose quantitative and qualitative modifications in the rhizospheric region due to the growth promotion or inhibition of specific rhizospheric bacterial communities (Dennis et al. 2010; Hartmann et al. 2009; Uren 2000; Van Overbeek and Van Elsas 2008). In P-deficiency, plants stimulate hyphal branching and colonization of AM fungi through releasing inducing chemicals (Akiyama et al. 2002; Akiyama et al. 2005). Genistein, a phenylpropanoid compound, and phenolic acids are influential compounds in root exudates that stimulate AMF root colonization and change soil microbial communities, respectively (Cesco et al. 2010; Qu and Wang 2008).
14.5.2 Effect of Soil Conditions on the Efficacy of Biofertilizers
Another critical factor in successful biofertilizer establishment is the soil in which microbial cell is introduced. Chemical (pH, nutrient content) and physical (texture) properties of soil profoundly affect biofertilizer establishment, colonization, and plant growth-promoting activities (Fierer and Jackson 2006; Girvan et al. 2003; Lauber et al. 2008). Acidic soils have a less diverse microbial community in comparison to neutral soils because of the narrow pH growth tolerance of bacterial taxa (Fierer and Jackson 2006; Rousk et al. 2010). Acaulospora species are exclusive to acidic soils in the tropics. Therefore, broad-range microbial species like Glomus intraradices can assure the efficiency of biofertilizers. Because it has been adapted to an extended range of environmental conditions, especially harsh situations including, unfavorable pH and temperature and less available nutrients (Antunes et al. 2011).
14.5.3 Effect of Interaction of Soil Microorganisms with Autochthonous on the Efficacy of Biofertilizers
Successful fertilization can be achieved by characterizing microorganisms, their activities, and the interrelationship between them and soil particles. However, there is limited knowledge about the ecological interactions of autochthonous soil microorganisms and microorganisms derived biofertilizers (Malusà et al. 2016). Once microbial cells forming biofertilizers are introduced in the soil, they are faced with an extreme competition condition due to the presence of indigenous microorganisms. Therefore, the exact evaluation of ecological interactions among indigenous soil microorganisms and introduced microbial inoculants is so critical in determining the biofertilizer’s efficiency in the short- and long-period of time. For this purpose, various indicators of soil microorganisms, including their biomass, activity, community structure, and diversity should be comprehensively analyzed (Trabelsi and Mhamdi 2013).
It must also be noted that the observed relationships between inhabitant and inoculant microorganisms would depend considerably on the methods used to show the dynamics of terrestrial microbial communities (Trabelsi and Mhamdi 2013). Simultaneous use of metagenomic approaches and culture-dependent methods can lead to the identification of a number of microbial taxa. However, identification of their related function is still very complicated. The evaluation of coding genes of significant enzymes or main genes in the interaction process between the introduced and native microorganisms may help to gain such information.
It has been revealed that diverse taxonomical or functional classes of autochthonous soil microorganisms are affected by complex inoculum through various strategies. Roots colonization of biofertilizers can be achieved through successful competition with indigenous microorganisms. In these competitive conditions, the ability to produce biofilm or having motility can be advantageou for colonizing root and competition. Therefore, to use these beneficial characteristics, a sufficient amount of microbial cells should be present to produce specific chemicals and consequently gain these properties through turning on quorum sensing (Gera and Srivastava 2006). Some of the soil habitants like protozoan grazing, bacterial grazer, fungi, and insects in soil adversely affect biofertilizer efficacy through reducing their number and colonization ability (Finlay 1985). It has been observed that the population of nematodes has been increased after applying biofertilizers (Malusá et al. 2012). Colonization of wheat rhizosphere by Pseudomonas species and Bacillus subtilis was greatly declined by nematode species (e.g., Caenorhabditis elegans, Acrobeloides thornei, and Cruznema sp.) (Knox et al. 2003).
14.5.4 Effect of Farmers’ Practices on the Efficacy of Biofertilizers
Another important factor in biofertilizer efficacy is the overall fertility or nutritional conditions of the soil. Some microbial inocula like Glomus are more mostly found in fertile soils, with a great amount of nutrients (Hayman and Stovold 1979). In most cases, applying a large amount of chemical fertilizers for a long term increases the nitrogen, phosphorus, and/or potassium accumulation in the soil, modifies interaction of plant and microbial cells, and simultaneously imposes adverse effects on colonization, establishment, and activities of soil microbial communities including autochthonous soil microorganisms and biofertilizer microbial cells (Gosling et al. 2006). For example, low levels of AMF colonization have been observed in maize, soybean, and wheat which were grown on chemically fertilized soils (Duan et al. 2010). The genera Scutellospora, Acaulospora, and Gigaspora are more frequent in soils with low level of nutrients (Hartmann 2006; Johnson et al. 2005; Mäder et al. 2002; Oehl et al. 2004). Long-term applications (10 or 90 years) of chemical phosphate fertilizers or irrigation with wastewater result in P-accumulation in the soils, which declined colonization and population of AM fungi (Cheng et al. 2013; Ortega-Larrocea et al. 2001). Moreover, in the presence of sufficient bioavailable nitrogen and phosphate, the growth of AM fungi is more likely suppressed, they show mutualistic symbiosis in soil with sufficient bioavailable nitrogen, along with limited P (Johnson et al. 2010).
Therefore, it has been proposed that to achieve efficient colonization of microbial inoculum and their corresponding activities, the quantity of applied chemical fertilizers must be reduced (by 20–50%) (Adesemoye et al. 2009; Jeffries et al. 2003). It was shown that most efficiencies of biofertilizer, which consists of two strains of Pseudomonas fluorescens on wheat, were achieved when it is applied via 25% of recommended NPK fertilizers dose (Shaharoona et al. 2008).
In most cases, organic fertilizers like manure, compost, stillage, and vermicompost extract stimulated colonization and growth of several microbial communities via plant growth-promoting activities (Canfora et al. 2015; Esperschütz et al. 2007; Toljander et al. 2008). Although some organic fertilizers reduce AMF richness like sewage sludge (Esperschütz et al. 2007; Toljander et al. 2008), application of some agrochemicals such as aliette, ridomil, benomyl, and benlate has some adverse effects on AM fungi development (Sukarno et al. 1996).
14.5.5 Other Factors Affecting the Efficacy of Biofertilizers
It has been shown that colonization and mycorrhiza-mediated nutrient uptake are detrimentally influenced by tillage, monoculture, and intensive agriculture detrimentally (Perron et al. 2001). Method of inoculum application has a significant role in its efficiency (Date 2001; Deaker et al. 2004). To achieve the best results, new machines are developed or existing machines are adapted to efficiently applying various physical forms of biofertilizers in specific conditions, e.g., inoculation of horticultural crops or big trees by liquid biofertilizer containing AMF is performed (Malusà et al. 2016; Malusa and Sas 2009).
Biofertilizers can be introduced through the foliar application, treating seeds, mixing with soil or organic matter like vermicompost, spraying through hydraulic atomization system (Bhattacharjya and Chandra 2013; Świechowski et al. 2012). Each of these strategies has a considerable effect on biofertilizer efficiency.
The number of delivered spores and their efficacy is influenced by water volume and adjuvants (Bailey et al. 2007). According to the possible recovery period of PGPR (30–40 days after inoculation), it has been suggested that it is suitable to repeat biofertilizer inoculation (2–4 times) during the growing season, with an interval of 3–4 weeks (Bashan et al. 1995).
In some cases, the activities of biofertilizers are slower than that of chemical fertilizers. The activity of a biofertilizer depends on various factors including inoculant delivery system, skill of farmers, viability of biofertilizer under adverse climatic, transport condition, and storage management. Generally, developing biofertilizers needs high investment costs. Moreover, occurring mutation during the production process is deemed as a major limitation of biofertilizers. It must also be noted that low awareness of the farmers can cause poor resource generation by the industries (Singh et al. 2016).
14.6 Production Process
As mentioned previously, biofertilizers can have one or more microbial strains. Preparing the microbial inoculum has a considerable effect on the final product efficiency and quality (Bashan et al. 2014; Stephens and Rask 2000). Recently, the application of complex microbial consortia in diverse annual and horticultural crops has attracted more attention due to favorable results on legumes and non-legume plants. For example, rhizobia with arbuscular mycorrhizal fungi (Alagawadi and Gaur 1988), (AMF), Rhizobium and phosphate solubilizing bacteria (Wang et al. 2011), Rhizobium and a phosphorus solubilizing bacteria (Prasad and Chandra 2003), AMF with free-living bacteria with a nitrogen-fixing ability (Adesemoye et al. 2008; Barea et al. 2002) and biofertilizer simultaneously containing AMF and various PGPR for diverse annual and horticultural crops (Malusa et al. 2007) are successful examples of biofertilizer with complex inocula. In selecting strains to prepare a consortium for a biofertilizer, it should be noted that the applied strains not only should not inhibit the growth of each other, but also coapplication of them must lead to higher colonization (Vestergård et al. 2008).
In designing a biofertilizer for a specific agrogeographical condition, adaptation of the microbial cells to ecosystem conditions should be investigated (Malusá et al. 2012; Zoppellari et al. 2014). Along with the selection of suitable and efficient microbial cells, the type of fermentation process which profoundly affects the shelf life of a biofertilizer is also important. In this period, the microbial cells in inoculant should preserve their survival and plant growth-promoting activities at an acceptable level (Bashan et al. 2014). One of the critical involved factors in biofertilizer shelf life is a multistep process, which is called formulation.
A suitable formulation containing additives (Bashan et al. 2014; Herrmann and Lesueur 2013; Malusá et al. 2012) which by protecting microbial cells during storage and transportation enhance their persistence in soil or even improve the microbial cell efficacy using nodulation elicitors (Legume biofertilizers) (Smith and Smith 2012) and colonization and establishment inducing metabolites like strigolactones assures biofertilizer efficiency (Manikandan et al. 2010; Skorupska et al. 2010). It has been shown that biofertilizer in the shape of granular inoculants represents better results under unfavorable conditions of the soil (Rice et al. 2000). Easier distribution of microbial cells in liquid inoculants can lead to their shorter shelf life (Bashan et al. 2014; Date 2001; Stephens and Rask 2000). Encapsulation of PGPR in alginate or other polymers with various compositions and structures was introduced (Vassilev et al. 2005); however, limit industrial application was seen (Bashan et al. 2014; John et al. 2011).
14.7 Fermentation Process
In order to commercialize a biofertilizer, suitable and efficient microbial strains should be selected and characterized. Large-scale production of these strains should be performed and the desired inoculants must be prepared (Sethi and Adhikary 2012). Mass production of microbial cells for biofertilization can be produced through fermentation processes including, submerged fermentation (SmF) and solid state fermentation (SSF) (De Roy et al. 2014).
Selecting a suitable and affordable nutrient medium is an essential prerequisite for a successful biofertilizer production process. Cost-effective substrates like liquid synthetic media, vegetable extracts, soluble sugars, fruit and dairy by-products, and wastewater can be used in submerged fermentation for large-scale production of biofertilizers (Subramaniyam and Vimala 2012). Low-cost substances or even industrial waste like agro-industrial wastes can be used as the substrate to mass production of microbial cells for biological fertilizers through SSF. In this fermentation, microorganisms are grown on solid materials such as sterilized peat or calcinated clay without the presence of free water (Gowthaman et al. 2001). In this strategy, tight contact between microorganisms and agro-industrial wastes provides the highest substrate concentrations for fermentation.
Also, fertilizers can be produced without a complicated formulation process by mixing microbial cells with agricultural by-products. Industrial wastes, like whey, molasses, bagasse, paper pulp, wheat bran, rice, and rice straw, vegetable and fruit wastes can be efficiently applied as low-cost substrates to solubilize insoluble, inorganic, and low-grade phosphate rocks by various fungi in solid state fermentation (Mendes et al. 2015; Pandey et al. 1999). Prepared biofertilizer using agro-industrial waste materials through solid state fermentation can enrich the soil with organic substances, minerals, and bioactive compounds. It has been revealed that a mixture inoculum of bacterial and fungal microorganisms accelerates the mineralization process of solid waste and their action results in the highly nutrient-rich final product (Cariello et al. 2007; Singh et al. 2011).
Agricultural residues which are treated by microorganisms have a significant ability to reinstate fertility and microbial diversity of disturbed soils. Some fermentation parameters, including pH, temperature, and incubation period, should be optimized in a pilot-scale study to achieve the best production yield.
14.8 Biofertilizer Formulation
The formulation process is a crucial multistep approach in commercializing new biofertilizers and directly affects their efficiency, stability, and quality (Bashan et al. 2014). During the formulation process, microbial cells (one or more strains) are mixed with certain carriers which preserve the cells and their activities under not optimized storage conditions (unfavorable temperature and light exposure) (Herrmann and Lesueur 2013). Good formulation assures successful multiplication of microbial cells, extending their shelf life, and enhances their activity to a higher rate after inoculation to the host plants (Arora et al. 2010). Since formulated biofertilizer largely consists of substances as carriers, they significantly affect the success or the failure of the inoculation.
Being non-toxic, non-pollutant, biodegradable, and biocompatible are critical prerequisites of carriers for formulation. They should be stable and preserve microbial survival under harsh conditions, having adjustable pH, sufficient shelf life, fine grinding in order to mix with other constituents (nutrients, adjuvants), and consist of low-priced substances (Catroux et al. 2001; Herrmann and Lesueur 2013). In desirable formulation, controlled release of microorganisms into the soil can be achieved. Also, applying this formulation can be performed via standard seeding machinery (Malusá et al. 2012). Adherence of microbial cells on the seeds can be improved by using adhesive material, which is known as stickers. Organic, inorganic, or synthetic substances can be used as carriers. Generally, they are categorized into four key classes including soils (inorganic soil peat, clays, coal, and lignite), herbal waste (farmyard manure, wheat bran, charcoal, composts, cellulose, soybean meal, soybean and peanut oil, press mud, and corn cobs), inert materials (ground rock phosphate, vermiculite, perlite, bentonite, calcium sulfate, polyacrylamide, and alginate), and lyophilized microbial cultures and old dried bacteria (Bashan 1998).
It is possible that a formulated biofertilizer be made from a mixture of mentioned carriers. Besides, the carriers and stickers, some macro- and micronutrients such as carbon or mineral resources, hormones, and fungicides, which are known as additives may be added during biofertilizer formulation (Arora and Mishra 2016). Additives, like skim milk (Vassilev et al. 1997), xanthan (Lorda et al. 2007), or sodium alginate (Tittabutr et al. 2007) provide nutrient and moisture, as well as inactivate toxic compounds, delay inoculant desiccation and improve its quality, stability, and shelf life (Manikandan et al. 2010).
Five formulations are currently used for biofertilizers, including peat formulations, liquid formulations, granules, and freeze-dried powders as well as the most recent strategy of stabilization (Bashan 1998).
14.8.1 Peat Formulations
Peat is composed of partially decayed vegetation that is accumulated for a long time. Microbial cells can successfully grow on it as a nutrient-enriched and protective environment (Bashan et al. 2014). Used peat in the formulation process should have acceptable content of organic matter and water retaining capacity. They must be free from toxic substances for microorganisms, plants, animals, and humans), should be cost-effective, highly adsorptive, and simply sterilizable. Peat processing steps include drainage, sieving, and drying (~5%). Drying must be performed at the lowest possible temperatures to avoid the release of hazardous compounds. After the drying process, they are passed through a 250-μm sieve, and their pH is adjusted at pH 6.5–7.0 by liming (Roughley 1976). Then sterilization of the prepared peat is conducted, and a sufficient quantity of liquid inoculum is added to the peat to achieve a final moisture content of 40–55%. Microbial inoculated peat is incubated for a period of time to allow bacterial multiplication in the carrier which is known as maturing or curing and has a tremendous effect on bacteria survival during storage and on seeds (Okon and Baker 1987). In order to increase the uniformity of biofertilizer coverage on seed, sticking agents including polymeric materials like polysaccharides (like Arabic gum or carboxymethylcellulose), polyalcohol derivatives, or caseinate salts are incorporated into the peat (Albareda et al. 2008; Stephens and Rask 2000). These adhesive agents should be free from hazardous compounds for plant seed or microorganisms, be dispersible in water, and improve microbial cells' survival rate and adherence to the seeds.
Microbially treated peat is generally applied on-site on the seeds just before sowing. The seed coating by microbial inoculated peats can be performed using cement mixers, and mechanical tumbling machines (Schulz and Thelen 2008). Some peat characters like its undefined and complex content, which are source-dependent, poor controllability on the quantity of microorganisms applied per seed, its costly processing, and probable release of toxic substances during its sterilization interfere in the consistent quality of peat formulations and influence the growth and survival of microbial cells (Bashan et al. 2014; Tittabutr et al. 2007). Extensive use of peat poses an adverse impact on the environment and ecosystem where it has been extracted (John et al. 2011). Cork industry derived compost by better ability in preserving the survival of various microbial cells in rhizospheric soil or on the seeds can be a suitable alternative to peat (up to six months) (Albareda et al. 2008).
14.8.2 Liquid Formulations
Easy handling and application either on seeds or in soil are some of the properties which make liquid formulations popular. These are various types of these formulations including, aqueous (broth cultures), mineral or organic oils, oil in water, or polymer-based suspensions (Herrmann and Lesueur 2013). Its physical form makes adding nutrients and cell protectants, including sucrose, glycerol, and Arabic gum, possible, which can improve its performance (John et al. 2011; Sahu and Brahmaprakash 2016). In comparison to peat formulations, they are easily sterilized, compatible with machinery on large farms, and eventually, these features enhanced their field efficacy (Bashan et al. 2014). Biofertilizer in liquid formulations needs more specific storage conditions (cool temperatures) (Stephens and Rask 2000).
14.8.3 Granule Formulations
Another formulation can be made using marble, calcite, and silica grains. For this purpose, created granules are wetted with an adhesive and coated with the microbial cells (Bashan et al. 2014). To have a high-quality end product, a microbial culture containing suitable microbial cells should be prepared (Herrmann and Lesueur 2013). Being less dusty and easier and controllable handling and application are some of the granule advantages compared to peat formulation, although the bulkier size of granules allows cost-effective transport and storage. To avoid direct contact of microbial cell coated granules with the chemicals or pesticides, they are put in a furrow near to the seed to facilitate lateral root interactions (Bashan et al. 2014; Herrmann and Lesueur 2013). Granular inoculants have more survival rate under unfavorable soil conditions such as soil acidity, moisture stress, or cool, wet soils than other formulations (Rice et al. 2000).
14.8.4 Freeze-Dry Formulations
Biofertilizers can be formulated in shapes of freeze-dried powders using various nontoxic and cost-effective, organic, inorganic, or synthetic carriers (Bashan et al. 2014). These carriers physically or nutritionally through supplying a protective surface or a specific substrate, respectively, provide temporarily niche for microbial cells of biofertilizers in soil. Therefore, they have an enormous significance (Arora et al. 2010). These carriers should have high moisture absorption capability, pH buffering capacity, and being sterilizable to assure delivering the right number of viable cells in good physiological condition (Bashan et al. 2014).
14.8.5 Cell Immobilization Formulations
Cell immobilization is a new promising approach which has also been implemented in the formulation of biofertilizer preparations (Jain et al. 2012; Stockwell et al. 2011). In this approach, microbial cells are attached, entrapped or immobilized into a matrix through various strategies including flocculation, adsorption on surfaces, covalent bonding to carriers, cross-linking of cells, and encapsulation in a natural or synthetic polymer gel-like polysaccharides, a protein material, polyacrylamide and polyurethane (Cassidy et al. 1996). Chemical compounds should have the ability to interact with other constituents for encapsulation. Polyacrylamide and alginate are the two commonly used chemicals in preparing encapsulated biofertilizers. Among these, alginate is a naturally occurring polymer with biodegradability and nontoxic feature. To perform encapsulation using alginate, microbial cells should be dispersed into the alginate solution and the microbial cells incorporated alginate matrix is prepared through dropping mixed solution into cationic solution. Shelf life and inoculation efficacy can be extended via adding nutrients and other additives (Malusá et al. 2012). Then dried beads are packaged (Date 2001). Many strategies including spray drying, solvent extraction/evaporation, coacervation, extrusion, emulsion technique, thermal gelation, pre-gel dissolving methods have been presented to precisely define the size, shape, and texture of the beads (Park and Chang 2000).
Encapsulation through protecting cells (bacteria, fungal spores, or small fragments of hypha) in a nutritive shell against mechanical and environmental stresses (like unfavorable pH, temperature, organic solvent, or toxins), as well as predators, assures biofertilizer efficiency (Bashan 1998; Jain et al. 2012; John et al. 2011) and contamination can be minimized through providing aseptic conditions. PSB encapsulation enhanced their efficiency in P solubilization (Jain et al. 2012). Due to a concentrated situation, low volume, and extended shelf life of encapsulated biofertilizers, their transportation, and storage (room temperatures) are easier than other formulations (John et al. 2011). Once the introduction of the encapsulated microbial cell into the soil occurs, they slowly degrade the capsules, which gradually released into the soil (Bashan 1998). In these regards, smaller beads (microencapsulation) enhance the application efficacy via providing direct contact with seeds (John et al. 2011). High production costs and technical handling are the limitations of this formulation. Gels consist of chemical components like fluidized bed, magnesium silicate, or cellulose-based gel revealed some promise, but none have been adopted on-farm (Jawson et al. 1989).
14.9 Advances in Formulation
It has been revealed that limited formulations cannot meet the need of diverse microorganisms to present new biofertilizers with better efficiency, stability, shelf life, lower cost, easier application, handling, and storage. Therefore, an extended range of materials including organic (water sludge, composts, sawdust, sugarcane bagasse, whey, coal, or enriched agro-industrial residues) and inorganic substances (clays, lapillus, volcanic pumice, or diatomite earth) are being evaluated to develop new carriers (Albareda et al. 2008; Malusá et al. 2012). Some of them have many drawbacks, e.g., sludge wastewater due to the presence of hazardous heavy metals (Malusá et al. 2012).
Various formulated biofertilizers can be applied through different routes. For instance, the seed can be directly inoculated by dry biofertilizers or be soaked with water, then mixed with peat powder (sprinkle method). In another approach, suspended biofertilizer can be added to the seeds and mixed with them (slurry method). Biofertilizer with peat formulation can be suspended in water and sprayed into the furrow during sowing. Moreover, biofertilizer and adhesive can be supplied as slurry to seeds and coated with ground material like lime. Finally, soil can directly be treated by biofertilizers (Bashan 1998).
14.10 Packaging and Quality Control
The nature of the packaging material for biofertilizers can affect its quality. These materials should allow the exchange of oxygen while limiting the water passage. The packaging should minimize biofertilizer contamination during storage and transportation (Roughley 1976). Unfavorable quality and unreliable efficiency under field conditions are the critical factors in biofertilizer failure to gain farmer's acceptance (Herridge 2008; Tarbell and Koske 2007). For example, it has been revealed that 90% of all commercial legume biofertilizers have no practical effect on the legume production yield (Catroux et al. 2001). Contamination is another extensive problem in commercialized biofertilizers. Herrmann and Lesueur (2013) analyzed 65 commercial biofertilizers among which only 37% are containing “pure” and the remaining products (63%) were contaminated with one or more bacterial strains (Herrmann and Lesueur 2013). It has been reported that a significant portion of the commercialized biofertilizers (40%) do not contain pure strains or do not have the claimed strains. Lack of facilities to produce and store high-quality inoculants generates these problems and often leads to inconsistent field results (Bashan 1998). In this regard, systems of quality control are greatly required for ensuring that efficacious biofertilizers are entered into the markets. Quality control and quality assurance systems remove low-quality inoculants from markets. Therefore, consistent results can be obtained in field conditions and better global acceptance can be achieved (Bashan 1998; Bhattacharyya and Jha 2012).
In addition, sufficient information including the name of the microorganisms, guaranteed numbers, nutrients, and other used components content, registration information, lot number, expiry date, dosage and method of application, instructions for disposal, precautions of use of commercialized biofertilizers should be represented on its label to evaluate the quality and the efficacy of a biofertilizer by farmers and make sure to purchase an effective product (Gemell et al. 2005; Husen et al. 2016). Accordingly, there is a great need to educate manufacturing workers and farmers to assure the quality requirements and a successful crop inoculation, respectively. To prepare biofertilizers with a stable and reproducible efficacy under a wide range of field conditions, it should contain pure isolates and contains no opportunistic pathogens for human, animals, and plants and possesses long term shelf life and its microbial cells should be potently propagated under an extended range of environmental condition (Catroux et al. 2001; John et al. 2011; Lupwayi et al. 2006). A list of several commercial biofertilizers is presented in (Table 14.5).
14.11 Conclusion and Future Prospects
Since the emergence of civilization, 10,0000 years ago, increasing the quality and quantity of agricultural products is one of the main concerns of humans. To achieve these goals, chemical fertilizers have been extensively used; however, their unfavorable effects were revealed on ecosystems. Although organic fertilizers have no adverse effect on soil and its organisms, their labor-intensive and time-consuming preparation makes them unsuitable for application on large scale as a commercial approach. Therefore, it needs promising, safe, and commercial alternatives without environmental adverse effects. Biofertilizers can be considered as cost-effective fertilizers that act in an eco-friendly manner without imposing adverse effects on plant growth and terrestrial and aquatic micro- and macro-organisms, improve soil fertility and its texture, and therefore, can flourish agriculture-related industries. But effective large-scale production and storage strategies should be invented and applied to produce biofertilizers that can be resistant and effective in a wide range of environmental conditions like high temperature and aridity.
References
Abd-Alla M (1994) Solubilization of rock phosphates by Rhizobium and Bradyrhizobium. Folia Microbiol 39:53–56
Abdel-Lateif KVV, Gherbi H, Verries C, Meudec E, Perrine-Walker F, Cheynier V, Svistoonoff S, Franche C, Bogusz D, Hocher V (2013) Silencing of the chalcone synthase gene in Casuarina glauca highlights the important role of flavonoids during nodulation. New Phytol 199:1012–1021
Abiala MAPO, Olawuyi OJ, Oyelude JO, Akanmu AO, Killani AS, Osonubi O, Odebode AC (2013) Harnessing the potentials of Vesicular Arbuscular Mycorrhizal (VAM) fungi to plant growth-a review. Int J Pure Appl Sci Technol 14:61
Adesemoye A, Torbert H, Kloepper J (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886
Adesemoye A, Torbert H, Kloepper J (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929
Adesemoye A, Torbert H, Kloepper J (2010) Increased plant uptake of nitrogen from 15 N-depleted fertilizer using plant growth-promoting rhizobacteria. Appl Soil Ecol 46:54–58
Agami RA, Medani RA, Abd El-Mola IA, Taha RS (2016) Exogenous application with plant growth promoting rhizobacteria (PGPR) or proline induces stress tolerance in basil plants (Ocimum basilicum L.) exposed to water stress. Int J Environ Agri Res 2:78
Ahemad MKM (2010) Phosphate solubilizing Enterobacter asburiae strain PS2. Res J Microbiol 5:849–857
Ahemad M, Khan MS (2011) Assessment of plant growth promoting activities of rhizobacterium Pseudomonas putida under insecticide-stress. Microbiol J 1:54–64
Ahemad M, Khan MS (2012b) Effect of fungicides on plant growth promoting activities of phosphate solubilizing Pseudomonas putida isolated from mustard (Brassica compestris) rhizosphere. Chemosphere 86:945–950
Ahemad M, Khan MS (2012a) Ecological assessment of biotoxicity of pesticides towards plant growthpromoting activities of pea (Pisum sativum)-specific rhizobium sp. strainmrp1. Emirates J Food Agric 334–343
Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud University-Sci 26:1–20
Ahmad F, Ahmad I, Khan M (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181
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
Ahmed AHS (2010) Auxin-producing Bacillus sp.: Auxin quantification and effect on the growth of Solanum tuberosum. Pure Appl Chem 82:313–319
Akiyama K, Matsuoka H, Hayashi H (2002) Isolation and identification of a phosphate deficiency-induced C-glycosylflavonoid that stimulates arbuscular mycorrhiza formation in melon roots. Mol Plant Microbe Interact 15:334–340
Akiyama K, Matsuzaki K-i, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824
Al Abboud MA, Alawlaqi MM (2014) Role of biofertilizers in agriculture: a brief review. Mycopath 11
Alagawadi A, Gaur A (1988) Interaction between Azospirillum brasilense and ‘Phosphate Solubilizing Bacteria’ and their influence on yield and nutrient uptake of Sorghum (Sorghum bicolor L.). Zentralblatt für Mikrobiologie 143:637–643
Al-Askar AA, Rashad YM, Hafez EE, Abdulkhair WM, Baka ZA, Ghoneem KM (2015) Characterization of alkaline protease produced by Streptomyces griseorubens E44G and its possibility for controlling Rhizoctonia root rot disease of corn. Biotechnol Biotechnol Equip 29:457–462
Albareda M, Rodríguez-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
Allen MF (2011) Linking water and nutrients through the vadose zone: a fungal interface between the soil and plant systems. J Arid Land 3:155–163
Allito BB, Alemneh AA (2014) Rhizobia strain and host-legume interaction effects on nitrogen fixation and yield of grain legume: a review. Mol Soil Biol
Altomare C, Norvell W, Björkman T, Harman G (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22. Appl Environ Microbiol 65:2926–2933
Amarger N, Macheret V, Laguerre G (1997) Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int J Syst Evol Microbiol 47:996–1006
Angus JF (2012) Fertilizer science and technology. Encyclopedia Sustain Sci Technol 3768–3786
Antunes PM, Koch AM, Morton JB, Rillig MC, Klironomos JN (2011) Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Phytol 189:507–514
Arora NK, Mishra J (2016) Prospecting the roles of metabolites and additives in future bioformulations for sustainable agriculture. Appl Soil Ecol 107:405–407
Arora NK, Khare E, Maheshwari DK (2010) Plant growth promoting rhizobacteria: constraints in bioformulation, commercialization, and future strategies. In: Plant growth and health promoting bacteria. Springer, pp 97–116
Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24
Babana AH, Antoun H (2006) Effect of Tilemsi phosphate rock-solubilizing microorganisms on phosphorus uptake and yield of field-grown wheat (Triticum aestivum L.) in Mali. Plant Soil 287:51–58
Baharlouei J, Pazira E, Solhi M (2011) Evaluation of inoculation of plant growth-promoting Rhizobacteria on cadmium uptake by canola and barley. In: International conference on environmental science and technology IPCBEE. Singapore
Bailey KL, Carisse O, Leggett M, Holloway G, Leggett F, Wolf TM et al (2007) Effect of spraying adjuvants with the biocontrol fungus Microsphaeropsis ochracea at different water volumes on the colonization of apple leaves. Biocontrol Sci Tech 17:1021–1036
Balestrini R, Lumini E, Borriello R, Bianciotto V (2015) Plant-soil biota interactions. Soil Microbiol Ecol Biochem:311–338
Barea J-M, Azcón R, Azcón-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie Van Leeuwenhoek 81:343–351
Barnawal DBN, Tripathi A, Pandey SS, Chanotiya CS, Kalra A (2016) ACC-deaminase-producing endophyte Brachybacterium paraconglomeratum strain SMR20 ameliorates Chlorophytum salinity stress via altering phytohormone generation. J Plant Growth Regul 35:553–564
Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol Adv 16:729–770
Bashan Y, De-Bashan L (2005) Plant growth-promoting. Encyclopedia of soils in the environment 1:103–115
Bashan Y, De-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth—a critical assessment. In: Advances in agronomy, vol 108. Elsevier, pp 77–136
Bashan Y, de-Bashan LE, Prabhu S, Hernandez J-P (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33
Bashan Y, Puente ME, Rodriguez-Mendoza MN, Holguin G, Toledo G, Ferrera-Cerrato R et al. (1995) Soil parameters which affect the survival of Azospirillum brasilense. In: Azospirillum VI and related microorganisms. Springer, pp 441–449
Beattie GA (2007) Plant-associated bacteria: survey, molecular phylogeny, genomics and recent advances. In: Plant-associated bacteria. Springer, pp 1–56
Benson D, Clawson M (2000) Evolution of the actinorhizal plant symbiosis. Prokaryotic nitrogen fixation: a model system for the analysis of a biological process 207–224
Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Fact 13:66
Bhattacharjee R, Dey U (2014) Biofertilizer, a way towards organic agriculture: a review. Afr J Microbiol Res 8:2332–2343
Bhattacharjya S, Chandra R (2013) Effect of inoculation methods of Mesorhizobium ciceri and PGPR in chickpea (Cicer areietinum L.) on symbiotic traits, yields, nutrient uptake and soil properties. Legume Res 36:331–337
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350
Bhat TA, Ahmad L, Ganai MA, Haq S, Khan O (2015) Nitrogen fixing biofertilizers; mechanism and growth promotion: a review. J Pure Appl Microbiol 9:1675–1690
Broderick NA, Goodman RM, Raffa KF, Handelsman J (2000) Synergy between zwittermicin A and Bacillus thuringiensis subsp. kurstaki against gypsy moth (Lepidoptera: Lymantriidae). Environ Entomol 29:101–107
Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124:3–22
Canfora L, Malusa E, Salvati L, Renzi G, Petrarulo M, Benedetti A (2015) Short-term impact of two liquid organic fertilizers on Solanum lycopersicum L. rhizosphere Eubacteria and Archaea diversity. Appl Soil Ecol 88:50–59
Cariello ME, Castañeda L, Riobo I, González J (2007) Inoculante de microorganismos endógenos para acelerar el proceso compostaje de residuos sólidos urbanos. J Soil Sc Plant Nutr 7:2007
Carvalho TL, Balsemão-Pires E, Saraiva RM, Ferreira PC, Hemerly AS (2014) Nitrogen signalling in plant interactions with associative and endophytic diazotrophic bacteria. J Exp Bot 65:5631–5642
Cassidy M, Lee H, Trevors J (1996) Environmental applications of immobilized microbial cells: a review. J Ind Microbiol 16:79–101
Catroux G, Hartmann A, Revellin C (2001) Trends in rhizobial inoculant production and use. Plant Soil 230:21–30
Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329:1–25
CH F (2018) Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environ Exp Bot 154:134–142
Chaiharn M, Sujada N, Pathom-Aree W, Lumyong S (2018) The antagonistic activity of bioactive compound producing streptomyces of fusarium wilt disease and sheath blight disease in rice. Chiang Mai J Sci 45:1680–1698
Chandramohan A, Sivasankar V, Ravichandran C, Sakthivel R (2013) A probe on the status of microorganisms in the air, soil and solid waste samples of Ariyamangalam dumping site at Tiruchirappalli District, South India. In: Microbiological research in agroecosystem management. Springer, pp 1–9
Chen J-H (2006) The combined use of chemical and organic fertilizers and/or biofertilizer for crop growth and soil fertility. In: International workshop on sustained management of the soil-rhizosphere system for efficient crop production and fertilizer use. Citeseer, p 20
Cheng Y, Ishimoto K, Kuriyama Y, Osaki M, Ezawa T (2013) Ninety-year-, but not single, application of phosphorus fertilizer has a major impact on arbuscular mycorrhizal fungal communities. Plant Soil 365:397–407
Chen WXYG, Yan GH, Li JL (1988) Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int J Syst Evol Microbiol 38:392–397
Chiariello N, Hickman JC, Mooney HA (1982) Endomycorrhizal role for interspecific transfer of phosphorus in a community of annual plants. Science 217:941–943
Chislock MF, Doster E, Zitomer RA, Wilson A (2013) Eutrophication: causes, consequences, and controls in aquatic ecosystems. Nat Educ Knowl 4:10
Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP et al (2016) Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stresses. J Plant Growth Regul 35:276–300
Conway G (2012) One billion hungry: can we feed the world? Cornell University Press
Damam M, Kaloori K, Gaddam B, Kausar R (2016) Plant growth promoting substances (phytohormones) produced by rhizobacterial strains isolated from the rhizosphere of medicinal plants. Int J Pharmaceutical Sci Rev Res 37:130–136
Das K, Prasanna R, Saxena AK (2017) Rhizobia: a potential biocontrol agent for soilborne fungal pathogens. Folia Microbiol 62:425–435
Date RA (2001) Advances in inoculant technology: a brief review. Aust J Exp Agric 41:321–325
Deaker R, Roughley RJ, Kennedy IR (2004) Legume seed inoculation technology: a review. Soil Biol Biochem 36:1275–1288
de Lajudie PWA, Nick G, Moreira F, Molouba F, Hoste B, Torck U, Neyra M, Collins MD, Lindström K, Dreyfus B (1998) Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int J Syst Evol Microbiol 48:369–382
Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327
De Roy K, Marzorati M, Van den Abbeele P, Van de Wiele T, Boon N (2014) Synthetic microbial ecosystems: an exciting tool to understand and apply microbial communities. Environ Microbiol 16:1472–1481
Devi R, Kaur T, Kour D, Rana KL, Yadav A, Yadav AN (2020) Beneficial fungal communities from different habitats and their roles in plant growth promotion and soil health. Microbial Biosystems 5:21–47. https://doi.org/10.21608/mb.2020.32802.1016
Dodd IC, Ruiz-Lozano JM (2012) Microbial enhancement of crop resource use efficiency. Curr Opin Biotechnol 23:236–242
Dotaniya ML, Meena VD, Basak BB, Meena RS (2016) Potassium uptake by crops as well as microorganisms. In: Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 267–280
Downey J, Van Kessel C (1990) Dual inoculation of Pisum sativum with Rhizobium leguminosarum and Penicillium bilaji. Biol Fertil Soils 10:194–196
Dreyfus B, Garcia J-L, Gillis M (1988) Characterization of Azorhizobium caulinodans gen. nov., sp. nov., a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata. Int J Syst Evol Microbiol 38:89–98
Duan T, Shen Y, Facelli E, Smith SE, Nan Z (2010) New agricultural practices in the Loess Plateau of China do not reduce colonisation by arbuscular mycorrhizal or root invading fungi and do not carry a yield penalty. Plant Soil 331:265–275
Duchesne L, Peterson R, Ellis B (1989) The future of ectomycorrhizal fungi as biological control agents. Phytoprotection 70:51–57
Effmert U, Kalderás J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703
Esperschütz J, Gattinger A, Mäder P, Schloter M, Fließbach A (2007) Response of soil microbial biomass and community structures to conventional and organic farming systems under identical crop rotations. FEMS Microbiol Ecol 61:26–37
Fageria N, Dos Santos A, Moraes M (2010) Influence of urea and ammonium sulfate on soil acidity indices in lowland rice production. Commun Soil Sci Plant Anal 41:1565–1575
FAO (2010) The state of food insecurity in the world: addressing food insecurity in protracted crises. FAO
FAO/WHO (2015) What is organic agriculture
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci 103:626–631
Finlay R (1985) Interactions between soil micro-arthropods and endomycorrhizal associations of higher plants. Special publications series of the British Ecological Society
Flury P, Vesga P, Péchy-Tarr M, Aellen N, Dennert F, Hofer N et al (2017) Antimicrobial and insecticidal: cyclic lipopeptides and hydrogen cyanide produced by plant-beneficial Pseudomonas strains CHA0, CMR12a, and PCL1391 contribute to insect killing. Front Microbiol 8:100
Fontaine MS, Young PH, Torrey JG (1986) Effects of long-term preservation of Frankia strains on infectivity, effectivity, and in vitro nitrogenase activity. Appl Environ Microbiol 51:694–698
Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59
Franco-Correa M, Quintana A, Duque C, Suarez C, Rodríguez MX, Barea J-M (2010) Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45:209–217
Fricke K, Vogtmann H (1993) Quality of source separated compost. BioCycle (USA)
Fujino A, Ose T, Yao M, Tokiwano T, Honma M, Watanabe N et al (2004) Structural and enzymatic properties of 1-aminocyclopropane-1-carboxylate deaminase homologue from Pyrococcus horikoshii. J Mol Biol 341:999–1013
Gaiero JRMC, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750
Gallon J (2001) N2 fixation in phototrophs: adaptation to a specialized way of life. Plant Soil 230:39–48
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892
Gamalero E, Marzachì C, Galetto L, Veratti F, Massa N, Bona E et al (2017) An 1-Aminocyclopropane-1-carboxylate (ACC) deaminase-expressing endophyte increases plant resistance to flavescence dorée phytoplasma infection. Plant Biosyst Int J Dealing Aspects Plant Biol 151:331–340
Gaur V (2010) Biofertilizer–necessity for sustainability. J Adv Dev 1:7–8
Gemell L, Hartley E, Herridge D (2005) Point-of-sale evaluation of preinoculated and custom-inoculated pasture legume seed. Aust J Exp Agric 45:161–169
Gera C, Srivastava S (2006) Quorum-sensing: the phenomenon of microbial communication. Curr Sci 90:666–676
Gerdemann J (1968) Vesicular-arbuscular mycorrhiza and plant growth. Annu Rev Phytopathol 6:397–418
Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica, https://doi.org/10.6064/2012/963401
Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39
Glick BR (2015) Beneficial plant-bacterial interactions. Springer, Cham
Godschalx AL (2017) Symbiosis with nitrogen-fixing rhizobia influences plant defense strategy and plant-predator interactions. Portland State University
Goldstein AH (1986) Bacterial solubilization of mineral phosphates: historical perspective and future prospects. Am J Alternative Agric 1:51–57
Goldstein AH (1994) Involvement of the quinoprotein glucose dehydrogenase in the solubilization of exogenous mineral phosphates by Gram negative bacteria. Phosphate in microorganisms: cellular and molecular biology. ASM Press, Washington, DC, pp 197–203
Gond SK, Bergen MS, Torres MS, White JF, Kharwar RN (2015) Effect of bacterial endophyte on expression of defense genes in Indian popcorn against Fusarium moniliforme. Symbiosis 66:133–140
Gonzalez AJ, Larraburu EE, Llorente BE (2015) Azospirillum brasilense increased salt tolerance of jojoba during in vitro rooting. Ind Crops Prod 76:41–48
Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. Biotech 5:355–377
Gosling P, Hodge A, Goodlass G, Bending G (2006) Arbuscular mycorrhizal fungi and organic farming. Agr Ecosyst Environ 113:17–35
Gowthaman M, Krishna C, Moo-Young M (2001) Fungal solid state fermentation—an overview. In: Applied mycology and biotechnology, vol 1. Elsevier, pp 305–352
Gray E, Smith D (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412
Guerinot M, Chelm BK (1984) Isolation and expression of the Bradyrhizobium japonicum adenylate cyclase gene (cya) in Escherichia coli. J Bacteriol 159:1068–1071
Gügi B, Orange N, Hellio F, Burini J, Guillou C, Leriche F et al (1991) Effect of growth temperature on several exported enzyme activities in the psychrotrophic bacterium Pseudomonas fluorescens. J Bacteriol 173:3814–3820
Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7:096–102
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 Biotech 14:764–773
Haggag WM, Abouziena H, Abd-El-Kreem F, El Habbasha S (2015) Agriculture biotechnology for management of multiple biotic and abiotic environmental stress in crops. J Chem Pharm Res 7:882–889
Halpern M, Bar-Tal A, Ofek M, Minz D, Muller T, Yermiyahu U (2015) The use of biostimulants for enhancing nutrient uptake. In: Advances in agronomy, vol 130. Elsevier, pp 141–174
Hamedi J, Mohammadipanah F (2015) Biotechnological application and taxonomical distribution of plant growth promoting actinobacteria. J Ind Microbiol Biotechnol 42:157–171
Hamedi J, Mohammadipanah F, Panahi HKS (2015) Biotechnological exploitation of actinobacterial members. In: Halophiles. Springer, pp 57–143
Handelsman J, Raffel S, Mester EH, Wunderlich L, Grau CR (1990) Biological control of damping-off of alfalfa seedlings with Bacillus cereus UW85. Appl Environ Microbiol 56:713–718
Han H, Lee K (2005) Phosphate and potassium solubilizing bacteria effect on mineral uptake, soil availability and growth of eggplant. Res J Agric Biol Sci 1:176–180
Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (cu, Zn, Mn, Fe, Ni, Mo, B, cl). Curr Opin Plant Biol 12:259–266
Han HS, Jung JS, Lee KD (2006) Rock phosphate-potassium and rock-solubilising bacteria as alternative, sustainable fertilisers. Agron Sustain Dev 26:233–240
Harman G, Hayes C, Lorito M, Broadway R, Di Pietro A, Peterbauer C et al (1993) Chitinolytic enzymes of Trichoderma harzianum: purification of chitobiosidase and endochitinase. Phytopathology 83:313–318
Hartmann MWF (2006) Community structure analyses are more sensitive to differences in soil bacterial communities than anonymous diversity indices. Appl Environ Microbiol 72:7804–7812
Hartmann A, Schmid M, Van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257
Hawkins H-J, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285
Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598
Hayman D, Stovold G (1979) Spore populations and infectivity of vesicular arbuscular mycorrhizal fungi in New South Wales. Aust J Bot 27:227–233
Heidari M, Golpayegani A (2012) Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.). J Saudi Soc Agric Sci 11:57–61
Hernández A, Castillo H, Ojeda D, Arras A, López J, Sánchez E (2010) Effect of vermicompost and compost on lettuce production. Chilean J Agric Res 70:583–589
Herridge D (2008) Inoculation technology for legumes. In: Nitrogen-fixing leguminous symbioses. Springer, pp 77–115
Herrmann L, Lesueur D (2013) Challenges of formulation and quality of biofertilizers for successful inoculation. Appl Microbiol Biotechnol 97:8859–8873
Hesham AE-L, Kaur T, Devi R, Kour D, Prasad S, Yadav N et al. (2021) Current trends in microbial biotechnology for agricultural sustainability: conclusion and future challenges. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer Singapore, Singapore, pp 555–572. https://doi.org/10.1007/978-981-15-6949-4_22
Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27:637–657
Huang C-J, Wang T-K, Chung S-C, Chen C-Y (2005) Identification of an antifungal chitinase from a potential biocontrol agent, Bacillus cereus 28-9. BMB Rep 38:82–88
Husen EH, Simanungkalit R, Saraswati R, Irawan I (2016) Characterization and quality assessment of Indonesian commercial biofertilizers
Imanparast S, Hamedi J, Faramarzi MA (2018) Enzymatic esterification of acylglycerols rich in omega-3 from flaxseed oil by an immobilized solvent-tolerant lipase from Actinomadura sediminis UTMC 2870 isolated from oil-contaminated soil. Food Chem 245:934–942
Ishizuka J (1992) Trends in biological nitrogen fixation research and application. In: Biological nitrogen fixation for sustainable agriculture. Springer, pp 197–209
Jadhav H, Sayyed R (2016) Hydrolytic enzymes of rhizospheric microbes in crop protection. MOJ Cell Sci Rep 3:00070
Jadhav H, Shaikh S, Sayyed R (2017) Role of hydrolytic enzymes of rhizoflora in biocontrol of fungal phytopathogens: an overview. In: Rhizotrophs: plant growth promotion to bioremediation. Springer, pp 183–203
Jain R, Saxena J, Sharma V (2012) Solubilization of inorganic phosphates by Aspergillus awamori S19 isolated from rhizosphere soil of a semi-arid region. Ann Microbiol 62:725–735
Jawson MD, Franzluebbers AJ, Berg RK (1989) Bradyrhizobium japonicum survival in and soybean inoculation with fluid gels. Appl Environ Microbiol 55:617–622
Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea J-M (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16
Jia Y-J, Kakuta Y, Sugawara M, Igarashi T, Oki N, Kisaki M et al. (1999) Synthesis and degradation of 1-aminocyclopropane-1-carboxylic acid by Penicillium citrinum. Biosci Biotechnol Biochem 63:542–549
Johnson D, Leake JR, Read DJ (2005) Liming and nitrogen fertilization affects phosphatase activities, microbial biomass and mycorrhizal colonisation in upland grassland. Plant Soil 271:157–164
Johnson NC, Wilson GW, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci 107:2093–2098
John RP, Tyagi R, Brar S, Surampalli R, Prévost D (2011) Bio-encapsulation of microbial cells for targeted agricultural delivery. Critical Rev Biotechnol 31:211–226
Kabaluk JT, Svircev AM, Goettel MS, Woo SG (2010) The use and regulation of microbial pesticides in representative jurisdictions worldwide. IOBC Global, pp 94–98
Kanchiswamy CN, Malnoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci 6:151
Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229
Khalid A, Arshad M, Zahir Z (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480
Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi–current perspective. Arch Agrono Soil Sci 56:73–98
Khan ALWM, Kang SM, Al-Harrasi A, Hussain J, Al-Rawahi A, Al-Khiziri S, Ullah I, Ali L, Jung HY, Lee IJ (2014) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52:689–695
Khan M, Mobin M, Abbas Z, Alamri S (2018) Fertilizers and their contaminants in soils, surface and groundwater. Encyclopedia Anthropocene 5:225–240
Kilian M, Steiner U, Krebs B, Junge H, Schmiedeknecht G, Hain R (2000) FZB24® Bacillus subtilis–mode of action of a microbial agent enhancing plant vitality. Pflanzenschutz-Nachrichten Bayer 1:1
Knox O, Killham K, Mullins C, Wilson MJ (2003) Nematode-enhanced microbial colonization of the wheat rhizosphere. FEMS Microbiol Lett 225:227–233
Kour D, Rana KL, Yadav AN, Yadav N, Kumar V, Kumar A et al. (2019a) Drought-tolerant phosphorus-solubilizing microbes: Biodiversity and biotechnological applications for alleviation of drought stress in plants. In: Sayyed RZ, Arora NK, Reddy MS (eds) Plant growth promoting Rhizobacteria for sustainable stress management, vol 1: Rhizobacteria in abiotic stress management. Springer, Singapore, pp 255–308. doi: https://doi.org/10.1007/978-981-13-6536-2_13
Kour D, Rana KL, Yadav N, Yadav AN, Kumar A, Meena VS et al. (2019b) Rhizospheric microbiomes: biodiversity, mechanisms of plant growth promotion, and biotechnological applications for sustainable agriculture. In: Kumar A, Meena VS (eds) Plant growth promoting Rhizobacteria for agricultural sustainability: from theory to practices. Springer, Singapore, pp 19–65. doi:https://doi.org/10.1007/978-981-13-7553-8_2
Kour D, Rana KL, Yadav AN, Yadav N, Kumar M, Kumar V et al (2020) Microbial biofertilizers: bioresources and eco-friendly technologies for agricultural and environmental sustainability. Biocatal Agric Biotechnol 23: https://doi.org/10.1016/j.bcab.2019.101487
Kour D, Rana KL, Kaur T, Yadav N, Yadav AN, Kumar M et al (2021) Biodiversity, current developments and potential biotechnological applications of phosphorus-solubilizing and -mobilizing microbes: a review. Pedosphere 31:43–75. https://doi.org/10.1016/S1002-0160(20)60057-1
Kucey R (1988) Effect of Penicillium bilaji on the solubility and uptake of P and micronutrients from soil by wheat. Can J Soil Sci 68:261–270
Kumar M, Yadav AN, Saxena R, Paul D, Tomar RS (2021) Biodiversity of pesticides degrading microbial communities and their environmental impact. Biocatal Agric Biotechnol 31: https://doi.org/10.1016/j.bcab.2020.101883
Laranjo MAA, Oliveira S (2014) Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. Microbiol Res 169:2–17
Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415
Lian B, Wang B, Pan M, Liu C, Henry H (2008) Microbial release of potassium from K-bearing minerals by thermophilic fungus Aspergillus fumigatus. Geochimica et Cosmochimica Acta 1 72(1):87–98
Li QS-L, Glick BRT (2005) he effect of native and ACC deaminasecontaining Azospirillum brasilense Cdl843 on the rooting of carnation cuttings. Can J Microbiol 51:511–514
Lindström K (1989) Rhizobium galegae, a new species of legume root nodule bacteria. Int J Syst Evol Microbiol 39:365–367
Lindström K, Martinez-Romero E (2007) International committee on systematics of prokaryotes; subcommittee on the taxonomy of Agrobacterium and Rhizobium. Int J Syst Evol Microbiol 57:1365–1366
Lindström K, Kokko-Gonzales P, Terefework Z, Räsänen LA (2006) Differentiation of nitrogen-fixing legume root nodule bacteria (Rhizobia). In: Molecular approaches to soil, rhizosphere and plant microorganism analysis, p 236
Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950
Lorda G, Breccia J, Barbeito V, Pagliero F, Boeris S, Castaño C et al (2007) Peat-based inoculum of Bradyrhizobium japonicum and Sinorhizobium fredii supplemented with xanthan gum. World J Microbiol Biotechnol 23:1–5
Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25
Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556
Lupwayi NZ, Clayton GW, Rice WA (2006) Rhizobial inoculants for legume crops. J Crop Improvement 15:289–321
Lynd LR, Weimer PJ, Van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577
Mabood F, Zhou X, Smith DL (2014) Microbial signaling and plant growth promotion. Can J Plant Sci 94:1051–1063
Mäder PFA, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697
Mahanty T, Bhattacharjee S, Goswami M, Bhattacharyya P, Das B, Ghosh A et al (2017) Biofertilizers: a potential approach for sustainable agriculture development. Environ Sci Pollut Res 24:3315–3335
Mahdi SS, Hussain Dar M, Hamid A, Ahmad L (2012) Soil phosphorus fixation chemistry and role of phosphate solubilizing bacteria in enhancing its efficiency for sustainable cropping-a review. J Pure Appl Microbiol
Malusa E, Sas L (2009) The development of innovative technologies and products for organic fruit production. An integrated project
Malusa E, Sas-Paszt L, Zurawicz E, Popinska W (2007) The effect of a mycorrhiza-bacteria substrate and foliar fertilization on growth response and rhizosphere pH of three strawberry cultivars. Int J Fruit Sci 6:25–41
Malusa E, Sas-Paszt L, Trzcinski P, Górska A (2010) Influences of different organic fertilizers and amendments on nematode trophic groups and soil microbial communities during strawberry growth. In: XXVIII international horticultural congress on science and horticulture for people (IHC2010): international symposium on 933, pp 253–260
Malusá E, Sas-Paszt L, Ciesielska J (2012) Technologies for beneficial microorganisms inocula used as biofertilizers. Sci World J
Malusà E, Pinzari F, Canfora L (2016) Efficacy of biofertilizers: challenges to improve crop production. In: Microbial inoculants in sustainable agricultural productivity. Springer, pp 17–40
Manikandan R, Saravanakumar D, Rajendran L, Raguchander T, Samiyappan R (2010) Standardization of liquid formulation of Pseudomonas fluorescens Pf1 for its efficacy against Fusarium wilt of tomato. Biol Control 54:83–89
Manocha M, Balasubramanian R (1994) Fungal chitinases: their properties and roles in morphogenesis, mycoparasitism and control of pathogenic fungi. Host Wall Alterations by Parasitic Fungi APS Press, San Paul Minnesota, pp 81–90
Martinez-Toledo M, De La Rubia T, Moreno J, Gonzalez-Lopez J (1988) Root exudates of Zea mays and production of auxins, gibberellins and cytokinins by Azotobacter chroococcum. Plant Soil 110:149–152
Martínez-Viveros O, Jorquera M, Crowley D, Gajardo G, Mora M (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319
Martin XM, Sumathi CS, Kannan VR (2011) Influence of agrochemicals and Azotobacter sp. application on soil fertility in relation to maize growth under nursery conditions. Eur J Biosci 5
Marulanda A, Azcón R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232:533–543
Mathivanan RUS, Ramasamy PK, Thangam Y (2015) Influence of vermicompost on the activity of the plant growth regulators in the leaves of the Indian butter bean plant. Int J Adv Res Biol Sci 2:84–89
McComb RB, Bowers GN, Posen S (2013) Alkaline phosphatase. Springer Science & Business Media
McDonnell L, Plett JM, Andersson-Gunnerås S, Kozela C, Dugardeyn J, Van Der Straeten D et al (2009) Ethylene levels are regulated by a plant encoded 1-aminocyclopropane-1-carboxylic acid deaminase. Physiol Plant 136:94–109
McGrath JW, Hammerschmidt F, Quinn JP (1998) Biodegradation of phosphonomycin by Rhizobium huakuii PMY1. Appl Environ Microbiol 64:356–358
Meena M, Swapnil P, Zehra A, Aamir M, Dubey MK, Goutam J et al. (2017) Beneficial microbes for disease suppression and plant growth promotion. In: Plant-microbe interactions in agro-ecological perspectives. Springer, pp 395–432
Mehnaz S (2015) Azospirillum: a biofertilizer for every crop. In: Plant microbes symbiosis: applied facets. Springer, pp 297–314
Meier S, Cornejo P, Cartes P, Borie F, Medina J, Azcón R (2015) Interactive effect between Cu-adapted arbuscular mycorrhizal fungi and biotreated agrowaste residue to improve the nutritional status of Oenothera picensis growing in Cu-polluted soils. J Plant Nutr Soil Sci 178:126–135
Mendes GDO, da Silva NMRM, Anastácio TC, Vassilev NB, Ribeiro JI Jr, da Silva IR et al (2015) Optimization of Aspergillus niger rock phosphate solubilization in solid-state fermentation and use of the resulting product as a P fertilizer. Microb Biotechnol 8:930–939
Minami R, Uchiyama K, Murakami T, Kawai J, Mikami K, Yamada T et al (1998) Properties, sequence, and synthesis in Escherichia coli of 1-aminocyclopropane-l-carboxylate deaminase from Hansenula saturnus. J Biochem 123:1112–1118
Mishra P, Dash D (2014) Rejuvenation of biofertilizer for sustainable agriculture and economic development. Consilience 41–61
Mishra D, Rajvir S, Mishra U, Kumar SS (2013) Role of bio-fertilizer in organic agriculture: a review. Res J Recent Sci 2:39–41
MM s (2001) Nutritional status and growth of maize plants as affected by green microalgae as soil additives. J Biol Sci 6:475–479
Mohammadi K, Sohrabi Y (2012) Bacterial biofertilizers for sustainable crop production: a review. J Agric Biol Sci 7:307–316
Mondal S, Halder SK, Yadav AN, Mondal KC (2020) Microbial consortium with multifunctional plant growth promoting attributes: future perspective in agriculture. In: Yadav AN, Rastegari AA, Yadav N, Kour D (eds) Advances in plant microbiome and sustainable agriculture, vol 2: functional annotation and future challenges. Springer, Singapore, pp 219–254. https://doi.org/10.1007/978-981-15-3204-7_10
Montañez A, Blanco AR, Barlocco C, Beracochea M, Sicardi M (2012) Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Appl Soil Ecol 58:21–28
Moore AW (1969) Azolla: biology and agronomic significance. Bot Rev 35(1):17–34
Morrison BA, Cozatl-Manzano R (2003) Initial evidence for use of periphyton as an agricultural fertilizer by the ancient Maya associated with the El Edén wetland, northern Quintana Roo, Mexico. The Lowland Maya area: Three millennia at the human-wildland interface Food Products Press, New York, pp 401–413
Muthukumarasamy R, Revathi G, Seshadri S, Lakshminarasimhan C (2002) Gluconacetobacter diazotrophicus (syn. Acetobacter diazotrophicus), a promising diazotrophic endophyte in tropics. Curr Sci 137–145
Nandi M, Selin C, Brassinga AKC, Belmonte MF, Fernando WD, Loewen PC et al (2015) Pyrrolnitrin and hydrogen cyanide production by Pseudomonas chlororaphis strain PA23 exhibits nematicidal and repellent activity against Caenorhabditis elegans. PLoS ONE 10:
Nandi M, Selin C, Brawerman G, Fernando WD, de Kievit T (2017) Hydrogen cyanide, which contributes to Pseudomonas chlororaphis strain PA23 biocontrol, is upregulated in the presence of glycine. Biol Control 108:47–54
Nascimento FX, Rossi MJ, Soares CR, McConkey BJ, Glick BR (2014) New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS ONE 9:
Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A (2014) Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul 73:121–131
Negi YK, Prabha D, Garg SK, Kumar J (2017) Biological control of ragi blast disease by chitinase producing fluorescent Pseudomonas isolates. Organ Agric 7:63–71
Nick GDLP, Eardly BD, Suomalainen S, Paulin L, Zhang X, Gillis M, Lindström K (1999) Sinorhizobium arboris sp. nov. and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya. Int J Syst Evol Microbiol 49:1359–1368
Nour SM, Fernandez MP, Normand P, Cleyet-Marel J-C (1994) Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpeas (Cicer arietinum L.). Int J Syst Evol Microbiol 44:511–522
Oehl F, Sieverding E, Mäder P, Dubois D, Ineichen K, Boller T et al (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583
Ohtake HKJ, Kuroda A, Wu H, Ikeda T (1998) Regulation of bacterial phosphate taxis and polyphosphate accumulation in response to phosphate starvation stress. J Biosci 23:491
Okon Y, Baker R (1987) Microbial inoculants as crop-yield enhancers. Crit Rev Biotechnol 6:61–85
Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197
Ortega-Larrocea M, Siebe C, Becard G, Mendez I, Webster R (2001) Impact of a century of wastewater irrigation on the abundance of arbuscular mycorrhizal spores in the soil of the Mezquital Valley of Mexico. Appl Soil Ecol 16:149–157
Otieno N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ et al (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745
Owen D, Williams AP, Griffith GW, Withers PJ (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphrous acquisition. Appl Soil Ecol 86:41–54
Palmer C, Golden K, Danniels L, Ahmad H (2007) ACC deaminase from Issatchenkia occidentalis. J Biol Sci 7:188–193
Pal S, Singh H, Farooqui A, Rakshit A (2015) Fungal biofertilizers in Indian agriculture: perception, demand and promotion. J Eco-friendly Agric 10:101–113
Pandey A, Selvakumar P, Soccol CR, Nigam P (1999) Solid state fermentation for the production of industrial enzymes. Curr Sci 149–162
Park J, Chang H (2000) Microencapsulation of microbial cells. Biotechnol Adv 18:303–319
Parmar P, Sindhu S (2013) Potassium solubilization by rhizosphere bacteria: influence of nutritional and environmental conditions. J Microbiol Res 3:25–31
Parray JA, Jan S, Kamili AN, Qadri RA, Egamberdieva D, Ahmad P (2016) Current perspectives on plant growth-promoting rhizobacteria. J Plant Growth Regul 35:877–902
Patagundi BI, Shivasharan C, Kaliwal B (2014) Isolation and characterization of cellulase producing bacteria from soil. Int J Curr Microbiol Appl Sci 3:59–69
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295
Perron F, Légère A, Tremblay G, Simard R, Angers D, Hamel C (2001) Crop and weed response to nutrient source, tillage and weed control method in a corn-soybean rotation. Can J Plant Sci 81:561–571
Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200
Prakash S, Verma JP (2016) Global perspective of potash for fertilizer production. In: Potassium solubilizing microorganisms for sustainable agriculture. Springer, pp 327–331
Prasad H, Chandra R (2003) Growth pattern of urdbean Rhizobium sp. with PSB and PGPR in consortia. J Indian Soc Soil Sci 51:76–78
Prasad RC, Prasad BN (2001) Cyanobacteria as a source biofertilizer for sustainable agriculture in Nepal. J Plant Sci Botanica Orientalis 127–133
Prasad S, Malav LC, Choudhary J, Kannojiya S, Kundu M, Kumar S et al. (2021) Soil microbiomes for healthy nutrient recycling. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer Singapore, Singapore, pp 1–21. https://doi.org/10.1007/978-981-15-6949-4_1
Prat D (1992) Effect of inoculation with Frankia on the growth of Alnus in the field. Acta Oecol 13:463–467
Priyadharsini P, Muthukumar T (2016) Interactions between arbuscular mycorrhizal fungi and potassium-solubilizing microorganisms on agricultural productivity. In: Potassium solubilizing microorganisms for sustainable agriculture. Springer, pp 111–125
Qin H, Lu K, Strong P, Xu Q, Wu Q, Xu Z et al (2015) Long-term fertilizer application effects on the soil, root arbuscular mycorrhizal fungi and community composition in rotation agriculture. Appl Soil Ecol 89:35–43
Qu XH, Wang J (2008) Effect of amendments with different phenolic acids on soil microbial biomass, activity, and community diversity. Appl Soil Ecol 39:172–179
Raghavendra M, Nayaka SC, Nuthan B (2016) Role of rhizosphere microflora in potassium solubilization. In: Potassium solubilizing microorganisms for sustainable agriculture. Springer, pp 43–59
Rai A, Rai S, Rakshit A (2013) Mycorrhiza-mediated phosphorus use efficiency in plants. Environ Exp Biol 11:107–117
Rai PK, Singh M, Anand K, Saurabhj S, Kaur T, Kour D et al. (2020) Role and potential applications of plant growth promotion rhizobacteria for sustainable agriculture. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 49–60. https://doi.org/10.1016/B978-0-12-820526-6.00004-X
Raj SA (2007) Bio-fertilizers for micronutrients. Biofertilizer Newsletter 8–10
Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149
Ramadan EM, AbdelHafez AA, Hassan EA, Saber FM (2016) Plant growth promoting rhizobacteria and their potential for biocontrol of phytopathogens. Afri J Microbiol Res 10:486–504
Ramette A, Moënne-Loccoz Y, Défago G (2006) Genetic diversity and biocontrol potential of fluorescent pseudomonads producing phloroglucinols and hydrogen cyanide from Swiss soils naturally suppressive or conducive to Thielaviopsis basicola-mediated black root rot of tobacco. FEMS Microbiol Ecol 55:369–381
Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V et al. (2019b) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer International Publishing, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6
Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN et al (2019a) Endophytic fungi: biodiversity, ecological significance and potential industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi, vol 1. Diversity and enzymes perspectives. Springer, Switzerland, pp 1–62
Rana KL, Kour D, Yadav AN (2019b) Endophytic microbiomes: biodiversity, ecological significance and biotechnological applications. Res J Biotechnol 14:142–162
Rana KL, Kour D, Kaur T, Devi R, Yadav AN, Yadav N et al (2020) Endophytic microbes: biodiversity, plant growth-promoting mechanisms and potential applications for agricultural sustainability. Antonie Van Leeuwenhoek 113:1075–1107. https://doi.org/10.1007/s10482-020-01429-y
Rastegari AA, Yadav AN, Yadav N (2020a) New and future developments in microbial biotechnology and bioengineering: trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam
Rastegari AA, Yadav AN, Yadav N (2020b) New and future developments in microbial biotechnology and bioengineering: trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam
Ravanbakhsh M, Sasidharan R, Voesenek LA, Kowalchuk GA, Jousset A (2017) ACC deaminase-producing rhizosphere bacteria modulate plant responses to flooding. J Ecol 105:979–986
Rawat J, Sanwal P, Saxena J (2016) Potassium and its role in sustainable agriculture. In: Potassium solubilizing microorganisms for sustainable agriculture. Springer, pp 235–253
Reid MS (1981) The role of ethylene in flower senescene. Acta Hortic 261:157–169
Reinhold-Hurek BHT (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443
Rice W, Clayton G, Olsen P, Lupwayi N (2000) Rhizobial inoculant formulations and soil pH influence field pea nodulation and nitrogen fixation. Can J Soil Sci 80:395–400
Richardson AEHP (1997) Soil isolates of Pseudomonas spp. that utilize inositol phosphates. Can J Microbiol 43:509–516
Rijavec T, Lapanje A (2016) Hydrogen cyanide in the rhizosphere: not suppressing plant pathogens, but rather regulating availability of phosphate. Front Microbiol 7:1785
Rodrı́guez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339
Rodríguez AASA, Storni MM, Zulpa G, Zaccaro MC (2006a) Effects of cyanobacterial extracellular products and gibberellic acid on salinity tolerance in Oryza sativa L. Saline Systems 2(1):7
Rodríguez HFR, Gonzalez T, Bashan Y (2006b) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21
Roger P-A, Pierre-Adrien R (1982) Free—living blue—green algae in tropical soils. In: Microbiology of tropical soils and plant productivity. Springer, Dordrecht, pp 147–168
Rome S, Fernandez MP, Brunel B, Normand P, Cleyet-Marel J-C (1996) Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. Int J Syst Evol Microbiol 46:972–980
Roughley R (1976) The production of high quality inoculants and their contribution to legume yield. Symbiotic Nitro Fix Plants 7:125
Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340
Roychowdhury D, Paul M, Banerjee SK (2014) A review on the effects of biofertilizers and biopesticides on rice and tea cultivation and productivity. Int J Sci Eng Technol 2:96–106
Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Paré PW et al (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932
Sadeghi A, Koobaz P, Azimi H, Karimi E, Akbari AR (2017) Plant growth promotion and suppression of Phytophthora drechsleri damping-off in cucumber by cellulase-producing Streptomyces. Biocontrol 62:805–819
Sahu P, Brahmaprakash G (2016) Formulations of biofertilizers–approaches and advances. In: Microbial inoculants in sustainable agricultural productivity. Springer, pp 179–198
Salimi F, Hamedi J, Motevaseli E, Mohammadipanah F (2018a) Isolation and screening of rare Actinobacteria, a new insight for finding natural products with antivascular calcification activity. J Appl Microbiol 124:254–266
Salimi F, Jafari-Nodooshan S, Zohourian N, Kolivand S, Hamedi J (2018b) Simultaneous anti-diabetic and anti-vascular calcification activity of Nocardia sp. UTMC 751. Lett Appl Microbiol 66:110–117
Salimi F, Hamedi J, Motevaseli E, Mohammadipanah F (2019) Coexistence of anticoagulant and anti-vascular calcification activities in Kribbella sp. UTMC 267 metabolites. Iran J Pharma Res IJPR 18:459
Salisbury FBRC (1992) Photosynthesis: environmental and agricultural aspects. Plant Physiol Wadsworth Publishing Company, Belmont, CA 286:249–265
Samoon HADS, Zehra B, Mahdi SS, Hassan GI (2010) Bio-fertilizers in organic agriculture. J Phytol 2:9–14
Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169:18–29
Sarkar A, Ghosh PK, Pramanik K, Mitra S, Soren T, Pandey S et al (2018) A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res Microbiol 169:20–32
Sarma RK, Saikia R (2014) Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21. Plant Soil 377:111–126
Savci S (2012) An agricultural pollutant: chemical fertilizer. Int J Environ Sci Dev 3:73
Saxena A, Tilak K (1998) Free-living nitrogen fixers: Its role in crop production. Microbes for Health, Wealth and Sustainable Environment, Malhotra Publ Co, New Delhi Edited by Verma AK, pp 25–64
Schlesinger WH, Bernhardt E (2013) Biogeochemistry: an analysis of global change. Academic press
Scholla MH, Elkan GH (1984) Rhizobium fredii sp. nov., a fast-growing species that effectively nodulates soybeans. Int J Syst Evol Microbiol 34:484–486
Schuessler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: evolution and phylogeny. Mycol Res 105:1413–1421
Schulz TJ, Thelen KD (2008) Soybean seed inoculant and fungicidal seed treatment effects on soybean. Crop Sci 48:1975–1983
Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK et al (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol Lett 9:501–515
Segovia L, Young JPW, Martínez-Romero E (1993) Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int J Syst Evol Microbiol 43:374–377
Sethi SK, Adhikary SP (2012) Cost effective pilot scale production of biofertilizer using Rhizobium and Azotobacter. Afr J Biotech 11:13490–13493
Shafi M, Shah A, Bakht J, Shah M, Mohammad W (2012) Integrated effect of inorganic and organic nitrogen sources on soil fertility and productivity of maize. J Plant Nutr 35:524–537
Shaharoona B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Appl Microbiol Biotechnol 79:147–155
Shahzad RKA, Bilal S, Waqas M, Kang SM, Lee IJ (2017) Inoculation of abscisic acid-producing endophytic bacteria enhances salinity stress tolerance in Oryza sativa. Environ Exp Bot 136:68–77
Sharifi R, Ryu C-M (2016) Are bacterial volatile compounds poisonous odors to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for eliciting induced resistance, or both? Front Microbiol 7:196
Sharma S, Kour D, Rana KL, Dhiman A, Thakur S, Thakur P et al. (2019) Trichoderma: biodiversity, ecological significances, and industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi: vol 1: diversity and enzymes perspectives. Springer, Cham, pp 85–120. https://doi.org/10.1007/978-3-030-10480-1_3
Sharma VP, Singh S, Dhanjal DS, Singh J, Yadav AN (2021) Potential strategies for control of agricultural occupational health hazards. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer Singapore, Singapore, pp 387–402. https://doi.org/10.1007/978-981-15-6949-4_16
Shrivastava M, Srivastava P, D’Souza S (2016) KSM soil diversity and mineral solubilization, in relation to crop production and molecular mechanism. In: Potassium solubilizing microorganisms for sustainable agriculture. Springer, pp 221–234
Simmons CR (1994) The physiology and molecular biology of plant 1, 3-β-d-glucanases and 1, 3; 1, 4-β-d-glucanases. Crit Rev Plant Sci 13:325–387
Singh R, Adholeya A (2003) Interactions between arbuscular mycorrhizal fungi and plant-growth promoting rhizobacteria. Mycorrhiza News 15:16–17
Singh N, Kashyap S (2012) In silico identification and characterization of 1-aminocyclopropane-1-carboxylate deaminase from Phytophthora sojae. J Mol Model 18:4101–4111
Singh JS, Pandey VC, Singh D (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agr Ecosyst Environ 140:339–353
Singh RP, Shelke GM, Kumar A, Jha PN (2015) Biochemistry and genetics of ACC deaminase: a weapon to “stress ethylene” produced in plants. Front Microbiol 6:937
Singh M, Dotaniya M, Mishra A, Dotaniya C, Regar K, Lata M (2016) Role of biofertilizers in conservation agriculture. In: Conservation agriculture. Springer, pp 113–134
Singh A, Kumar R, Yadav AN, Mishra S, Sachan S, Sachan SG (2020) Tiny microbes, big yields: microorganisms for enhancing food crop production sustainable development. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 1–15. https://doi.org/10.1016/B978-0-12-820526-6.00001-4
Sivakumar T, Shankar T, Vijayabaskar P, Ramasubramanian V (2012) Plant growth promoting activity of nickel tolerant Bacillus cereus TS1. J Agric Technol 8:2101–2113
Skorupska A, Wielbo J, Kidaj D, Marek-Kozaczuk M (2010) Enhancing Rhizobium–legume symbiosis using signaling factors. In: Microbes for legume improvement. Springer, pp 27–54
Skraly FA, Cameron DC (1998) Purification and characterization of a Bacillus licheniformis phosphatase specific ford-α-glycerophosphate. Arch Biochem Biophys 349:27–35
Smith BE RR, Newton WE (2013) Catalysts for nitrogen fixation: nitrogenases, relevant chemical models and commercial processes. Springer Science & Business Media
Smith S, Read D (2008) Mineral nutrition, toxic element accumulation and water relations of arbuscular mycorrhizal plants. Mycorrhizal Symbiosis 3:145–148
Smith F, Smith S (1997) Tansley review no. 96 structural diversity in (vesicular)–arbuscular mycorrhizal symbioses. The New Phytologist 137:373–388
Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104:1–13
Song X, Liu M, Wu D, Griffiths BS, Jiao J, Li H et al (2015) Interaction matters: synergy between vermicompost and PGPR agents improves soil quality, crop quality and crop yield in the field. Appl Soil Ecol 89:25–34
Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3:
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
Stephens J, Rask H (2000) Inoculant production and formulation. Field Crops Res 65:249–258
Stockwell V, Johnson K, Sugar D, Loper J (2011) Mechanistically compatible mixtures of bacterial antagonists improve biological control of fire blight of pear. Phytopathology 101:113–123
Strange RN, Scott PR (2005) Plant disease: a threat to global food security. Annu Rev Phytopathol 43:83–116
Subrahmanyam G, Kumar A, Sandilya SP, Chutia M, Yadav AN (2020) Diversity, plant growth promoting attributes, and agricultural applications of rhizospheric microbes. In: Yadav AN, Singh J, Rastegari AA, Yadav N (eds) Plant microbiomes for sustainable agriculture. Springer, Cham, pp 1–52. https://doi.org/10.1007/978-3-030-38453-1_1
Subramanian GUL (1996) Cyanobacteria in pollution control. J Sci Ind Res 1:685–692
Subramaniyam R, Vimala R (2012) Solid state and submerged fermentation for the production of bioactive substances: a comparative study. Int J Sci Nat 3:480–486
Sukarno N, Smith F, Smith S, Scott E (1996) The effect of fungicides on vesicular-arbuscular mycorrhizal symbiosis: II. The effects on area of interface and efficiency of P uptake and transfer to plant. New Phytol 132:583–592
Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Singh DP, Singh HB, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity: vol. 1: research perspectives. Springer, New Delhi, pp 117–143. https://doi.org/10.1007/978-81-322-2647-5_7
Suthar H, Hingurao K, Vaghashiya J, Parmar J (2017) Fermentation: a process for biofertilizer production. In: Microorganisms for green revolution. Springer, pp 229–252
Suyal DC, Soni R, Yadav AN, Goel R (2021) Cold adapted microorganisms: survival mechanisms and applications. In: Yadav AN, Rastegari AA, Yadav N (eds) Microbiomes of extreme environments: biodiversity and biotechnological applications. CRC Press, Taylor & Francis, Boca Raton, pp 177–192
Świechowski W, Doruchowski G, Trzciński P (2012) Effect of spray application parameters on viability of bacterium Pseudomonas fluorescens used as bio-pesticide in organic fruit production. In: Proceedings of the II international congress on organic fruit research symposium. ISHS, Leavenworth WA, USA, p 9
Tairo EV, Ndakidemi PA (2013) Possible benefits of rhizobial inoculation and phosphorus supplementation on nutrition, growth and economic sustainability in grain legumes. Am J Res Commun 1:532–556
Taiz LZE (2010) Photosynthesis: the light reactions. Plant Physiol 5:163–198
Tarbell T, Koske R (2007) Evaluation of commercial arbuscular mycorrhizal inocula in a sand/peat medium. Mycorrhiza 18:51–56
Thakur N, Kaur S, Tomar P, Thakur S, Yadav AN (2020) Microbial biopesticides: current status and advancement for sustainable agriculture and environment. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 243–282. https://doi.org/10.1016/B978-0-12-820526-6.00016-6
Thaller MC, Berlutti F, Schippa S, Iori P, Passariello C, Rossolini GM (1995) Heterogeneous patterns of acid phosphatases containing low-molecular-mass polypeptides in members of the family Enterobacteriaceae. Int J Syst Evol Microbiol 45:255–261
Thomine S, Lanquar V (2011) Iron transport and signaling in plants. In: Transporters and pumps in plant signaling. Springer, pp 99–131
Tien T, Gaskins M, Hubbell D (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl Environ Microbiol 37:1016–1024
Tittabutr P, Payakapong W, Teaumroong N, Singleton PW, Boonkerd N (2007) Growth, survival and field performance of bradyrhizobial liquid inoculant formulations with polymeric additives. Sci Asia 33:69–77
Tiwari P, Bajpai M, Singh LK, Mishra S, Yadav AN (2020) Phytohormones producing fungal communities: metabolic engineering for abiotic stress tolerance in crops. In: Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (eds) Agriculturally important fungi for sustainable agriculture, volume 1: perspective for diversity and crop productivity. Springer, Cham, pp 1–25. https://doi.org/10.1007/978-3-030-45971-0_8
Tiwari P, Bajpai M, Singh LK, Yadav AN, Bae H (2021) Portraying fungal mechanisms in stress tolerance: perspective for sustainable agriculture. In: Yadav AN (ed) Recent trends in mycological research: volume 1: agricultural and medical perspective. Springer International Publishing, Cham, pp 269–291. https://doi.org/10.1007/978-3-030-60659-6_12
Toljander JF, Santos-González JC, Tehler A, Finlay RD (2008) Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol Ecol 65:323–338
Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. BioMed Res Int
Uren NC (2000) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: The rhizosphere. CRC Press, pp 35–56
Van Overbeek L, Van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296
Vassilev N, Toro M, Vassileva M, Azcon R, Barea JM (1997) Rock phosphate solubilization by immobilized cells of Enterobacter sp. in fermentation and soil conditions. Biores Technol 61:29–32
Vassilev N, Nikolaeva I, Vassileva M (2005) Polymer-based preparation of soil inoculants: applications to arbuscular mycorrhizal fungi. Rev Environ Sci Bio/Technol 4:235–243
Vassilev N, Medina A, Azcon R, Vassileva M (2006a) Microbial solubilization of rock phosphate on media containing agro-industrial wastes and effect of the resulting products on plant growth and P uptake. Plant Soil 287:77
Vassilev N, Vassileva M, Nikolaeva I (2006b) Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71:137–144
Velázquez E, Igual JM, Willems A, Fernández MP, Muñoz E, Mateos PF et al (2001) Mesorhizobium chacoense sp. nov., a novel species that nodulates Prosopis alba in the Chaco Arido region (Argentina). Int J Syst Evol Microbiol 51:1011–1021
Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017) Beneficial plant-microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crop improvement. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives, vol 2: microbial interactions and agro-ecological impacts. Springer, Singapore, pp 543–580. https://doi.org/10.1007/978-981-10-6593-4_22
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
Vestergård M, Henry F, Rangel-Castro JI, Michelsen A, Prosser JI, Christensen S (2008) Rhizosphere bacterial community composition responds to arbuscular mycorrhiza, but not to reductions in microbial activity induced by foliar cutting. FEMS Microbiol Ecol 64:78–89
Viterbo A, Landau U, Kim S, Chernin L, Chet I (2010) Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol Lett 305:42–48
Voß U, Bishopp A, Farcot E, Bennett MJ (2014) Modelling hormonal response and development. Trends Plant Sci 19:311–319
Walder F, van der Heijden MG (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nature Plants 1:15159
Wall L, Berry A (2007) Early interactions, infection and nodulation in actinorhizal symbiosis. In: Nitrogen-fixing actinorhizal symbioses. Springer, pp 147–166
Wang X, Pan Q, Chen F, Yan X, Liao H (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181
Wang X, Mavrodi DV, Ke L, Mavrodi OV, Yang M, Thomashow LS et al (2015) Biocontrol and plant growth-promoting activity of rhizobacteria from C hinese fields with contaminated soils. Microb Biotechnol 8:404–418
Wani S (1990) Inoculation with associative nitrogen-fixing bacteria: Role in cereal grain production improvement. Indian J Microbiol 30:363–393
Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate solubilizing fungi. In: Sparks DL (ed) Advances in agronomy. Academic Press, pp 99–151
Wu S, Cao Z, Li Z, Cheung K, Wong MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125:155–166
Xavier LJ, Germida JJ (2003) Selective interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum bv. viceae enhance pea yield and nutrition. Biol Fertil Soils 37:261–267
Xiang W, Zhao L, Xu X, Qin Y, Yu G (2012) Mutual information flow between beneficial microorganisms and the roots of host plants determined the bio-functions of biofertilizers. Am J Plant Sci 3:1115
Xie X, Huang W, Liu F, Tang N, Liu Y, Lin H et al (2013) Functional analysis of the novel mycorrhiza-specific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis. New Phytol 198:836–852
Yadav AN (2021) Beneficial plant-microbe interactions for agricultural sustainability. J Appl Biol Biotechnol 9:1–4. https://doi.org/10.7324/JABB.2021.91ed
Yadav AN, Kaur T, Kour D, Rana KL, Yadav N, Rastegari AA et al. (2020a) Saline microbiome: biodiversity, ecological significance and potential role in amelioration of salt stress in plants. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam pp 283–309. https://doi.org/10.1016/B978-0-12-820526-6.00018-X
Yadav AN, Sachan SG, Verma P, Kaushik R, Saxena AK (2016) Cold active hydrolytic enzymes production by psychrotrophic Bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. J Basic Microbiol 56:294–307
Yadav AN, Singh J, Rastegari AA, Yadav N (2020b) Plant microbiomes for sustainable agriculture. Springer, Cham
Yadav AN, Singh J, Singh C, Yadav N (2021) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore
Yang J, Kloepper JW, Ryu C-M (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4
Youssef M, Eissa M (2014) Biofertilizers and their role in management of plant parasitic nematodes. A review. E3 J Biotechnol Pharm Res 5:1–6
Yu WQ, Zheng GP, Yan FC, Liu WZ, Liu WX (2019) Paenibacillus terrae NK3-4: A potential biocontrol agent that produces β-1, 3-glucanase. Biol Control 129:92–101
Zachow C, Müller H, Monk J, Berg G (2017) Complete genome sequence of Pseudomonas brassicacearum strain L13-6-12, a biological control agent from the rhizosphere of potato. Stand Genom Sci 12:6
Zoppellari F, Malusà E, Chitarra W, Lovisolo C, Spanna F, Bardi L (2014) Improvement of drought tolerance in maize (Zea mays L.) by selected rhizospheric microorganisms. Ital J Agrometeorol 18:5–18
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Salimi, F., Hamedi, J. (2021). Biofertilizers: Microbes for Agricultural Productivity. In: Yadav, A.N. (eds) Soil Microbiomes for Sustainable Agriculture. Sustainable Development and Biodiversity, vol 27. Springer, Cham. https://doi.org/10.1007/978-3-030-73507-4_14
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