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Significance of Plant Growth Promoting Rhizobacteria in Grain Legumes: Growth Promotion and Crop Production

Division of Microbiology, ICAR-Indian Agricultural Research Institute (IARI), New Delhi 110012, India
International Centre for Agricultural Research in the Dry Areas (ICARDA), Rabat 10112, Morocco
Authors to whom correspondence should be addressed.
Plants 2020, 9(11), 1596;
Original submission received: 23 September 2020 / Revised: 24 October 2020 / Accepted: 28 October 2020 / Published: 17 November 2020
(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)


Grain legumes are an important component of sustainable agri-food systems. They establish symbiotic association with rhizobia and arbuscular mycorrhizal fungi, thus reducing the use of chemical fertilizers. Several other free-living microbial communities (PGPR—plant growth promoting rhizobacteria) residing in the soil-root interface are also known to influence biogeochemical cycles and improve legume productivity. The growth and function of these microorganisms are affected by root exudate molecules secreted in the rhizosphere region. PGPRs produce the chemicals which stimulate growth and functions of leguminous crops at different growth stages. They promote plant growth by nitrogen fixation, solubilization as well as mineralization of phosphorus, and production of phytohormone(s). The co-inoculation of PGPRs along with rhizobia has shown to enhance nodulation and symbiotic interaction. The recent molecular tools are helpful to understand and predict the establishment and function of PGPRs and plant response. In this review, we provide an overview of various growth promoting mechanisms of PGPR inoculations in the production of leguminous crops.

1. Introduction

Grain legumes (Family Leguminosae), also called pulses, are high in protein content (20–25%) and form an essential part of daily diets across the globe. The protein-rich grains of these crops are also a good source of vitamins, minerals, prebiotics, and other important nutrients. Globally, pulses are grown on 95.7 million ha area, as rainfed crops, mainly on marginal lands with minimum agro-inputs wherein a diverse range of soil microorganisms play a vital role. Soil microorganisms form an integral part of nutrient cycling processes and are crucial determinants of soil fertility and health. The beneficial soil bacteria which colonize roots and their surroundings (rhizosphere) are collectively called plant growth-promoting rhizobacteria (PGPR) [1]. They form symbiotic, associative or neutral association with plants and have a significant influence on crop growth and development. PGPRs stimulate plant growth by nutrient mobilization, solubilization, and transformation [2,3,4] and protect plants from pathogenic infections [5,6,7]. The colonization potential of PGPRs is driven by chemo-taxis response with root exudates that either attract or deter rhizospheric microorganisms [8,9]. It is estimated that about 30% of plant photosynthates are released via root exudation [10], which consists of high and low molecular weight compounds like sugars, proteins, organic acids, flavonoids, mucilage, etc. [11]. A proportion of the root exudate molecules can be metabolized by rhizobacteria for their own utilization in the immediate vicinity of roots, or can be taken up by plants for growth. Root exuded flavonoids are the key signals for legume-rhizobial and legume-mycorrhizal interactions and their establishment [12]. Rhizobia along with other PGPRs inhabit the roots of legumes, which can directly improve plant growth through their influence on physiological and biochemical parameters of the host. Hence, the present review attempts to understand the role of PGPRs and their applications in leguminous crops.

2. Growth-Promoting Mechanisms of PGPR

Plant growth promotion by rhizobacteria can occur directly or indirectly at different times during the life cycle of the plant [13]. Direct growth promotion includes nitrogen fixation [14], phosphate solubilization [15], phytohormone production [16] or enhancement in the availability of minerals [17]. The N fixation process is mediated by an oxygen-sensitive, nitrogenase enzyme complex which converts the atmospheric nitrogen into an ammonical form (biologically fixed nitrogen) that is either made available to the plants or released in the soil. Phosphate solubilizers mobilize fixed forms of phosphorus already present in the soil in the available form to the plant. The production of plant hormones such as auxins, gibberellins and cytokinins also influence plant growth. Production of siderophores by PGPR helps the plant with enough iron in iron-limited soils. Other beneficial effects on plant growth attributed to PGPR include osmotic adjustment, stomatal regulation, modification of root morphology, etc. under abiotic stress conditions [18,19]. Indirect growth promotion of PGPR is attributed to the prevention of the deleterious effects of phytopathogens [5] by producing antagonistic substances such as phenazine, diacetylphloroglucinol (DAPG), hydrogen cyanide (HCN), 2–3 butanediol, acetoin [20] and siderophores [21]. The lytic enzymes viz., chitinase and glucanase produced by these PGPRs can degrade the cell-wall of fungal pathogens, thus inducing systematic resistance throughout the entire plant system [22]. However, the ways by which PGPRs influence plant growth directly may differ from species to species or can be strain specific. The positive effects of PGPR inoculations have been studied in many plants, and Table 1 enlists some of the examples where these bacteria have significantly enhanced the growth and development of legumes. PGPRs interact with plants through various direct and indirect mechanisms which are functions of PGPR activities and biotic as well as abiotic factors present in the surroundings (Figure 1).

2.1. Nitrogen Fixation

Diazotrophic microorganisms fix atmospheric nitrogen either as free-living or in symbiotic association with higher plants. N requirement for sustained productivity of pulses relies on symbiotic nitrogen fixation (SNF) by root nodulating bacteria called rhizobia. The genetic and metabolic integrity of rhizobia imparts ecologically effective adaptation to legume crops under nitrogen-depleted soil [59]. These organisms are Gram-negative, rod-shaped motile, non-spore forming and live freely in the soil, showing chemoheterotrophic mode of nutrition with G+C content of 59–65.5%. They have an ability to produce extracellular polysaccharides of varying compositions and exhibit slimy growth on YEMA (yeast extract mannitol agar) medium. Taxonomical studies on rhizobia gave the theory of cross-inoculation groups in which rhizobia isolated from one plant can nodulate other plants of the same group [60]. Later, fast-growing Rhizobium and slow-growing Bradyrhizobium were reported on the basis of their growth on laboratory media [61]. Rhizobial strains isolated from pea, bean and clover are known as fast growers, whereas those isolated from soybean and cowpea are characterized as slow growers. Mesorhizobium species that nodulates a wide range of hosts including acacia, astragalus, chickpea, lotus, lupinus, leucaena, prosopis, etc. show characteristics of intermediate growth rates [62]. On the basis of 16S rRNA gene sequence, rhizobia have been divided into six genera namely, Azorhizobium, Allorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium, and Sinorhizobium [63], with a strong specificity between leguminous hosts and nodulating rhizobial strains [60]. According to current taxonomic classification, 14 genera and 98 species have been identified in rhizobia belonging to diverse groups such as α-proteobacteria (Azorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium, Ensifer, Phyllobacterium, Microvirga, Ochrobactrum, Methylobacterium, Devosia and Shinella), β-proteobacteria (close to Burkholderia, Cupriavidus (formerly Ralstonia) and γ-proteobacteria (Pseudomonas) [64]. The complex interaction between rhizobia and host legumes is mediated by plant signals, particularly flavonoids, which in turn can activate nodulation genes (nod/nol/noe) and synthesize Nod factor, which is a host determinant in rhizobia [65]. Rhizobia form two types of nodules, determinate and indeterminate [66]. Determinate nodules are spherical due to early meristem termination and are found in soybean, common bean, Lotus, and Vigna species, whereas indeterminate nodules are cylindrical in shape due to later meristem termination, and are found in pea, alfalfa, clover and vetch. Different strains of rhizobia can fix atmospheric nitrogen into ammonia with the help of enzyme nitrogenase.
N2 + 8H+ + 8e + 16 ATP → 2NH3 + H2 + 16ADP + 16 Pi
The nif and fix genes are involved in symbiotic nitrogen fixation [67] and the symbiotic effectiveness of different legumes varies depending on the host and rhizobial strains. It is estimated that 100–175 million metric tons of nitrogen is fixed through the biological nitrogen fixation process [68], in which SNF contributes 70 million metric tons annually [69] or 24 to 584 kg N ha−1 yr−1 [70]. SNF also offers organic nitrogen that becomes slowly available to non-legume crops [71]. Legume–rhizobial symbiosis alone fulfils the one-third of the global N demand. The amount of nitrogen fixed as a result of SNF by rhizobia is summarized in Table 2. Besides rhizobia, some non-rhizobial nodule inhabiting bacteria such as Arthrobacter, Bacillus, Burkholderia, Dyella, Methylobacterium, Microbacterium, Staphylococcus and Streptomyces isolated from legume root nodules are reported to possess plant growth, promoting activities such as nitrogen fixation, P solubilization and growth promotion [72,73,74]. In addition to root nodulating bacteria, other free-living diazotrophic bacteria such as Azotobacter, Arthrobacter, Acinetobacter, Bacillus, Burkholderia, Enterobacter, Erwinia, Azospirillum, Acetobacter, Azoarcus, Beijerinckia, Herbaspirillum, and Gluconacetobacter isolated from rhizosphere soil can also contribute up to 36 kg N ha−1 year−1 [70].

2.2. P Solubilization

Phosphorus is one of the macronutrients essential for legume growth and symbiotic nitrogen fixation. P application, along with Rhizobium tropici inoculation, resulted in an increase of plant parameters in Phaseolus vulgaris. There was also an enhanced effect on nodulation and N fixation with a 20-fold increase in ARA (acetylene reduction assay) activity with P application [89]. Phosphorus is required for nodule initiation, its development and functioning, along with the whole plant growth [90]. Application of low phosphorus markedly affected plant growth and SNF in soybean while an increase in P enhanced whole plant N associated with an increase in the number of nodules and nodule mass. Co-inoculation with P solubilizer along with rhizobia resulted in increased growth, nodulation and grain yield in common bean [17] and chickpea [91,92] in comparison to control.
In spite of the abundance of phosphorus in organic and inorganic forms in the soils, the available P remains low. When P is applied to the soil, it gets rapidly fixed, resulting in low P availability for the plants. As a result, a large proportion of P in soil is in insoluble form and only a small proportion gets immediately available to plants. Since the world reserves of non-renewable P rocks are becoming increasingly scarce and geologic P deposits will get depleted in 50–100 years [93], the application of P solubilizing microorganisms (PSMs) has shown potential in the transformation of unavailable forms of phosphorus to available form, which, in turn, can help in reducing the escalating price of rock phosphate due to fast depletion of its reserves.
Conversion of insoluble phosphates to orthophosphate by PSMs is an important PGPR trait, which can increase P nutrition in pulses (Table 3). The most efficient bacteria having P solubilization efficiency include Bacillus, Pseudomonas and Rhizobium. Fungi like Aspergillus and Penicillium can also convert insoluble phosphorus to soluble forms. Alikhani et al. [94] reported that amongst the rhizobial groups, Rhizobium leguminosarum bv. viciae exhibited highest inorganic P solubilization. Other inorganic P solubilizers include Sinorhizobium meliloti, Rhizobium leguminosarum bv. phaseoli, Mesorhizobium ciceri and Mesorhizobium mediterraneum. Mineral phosphate solubilization (MPS) by PSMs is due to the lowering of the pH of the medium either by H+ extrusion or due to excretion of low molecular weight organic acids such as gluconic acid which chelates the cations bound with phosphate [95]. In Gram-negative PSMs, extracellular oxidation of glucose to gluconic acid via quinoprotein (pyrroloquinoline quinine, PQQ) glucose dehydrogenase (coded by gcd gene) is suggested to be a major mechanism for MPS under P starvation [96]. However, glucose dehydrogenase is an inducible enzyme and the P-solubilizing capacity is adversely affected by the presence of organic acids such as succinate and malate. Inoculation with PSM and PGPR together with mineral phosphorus increases the efficiency of P fertilizer utilization and reduces P application by 50% without any significant reduction of grain yield in plants [97]. On the other hand, a large pool of organic P in most soils is as high as 80% of total P, which is not readily available to plants. Several PSMs capable of producing extracellular enzymes like phosphatase, phytase, etc. can hydrolyze organic P compounds. Thus, PGPR is an integral component of soil-P cycle, playing an important role in solubilization as well as mineralization of P, and transfer P between different soil fractions (between inorganic and organic P pools). In addition to PSM, P uptake is influenced by the association of arbuscular mycorrhizal fungi with roots and these processes occur as a natural response of plants to P deficiency. Arbuscular mycorrhiza can explore available P in the surrounding soil with the aid of hyphae [98] and can solubilize the inorganic phosphates as well as mineralize the organic P [99].

2.3. Production of Plant Growth Regulators (Hormones)

Many PGPRs have the ability to produce phytohormones that regulate plant growth. The prominent plant growth regulators and their analogues are auxins, cytokinins, and gibberellins which may modify root system architecture (RSA) [101,102,103]. These phytohormones affect physiological and morphological processes of plants at a very low concentration [104]. They can also change growth pattern and result in bigger and branched roots with a greater surface area. As a result, plants are able to access more nutrients from soil. Besides Nod factor signaling in legume-rhizobial symbiosis, phytohormones are known to play an important role in proper symbiotic development [105].
Auxin is an important group of hormones, which influence plant development through organogenesis, tropic responses, cellular responses such as cell expansion, division, and differentiation, as well as gene regulation [106]. These hormones regulate rhizobial infection, infection thread progression and formation of nodule primordia during early nodulation [107,108,109]. Variety of auxins like IAA (indole-3-acetic acid), IBA (indole-3-butyric acid), IPA (indole-3-pyruvic acid), tryptophol (TOL) and ILA (indole lactic acid) are produced by PGPRs. Out of these, IAA is an essential auxin produced by Alcaligenes, Azospirillum, Pseudomonas, Pantoea, Rhizobium and Enterobacter in the presence of L-tryptophan as a precursor. However, the pure culture of fluorescent Pseudomonas sp. produces IAA both in the presence and absence of tryptophan. IAA is also present in the nodules of legumes in much higher quantity than in the roots [105] and auxin accumulation in nodules could be derived from rhizobia. The rhizobial production of IAA in legumes is induced by plant flavonoids [110]. The role of IAA in plant-microbe interactions varies from phytostimulation and pathogenesis, as well as the degradation of aromatic amino acids [111]. The inoculation of IAA-producing Pseudomonas thivervalensis induces plant growth at a low cell concentration (105 CFU mL−1), however, high cell load (>106 CFU mL−1) is proved to be inhibitory [112]. The production of IAA by Azospirillum, Agrobacterium, Pseudomonas and Erwinia increases seedling root length, root hairs, root branching and root surface area [113]. IAA producing Rhizobium strains showed enhanced lateral root development and increased nodulation [114] with delayed nodule senescence [115]. On the other hand, IAA- deficient mutants of Bradyrhizobium elkanii USDA 31 showed a reduced number of nodules in soybean [116]. Failure to develop a mutant for IAA production indicates multiple pathways involved in the production of this hormone, and IAA can be produced via both tryptophan—dependent and tryptophan—independent pathways. In tryptophan dependent pathways, at least five different pathways such as indole-3-acetamide (IAM), indole-3-acetonitrile (IAN), indole-3-pyruvate (IPyA), tryptamine (TAM) and tryptophan side-chain oxidase (TSO) pathways are reported, in which the source of tryptophan can be either degrading roots or bacterial cell exudates [111]. IPyA pathway is linked to rhizosphere fitness, whereas IAM route is associated with pathogenesis [117].
Cytokinins (CK) are purine derivatives characterized by their potential to promote cell division (cytokinesis), cell enlargement and tissue expansion in the plant. Its production has been documented in Azotobacter, Azospirillum, Rhizobium, Bacillus, Burkholderia, Klebsiella, Paenibacillus and Pseudomonas species [118,119,120,121,122,123]. Cytokinins increase root surface area through the enhanced formation of adventitious and lateral roots, and affect apical dominance, axillary bud growth and leaf senescence. CKs are also involved in signal mediation from roots to shoots under environmental stresses [124]. The cytokinin producing PGPRs also affect the auxin/cytokinin ratio, which in turn regulates plant root architecture [124]. Cytokinins enhance plant growth in soybean, rapeseed and other crops [121,122,123,125]. These are also known to play a vital role in rhizobial infection and nodule differentiation in legumes [126]. Nod- mutant of Rhizobium harboring constitutive trans-zeatin secretion (tzs) gene mimics the morphogenetic effects of Nod factors and stimulates expression of early nodulin gene (ENOD2) in Medicago sativa [127]. Strains of Sinorhizobium sp. and Mesorhizobium loti produce four different types of CKs viz., nucleotides (CK-NT), ribosides (CK-RB), free bases (CK-FB) and methyl-thiol CK (CK-MET). The CK-MET is the predominant cytokinin, however, CK-FB is the most biologically active form secreted out [128]. It has been shown that exogenous application of low level of cytokinins was stimulatory, while elevated concentration reduced nodule formation in soybean [129]. The cytokinin receptor mutant phenotype of Medicago truncatula and Lotus japonicus produced defective nodules [130,131]. Analysis of wild-type and Fix- sym33 (gene encoding transcription factor IPD3/CYCLOPS regulates infection process and nodule differentiation), as well as sym40 (gene coding for EFD transcription factor that negatively controls nodulation) mutants of pea revealed a low level of trans-zeatin riboside in mutant nodules, suggesting the role of plant CKs in infection thread formation and bacteroid differentiation [132].
Use of cytokinin producing Penibacillus polymyxa affects abscisic acid (ABA) signaling of plants or rhizobia-elicited nodulation [133]. The cytokinin–ABA antagonism is the result of metabolic interactions due to their common biosynthetic origin. The inoculation with cytokinin producing bacteria stimulates shoot growth and magnifies ABA content; thus, eliciting stomatal closure under drought conditions [134]. Inoculation of Arabidopsis thaliana with Azospirillum brasilense Sp245 increased the plant’s ABA content and helped in stress alleviation [135]. Similarly, Pseudomonas putida H-2-3 inoculation reduced stress induced ABA accumulation in soybean plant [136]. A low level of endogenous ABA promotes nodulation efficiency and nitrogen fixation. The enhanced nitrogen fixation is correlated with decreased nitric oxide (NO) production in root nodules without concomitant increase in nifH gene expression [137]. It was reported that the exogenous ABA application after rhizobial inoculation suppressed nodulation, while ABA content lower than the normal enhanced nodule formation in Lotus japonicus [138]. Studies suggest that ABA induces nodule senescence [139,140].
Gibberellins (GAs) are tetracyclic diterpenoids that regulate germination, stem elongation, flowering and fruiting in plants [141]. Production of GAs by Achromobacter, Acinetobacter, Azospirillum, Agrobacterium, Azotobacter, Bacillus, Herbaspirillum, Gluconobacter, Pseudomonas and Rhizobia is well documented [142,143,144,145]. Inoculation of Azospirillium sp. reversed rice dwarfism [146] by metabolizing inactive GA precursors into in planta active gibberellins [147]. The presence of cytochrome p450 monooxygenase gene cluster involved in GA biosynthetic pathway is reported in Rhizobium NGR234 [148] and Bradyrhizobium japonicum [149]. The genomic analysis of Bradyrhizobium japonicum USDA 110 provided first evidence for the role of diterpenoid operon in GA biosynthesis [150]. Tatsukami and Ueda [151] found that GA synthetic genes are distributed in rhizobial species viz., Mesorhizobium loti, Bradyrhizobium japonicum, Sinorhizobium (Ensifer) fredii and Rhizobium etli that inhabit determinate nodules. They observed increased number of nodules in Lotus japonicus with GA- deficient Mesorhizobium loti mutant and suggested that the putative rhizobial GA possibly regulates optimal N fixation and prevents delayed infection. The low concentration of GA (0.001 mM) promotes nodule formation, while high levels of GA inhibit infection thread formation in pea [152]. GAs differentially influence infection thread formation in root epidermis and nodule organogenesis in cortex cells of legume root nodules. GA- deficient root phenotypes of pea reduced nodule initiation and development by producing more ethylene, which negatively affects nodule formation [152]. The GA- mutant line (na-1) showed few underdeveloped nodules, smaller bacteroids with broken peribacteroid membranes that showed reduced nitrogen fixation [152,153]. The application of bioactive GA3 significantly increased the number of nodules compared to wild type [153]. It was also observed that a reduced nodule number in Lotus japonicus and Medicago truncatula with application of GA biosynthesis inhibitors was due to disruption in DELLA proteins (transcriptional activator of GA signaling) [154,155,156]. Changes in the expression of early nodulation gene in DELLA- deficient pea could be due to disruption in lipo-chitooligosaccharide (LCO) or Nod factor signaling [153,157]. Expression analysis of pea plants treated with bioactive GA3 showed a negative effect of GA on the nodule senescence [158]. This study revealed that the stimulatory effect of GA application is associated with the down regulation of senescence-associated genes (encoding cysteine proteases 1 and 15a, thiol protease, bZIP transcription factor, 1 aminocyclopropane-1-carboxylate (ACC) synthase, ACC oxidase, and aldehyde oxidase). It was also observed that GA treated plants decrease senescence zone, increase nitrogen fixation zone, nodule size, and stimulate meristem bifurcation.
Ethylene is another key phytohormone which evokes physiological responses in plants at low concentrations. However, elevated levels of ethylene suppress shoot and root growth as well as inhibit nodule development by suppressing the infection thread formation [159,160]. The production of IAA by PGPR activates ACC (1-aminocyclopropane-1-carboxylate) synthase, leading to the production of ACC, which is an ethylene precursor in plants [161]. Certain strains of rhizobia capable of producing ACC deaminase can deaminate ACC to ammonia and α-ketobutyrate, which in turn can reduce the level of ethylene’s inhibition on root elongation [162]. This process can increase nodule number, nitrogen content and plant growth [163]. Mesorhizobium strains expressing exogenous ACC deaminase activity improved nodulation ability in chickpea [164]. The genomes of Rhizobium leguminosarum bv. viciae 128C53K [160], Bradyrhizobium japonicum USDA110 [150], Mesorhizobium sp. MAFF303099 [165], and Mesorhizobium ciceri bv. biserrulae WSM1271 [166] are reported to have a structural gene (acdS) encoding for ACC deaminase. Moreover, in Rhizobium, NifA (positive regulator of nif gene) regulated acdS expression associated with decreased rate of nodule senescence and increased amount of nitrogen fixation [167]. On the other hand, AcdR (leucine responsive regulatory protein) located in upstream of acdS gene regulated acdS expression that facilitates nodule formation [162]. Like rhizobia, ACC deaminase producing rhizobacteria can reduce ethylene inhibition and plant growth under biotic and abiotic stress conditions (Table 4). In addition to plant growth promotion and root system architecture, the phytohormones produced by PGPRs are involved in defense signaling network through jasmonate and salicylic acid pathways [168]. Although the synthesis of phytohormones by microbes is well documented, their role in the modulation of plant hormone balance is not fully understood.

3. Influence of PGPR Strains on Plant Growth Promotion and Nutrient Uptake

Plant growth-promoting rhizobacteria either alone or in combinations can improve the nutrient use efficiency, thus reducing the application of chemical fertilizers. Combined inoculation of rhizobia and rhizobacteria showed a positive effect on root nodulation and growth in legumes (Table 5). The basic mechanisms involved in this synergistic activity are by altering the host’s secondary metabolism and/or eliminating competition of rhizobia with deleterious microorganisms for colonization of the plants. Alteration in the flavonoid metabolism was another mechanism of synergistic activity of PGPR and rhizobia. Increase in plant yield with PGPR inoculation is attributed to improved root development that facilitates water and nutrient uptake [17,92,182]. Organic acid secretions by PGPRs via proton pump through ATPase [183] can also cause acidification of rhizosphere, which in turn increases the plant uptake of mineral nutrients such as Ca, K, Fe, Cu, Mn and Zn [184]. Inoculation with Azospirillum has shown to modify root morphology by increasing finer roots (with greater surface area and lower C costs to plants), root hair density, root branching and conferred greater tolerance to drought stress in common bean [185] and soybean [182]. Azospirillum improved root nodulation by creating additional sites for rhizobial root infection [186] as well as induced nod genes in Bradyrhizobium japonicum USDA 110 at lower–density inoculum through inter-species quorum sensing (QS) communication [187]. PGPRs also alleviate salt and drought stress by altering physiological and molecular processes in plants. Enhanced nutrient uptake and amelioration of adverse effect of salt stress in soybean have been observed with Bacillus firmus SW5 inoculation [19]. This strain has significantly boosted proline, glycine betaine content, antioxidant activities and stress-responsive gene expression (GmVSP, GmPHD2, GmbZIP62, GmWRKY54, GmOLPb, CHS) besides promoting root system architecture. Upregulation of AUX/IAA1 (transcriptional repressor of auxin responsive gene), TaCTR1 (regulatory component of the ethylene signaling pathway) and TaDREB2 (dehydration responsive element binding2) genes with inoculation of PGPR under salt and drought stress conditions has also been demonstrated [188]. Tripartite symbiosis of rhizobial and arbuscular mycorrhizal fungi with legumes improved N and P uptake. Transcriptomic analysis in soybean revealed that rhizobial nodulation was enhanced with AM fungi colonization. High transcript levels of genes encoding for endo-ß-1-4-glucanase (responsible for cell wall degradation during root nodule formation), early nodulin and carbonic anhydrase (helps in nodule development) in rhizobial-AM symbiosis suggested the contribution of AM fungal colonization to biological nitrogen fixation [189]. Our recent study showed that chickpea seeds inoculated with culturable endophytic fungi (Piriformospora indica) and Mesorhizobium ciceri had a synergistic effect with nodulation and nutrient uptake [92]. The use of antibiotic producing actinobacteria as PGPR could offer a competitive advantage over other microbial communities. The inoculation with Streptomyces species enhanced mesorhizobial nodulation and plant growth in chickpea under field conditions [190]. Tokala group [191] observed that dual inoculation of plant-growth promoting Streptomyces lydicus WYEC 108 with Rhizobium leguminosarum enhanced nodulation and nitrogen fixation in pea. This study showed that Streptomyces lydicus colonizes the root hairs of pea plants and helps in rhizobial infection, root nodule initiation and bacteroid differentiation.

4. Molecular Techniques Used in PGPR Study

For a long time, research has focused on various biochemical and inoculation-based methods to study PGPR, but with recent advances in molecular technologies, the huge amount of genomic, metagenomic, transcriptomic and proteomic data are made available on the worldwide web. Genomic analysis of PGPRs can be divided into two broad categories; namely, (a) whole-genome sequencing analysis of PGPR species where the entire chromosome and plasmid are sequenced and annotated (Table 6), and (b) partial/targeted genome or specific gene sequence analysis where a part of the genome is studied and used for characterization and comparison.
Whole-genome analysis using next-generation sequencing (NGS) gives a detailed account of an organism’s genetics. The most popular gene in this category is 16S ribosomal DNA/RNA, which bears a unique marker of identification of PGPR at the genus level. 16S–23S intra genomic spacer (IGS) has also been targeted for species level identification of PGPRs. The repetitive sequence-based PCR (rep-PCR), which is based on amplifying and sequencing of highly conserved inverted repeats has been performed by different research groups. These inverted repeats can be divided into two categories, namely repetitive extragenic palindromic (REP) elements and enterobacterial repetitive intergenic consensus (ERIC) sequences. Along with these, the 154 bp BOX element is also used to characterize genomes. All three methods, like ERIC-PCR, REP-PCR and BOX-PCR, are efficient to study the genetic diversity of PGPRs. Restriction fragment length polymorphism (RFLP) analysis of 16S rRNA gene was used to group PGPRs (ARDRA-amplified ribosomal DNA restriction analysis of 16S rDNA). A multi-locus sequence analysis (MLSA) of several housekeeping genes such as atpD, recA, rpoA, rpoB, thrC, dnaK, dnaJ, glnII, gap, glnA, gltA, gyrB and pnp is used for strain typing [207,208]. Arbitrary primers are used to amplify genome sequences in a random fashion, referred to as random amplified polymorphic DNA (RAPD) analysis. In addition, the amplification of specific genes (for instance 16S or 16S–23S (IGS amplicons)) coupled with secondary analysis methods like restriction profiling and denaturing gradient gel electrophoresis (DGGE) to deduce the groupings formed by mis-matches in restriction sites or difference in GC content of genomes has also been studied (Table 7).
Biological nitrogen fixation is one of the most important growth promoting mechanisms of rhizobacteria with primary involvement of nif genes coding for nitrogenase enzyme. While the nitrogenase enzyme is collectively coded by three nif genes, namely nifH, nifD and nifK, most of the studies are based on nifH PCR and sequencing. Phosphate solubilization by PGPRs involves the secretion of gluconic acid, which requires the enzyme glucose dehydrogenase and its cofactor PQQ [228]. PQQ is encoded by pqq operon which consists of 6 core genes: pqq A, B, C, D, E and F. Besides these, PGPRs produce several phytohormones like IAA, auxins, cytokinins and abscisic acid. Genes involved in IAA production include ipdC, amiE and nhase, but for auxin production, aec (auxin efflux carrier) gene is studied (Table 8). For iron sequestering, PGPRs produce siderophores which require the upregulation of sid gene. Pseudomonas employs a membrane receptor coded by pupA gene for the transport of iron-complexed siderophore back into the cell. NtEXP is another plant growth promoting gene which encodes expansin proteins and acc (ACC deaminase) gene is also implicated in promoting plant growth and strengthening defense mechanisms by inhibiting excessive ethylene production.

5. Conclusions and Prospects

The significance of legumes for improvement and sustenance of soil fertility has been known since crop domestication. Mixed cropping, intercropping and crop rotations of non-legumes with legumes have been employed to capitalize on the biological nitrogen fixation. Besides the natural association between N fixing rhizobia and legume crops, other beneficial rhizobacteria have been used as biofertilizers, phyto-stimulators and biopesticides for enhancing plant growth and soil health, and imparting stress tolerance to plants. However, growth promotion influenced by PGPRs under in vitro conditions needs to be confirmed under in situ conditions. The strain efficacy is usually related to the establishment and population density of the introduced strain in the rhizosphere. Hence, an in-depth study to predict their colonization potential, establishment and plant response under field conditions is essentially required. Diverse microbes form natural colonization with legume roots are known to help in nutrient acquisition and disease protection. Comprehensive information on the impact of potential PGPRs on the resident rhizosphere microbial community vis-a-vis the interactive effect of natural microbial community with the introduced PGPRs is required to delineate their rhizosphere competency and functional potential. The type and kind of molecules in root exudates secreted by plants determine the rhizosphere microbial diversity, in which only a fraction of PGPRs are culturable. Therefore, the identification of novel unculturable PGPRs using high throughput sequencing methods and devising strategies to improve their cultivation efficiency needs to be undertaken. Various environmental factors, plant genotypes and soil types can affect PGPR performance under field conditions. An understanding of genetic variation in beneficial host-PGPR interactions can be integrated in breeding varieties with heritable plant-associated microbial community for improving legume productivity.

Author Contributions

All authors contributed equally to the writing and editing of the manuscript. All authors have read and agreed to the published version of the manuscript.


The funding support provided by the CGIAR Research Program on Grain Legumes and Dryland Cereals (GLDC), ICARDA and ICAR, Government of India is duly acknowledged.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Kloepper, J.W. Plant Growth-Promoting Rhizobacteria on Radishes. In Proceedings of the 4th International Conference on Plant Pathogenic Bacter, Station de Pathologie Vegetale et Phytobacteriologie, INRA, Angers, France, 27 August–2 September 1978; Volume 2, pp. 879–882. [Google Scholar]
  2. Dobereiner, J.; Day, J.M. Associative Symbioses in Tropical Grasses: Characterization of Microorganisms and Dinitrogen-Fixing Sites. In Proceedings of the 1st International Symposium on Nitrogen Fixation; Washington State University Press: Pullman, WA, USA, 1976; Volume 2, pp. 518–538. [Google Scholar]
  3. Raaijmakers, J.M.; Paulitz, T.C.; Steinberg, C.; Alabouvette, C.; Moënne-Loccoz, Y. The rhizosphere: A playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 2009, 321, 341–361. [Google Scholar] [CrossRef][Green Version]
  4. Gopalakrishnan, S.; Sathya, A.; Vijayabharathi, R.; Varshney, R.K.; Gowda, C.L.L.; Krishnamurthy, L. Plant growth promoting rhizobia: Challenges and opportunities. 3 Biotech 2015, 5, 355–377. [Google Scholar] [CrossRef] [PubMed][Green Version]
  5. Compant, S.; Duffy, B.; Nowak, J.; Clément, C.; Barka, E.A. Use of plant growth-promoting bacteria for biocontrol of plant diseases: Principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 2005, 71, 4951–4959. [Google Scholar] [CrossRef] [PubMed][Green Version]
  6. Beneduzi, A.; Ambrosini, A.; Passaglia, L.M.P. Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. Genet. Mol. Biol. 2012, 35, 1044–1051. [Google Scholar] [CrossRef] [PubMed][Green Version]
  7. Ali, S.; Hameed, S.; Shahid, M.; Iqbal, M.; Lazarovits, G.; Imran, A. Functional characterization of potential PGPR exhibiting broad-spectrum antifungal activity. Microbiol. Res. 2020, 232, 126389. [Google Scholar] [CrossRef] [PubMed]
  8. Bais, H.P.; Weir, T.L.; Perry, L.G.; Gilroy, S.; Vivanco, J.M. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 2006, 57, 233–266. [Google Scholar] [CrossRef][Green Version]
  9. Sasse, J.; Martinoia, E.; Northen, T. Feed your friends: Do plant exudates shape the root microbiome? Trends Plant Sci. 2018, 23, 25–41. [Google Scholar] [CrossRef][Green Version]
  10. Jones, D.L.; Nguyen, C.; Finlay, R.D. Carbon flow in the rhizosphere: Carbon trading at the soil-root interface. Plant Soil 2009, 321, 5–33. [Google Scholar] [CrossRef]
  11. Badri, D.V.; Vivanco, J.M. Regulation and function of root exudates. Plant Cell Environ. 2009, 32, 666–681. [Google Scholar] [CrossRef]
  12. Steinkellner, S.; Lendzemo, V.; Langer, I.; Schweiger, P.; Khaosaad, T.; Toussaint, J.-P.; Vierheilig, H. Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 2007, 12, 1290–1306. [Google Scholar] [CrossRef][Green Version]
  13. Gamalero, E.; Glick, B.R. Mechanisms used by plant growth-promoting bacteria. In Bacteria in Agrobiology: Plant Nutrient Management; Maheshwari, D., Ed.; Springer: Berlin/Heidelberg, Germany, 2011; pp. 17–46. [Google Scholar] [CrossRef]
  14. Malik, K.; Bilal, R.; Mehnaz, S.; Rasyl, G.; Mirza, M.S.; Ali, A. Association of nitrogen-fixing, plant-growth-promoting rhizobacteria (PGPR) with kallar grass and rice. Plant Soil 1997, 194, 37–44. [Google Scholar] [CrossRef]
  15. Alori, E.T.; Glick, B.R.; Babalola, O.O. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front. Microbiol. 2017, 8, 971. [Google Scholar] [CrossRef] [PubMed][Green Version]
  16. Egamberdieva, D.; Wirth, S.J.; Alqarawi, A.A.; Abd-Allah, E.F.; Hashem, A. Phytohormones and beneficial microbes: Essential components for plants to balance stress and fitness. Front. Microbiol. 2017, 8, 2104. [Google Scholar] [CrossRef]
  17. Korir, H.; Mungai, N.W.; Thuita, M.; Hamba, Y.; Masso, C. Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil. Front. Plant Sci. 2017, 8, 141. [Google Scholar] [CrossRef][Green Version]
  18. Ngumbi, E.; Kloepper, J. Bacterial-mediated drought tolerance: Current and future prospects. Appl. Soil Ecol. 2016, 105, 109–125. [Google Scholar] [CrossRef]
  19. El-Esawi, M.A.; Alaraidh, I.A.; Alsahli, A.A.; Alamri, S.A.; Ali, H.M.; Alayafi, A.A. Bacillus firmus (SW5) augments salt tolerance in soybean (Glycine max L.) by modulating root system architecture, antioxidant defense systems and stress-responsive genes expression. Plant Physiol. Biochem. 2018, 132, 375–384. [Google Scholar] [CrossRef]
  20. Ryu, C.M.; Farag, M.A.; Hu, C.H.; Reddy, M.S.; Wei, H.X.; Paré, P.W.; Kloepper, J.W. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. USA 2003, 100, 4927–4932. [Google Scholar] [CrossRef] [PubMed][Green Version]
  21. Sharma, M.; Mishra, V.; Rau, N.; Sharma, R.S. Increased iron-stress resilience of maize through inoculation of siderophore-producing Arthrobacter globiformis from mine. J. Basic Microbiol. 2016, 56, 719–735. [Google Scholar] [CrossRef]
  22. Kloepper, J.W.; Ryu, C.M. Bacterial endophytes as elicitors of induced systemic resistance. In Microbial Root Endophytes; Springer: Berlin/Heidelberg, Germany, 2006; pp. 33–52. [Google Scholar]
  23. Valverde, G.; Otabbong, E. Evaluation of N2-fixation measured by the 15N-dilution and N-difference methods in Nicaraguan and Ecuadorian Phaseolus vulgaris L. plants inoculated with Rhizobium leguminosarum biovar. Acta Agric. Scand. 1997, 47, 71–80. [Google Scholar]
  24. Akhtar, M.S.; Siddiqui, Z.A. Glomus intraradices, Pseudomonas alcaligenes, and Bacillus pumilus: Effective agents for the control of root-rot disease complex of chickpea (Cicer arietinum L.). J. Gen. Plant Pathol. 2008, 74, 53–60. [Google Scholar] [CrossRef]
  25. Verma, J.P.; Yadav, J.; Tiwari, K.N. Enhancement of nodulation and yield of chickpea by co-inoculation of indigenous Mesorhizobium spp. and plant growth–promoting rhizobacteria in eastern Uttar Pradesh. Commun. Soil Sci. Plant Anal. 2012, 43, 605–621. [Google Scholar] [CrossRef]
  26. Hamaoui, B.; Abbadi, J.; Burdman, S.; Rashid, A.; Sarig, S.; Okon, Y. Effects of inoculation with Azospirillum brasilense on chickpeas (Cicer arietinum) and faba beans (Vicia faba) under different growth conditions. Agronomy 2001, 21, 553–560. [Google Scholar] [CrossRef][Green Version]
  27. Abdiev, A.; Khaitov, B.; Toderich, K.; Park, K.W. Growth, nutrient uptake and yield parameters of chickpea (Cicer arietinum L.) enhance by Rhizobium and Azotobacter inoculations in saline soil. J. Plant Nutr. 2019, 42, 2703–2714. [Google Scholar] [CrossRef]
  28. Kumar, R.; Chandra, R. Influence of PGPR and PSB on Rhizobium leguminosarum bv. viciae strain competition and symbiotic performance in lentil. World J. Agric. Sci. 2008, 4, 297–301. [Google Scholar]
  29. Saini, P.; Khanna, V. Evaluation of native rhizobacteria as promoters of plant growth for increased yield in lentil (Lens culinaris). Recent Res. Sci. Technol. 2012, 4, 5–9. [Google Scholar]
  30. Mishra, P.K.; Bisht, S.C.; Ruwari, P.; Joshi, G.K.; Singh, G.; Bisht, J.K.; Bhatt, J.C. Bioassociative effect of cold tolerant Pseudomonas spp. and Rhizobium leguminosarum-PR1 on iron acquisition, nutrient uptake and growth of lentil (Lens culinaris L.). Eur. J. Soil Biol. 2011, 47, 35–43. [Google Scholar] [CrossRef]
  31. Tsigie, A.; Tilak, K.V.B.R.; Saxena, A.K. Field response of legumes to inoculation with plant growth-promoting rhizobacteria. Biol. Fertil. Soils 2011, 47, 971–974. [Google Scholar] [CrossRef]
  32. Zaidi, A.; Khan, M.S. Co-inoculation effects of phosphate solubilizing microorganisms and Glomus fasciculatum on green gram-Bradyrhizobium symbiosis. Turk. J. Agric. For. 2006, 30, 223–230. [Google Scholar]
  33. Qureshi, M.A.; Shakir, M.A.; Iqbal, A.; Akhtar, N.; Khan, A. Co-inoculation of phosphate solubilizing bacteria and rhizobia for improving growth and yield of mungbean (Vigna radiata L.). J. Anim. Plant Sci. 2011, 21, 491–497. [Google Scholar]
  34. Sharma, A.; Johri, B.N. Combat of iron-deprivation through a plant growth promoting fluorescent Pseudomonas strain GRP3A in mung bean (Vigna radiata L. Wilzeck). Microbiol. Res. 2003, 158, 77–81. [Google Scholar] [CrossRef]
  35. Noreen, R.; Ali, S.A.; Hasan, K.A.; Sultana, V.; Ara, J.; Ehteshamul-Haque, S. Evaluation of biocontrol potential of fluorescent Pseudomonas associated with root nodules of mungbean. Crop Prot. 2015, 75, 18–24. [Google Scholar] [CrossRef]
  36. Desai, G.P.K.S.; Pinisetty, S. Impact of seed bacterization with PGPR on growth and nutrient uptake in different cultivable varieties of green gram. Asian J. Agric. Res. 2015, 9, 113–122. [Google Scholar] [CrossRef]
  37. Harish, S.; Manjula, K.; Podile, A.R. Fusarium udum is resistant to the mycolytic activity of a biocontrol strain of Bacillus subtilis AF1. FEMS Microbiol. Ecol. 1998, 25, 385–390. [Google Scholar] [CrossRef]
  38. Dutta, S.; Morang, P.; Kumar, S.N.; Kumar, B.S.D. Fusarial wilt control and growth promotion of pigeon pea through bioactive metabolites produced by two plant growth promoting rhizobacteria. World J. Microbiol. Biotechnol. 2014, 30, 1111–1121. [Google Scholar] [CrossRef] [PubMed]
  39. Kumar, G.P.; Desai, S.; Reddy, G.; Amalraj, E.L.D.; Rasul, A.; Ahmed, S.K.M.H. Seed bacterization with fluorescent Pseudomonas spp. enhances nutrient uptake and growth of Cajanus cajan L. Commun. Soil Sci. Plant Anal. 2015, 46, 652–655. [Google Scholar] [CrossRef]
  40. Sharma, R.; Paliwal, J.S.; Chopra, P.; Dogra, D.; Pooniya, V.; Bisaria, V.S.; Swarnalakshmi, K.; Sharma, S. Survival, efficacy and rhizospheric effects of bacterial inoculants on Cajanus cajan. Agric. Ecosyst. Environ. 2017, 240, 244–252. [Google Scholar] [CrossRef]
  41. Dey, R.; Pal, K.K.; Bhatt, D.M.; Chauhan, S.M. Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol. Res. 2004, 159, 371–394. [Google Scholar] [CrossRef] [PubMed]
  42. Yuttavanichakul, W.; Lawingsa, P.; Wongkaew, S.; Teaumroong, N.; Boonkerd, N.; Nomura, N.; Tittabutr, P. Improvement of peanut rhizobial inoculant by incorporation of plant growth promoting rhizobacteria (PGPR) as biocontrol against the seed borne fungus, Aspergillus niger. Biol. Control 2012, 63, 87–97. [Google Scholar] [CrossRef]
  43. Masciarelli, O.; Llanes, A.; Luna, V. A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol. Res. 2014, 169, 609–615. [Google Scholar] [CrossRef]
  44. Molla, A.H.; Shamsuddin, Z.H.; Halimi, M.S.; Morziah, M.; Puteh, A.B. Potential for enhancement of root growth and nodulation of soybean co-inoculated with Azospirillum and Bradyrhizobium in laboratory systems. Soil Biol. Biochem. 2001, 33, 457–463. [Google Scholar] [CrossRef]
  45. Argaw, A. Evaluation of Co-inoculation of Bradyrhizobium japonicum and phosphate solubilizing Pseudomonas spp. effect on soybean (Glycine max L. (Merr.)) in Assossa Area. J. Agric. Sci. Technol. 2012, 14, 213–224. [Google Scholar]
  46. Cattelan, A.J.; Hartel, P.G.; Fuhrmann, J.J. Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Sci. Soc. Am. J. 1999, 63, 1670–1680. [Google Scholar] [CrossRef]
  47. Elkoca, E.; Turan, M.; Dinmez, M.F. Effects of single, dual and triple inoculations with Bacillus subtilis, Bacillus megaterium and Rhizobium leguminosarum bv. Phaseoli on nodulation, nutrient uptake, yield and yield parameters of common bean (Phaseolus vulgaris L. Cv. ’Elkoca-05’). J. Plant Nutr. 2010, 33, 2104–2119. [Google Scholar] [CrossRef]
  48. Figueiredo, M.V.B.; Martinez, C.R.; Burity, H.A.; Chanway, C.P. Plant growth-promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean (Phaseolus vulgaris L.). World J. Microbiol. Biotechnol. 2008, 24, 1187–1193. [Google Scholar] [CrossRef]
  49. Yadegari, M.; Rahmani, H.A.; Noormohammadi, G.; Ayneband, A. Evaluation of bean (Phaseolus vulgaris) seeds inoculation with Rhizobium phaseoli and plant growth promoting rhizobacteria on yield and yield components. Pak. J. Biol. Sci. 2008, 11, 1935–1939. [Google Scholar] [CrossRef][Green Version]
  50. Burdman, J.; Kigel, Y.O. Effects of Azospirillum brasilense on nodulation and growth of common bean (Phaseolus vulgaris L.). Soil Biol. Biochem. 1997, 29, 923–929. [Google Scholar] [CrossRef]
  51. Sánchez, A.C.; Gutiérrez, R.T.; Santana, R.C.; Urrutia, A.R.; Fauvart, M.; Michiels, J.; Vanderleyden, J. Effects of co-inoculation of native Rhizobium and Pseudomonas strains on growth parameters and yield of two contrasting Phaseolus vulgaris L. genotypes under Cuban soil conditions. Eur. J. Soil Biol. 2014, 62, 105–112. [Google Scholar] [CrossRef]
  52. Samy, A.; El-Azeem, A.; Mehana, T.A.; Shabayek, A. Response of faba bean (Vicia faba L.) to inoculation with plant growth-promoting rhizobacteria. Catrina. Int. J. Environ. Sci. 2007, 2, 67–75. [Google Scholar]
  53. Rodelas, B.; González-López, J.; Pozo, C.; Salmerón, V.; Martínez-Toledo, M.V. Response of faba bean (Vicia faba L.) to combined inoculation with Azotobacter and Rhizobium leguminosarum bv. viceae. Appl. Soil Ecol. 1999, 12, 51–59. [Google Scholar] [CrossRef][Green Version]
  54. Radwan, S.S.; Dashti, N.; El-Nemr, I.M. Enhancing the growth of Vicia faba plants by microbial inoculation to improve their phytoremediation potential for oily desert areas. Int. J. Phytoremediation 2005, 7, 19–32. [Google Scholar] [CrossRef]
  55. Egamberdiyeva, D.; Höflich, G. Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. J. Arid Environ. 2004, 56, 293–301. [Google Scholar] [CrossRef]
  56. Zahir, Z.A.; Munir, A.; Asghar, H.N.; Shaharoona, B.; Arshad, M. Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J. Microbiol. Biotechnol. 2008, 18, 958–963. [Google Scholar] [PubMed]
  57. Mishraa, P.K.; Bishta, S.C.; Jeevanandana, K.; Kumara, S.; Bisht, J.K.; Bhatt, J.C. Synergistic effect of inoculating plant growth-promoting Pseudomonas spp. and Rhizobium leguminosarum-FB1 on growth and nutrient uptake of rajmash (Phaseolus vulgaris L.). Agron. Soil Sci. 2014, 60, 799–815. [Google Scholar] [CrossRef]
  58. Dastager, S.G.; Deepa, C.K.; Pandey, A. Plant growth promoting potential of Pontibacter niistensis in cowpea (Vigna unguiculata (L.) Walp.). Appl. Soil Ecol. 2011, 49, 250–255. [Google Scholar] [CrossRef]
  59. Zhukov, V.A.; Shtark, O.Y.; Borisov, A.Y.; Tikhonovich, I.A. Breeding to improve symbiotic effectiveness of legumes. In Plant Breeding from Laboratories to Fields; Intech: Rijeka, Croatia, 2013; pp. 167–207. [Google Scholar]
  60. Fred, E.B.; Baldwin, I.L.; McCoy, E. Root Nodule Bacteria and Leguminous Plants; University of Wisconsin: Madison, WI, USA, 1932. [Google Scholar]
  61. Graham, P.H. Studies on the utilisation of carbohydrates and Krebs cycle intermediates by Rhizobia, using an agar plate method. Antonie Van Leeuwenhoek 1964, 30, 68–72. [Google Scholar] [CrossRef] [PubMed]
  62. Jarvis, B.D.W.; Van Berkum, P.; Chen, W.X.; Nour, S.M.; Fernandez, M.P.; Cleyet-Marel, J.C.; Gillis, M. Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int. J. Syst. Evol. Microbiol. 1997, 47, 895–898. [Google Scholar] [CrossRef][Green Version]
  63. Young, J.P.W. Phylogeny and taxonomy of rhizobia. Plant Soil 1996, 186, 45–52. [Google Scholar] [CrossRef]
  64. Berrada, H.; Fikri-Benbrahim, K. Taxonomy of the rhizobia: Current perspectives. Microbiol. Res. J. Int. 2014, 4, 616–639. [Google Scholar] [CrossRef][Green Version]
  65. Zuanazzi, J.A.S.; Clergeot, P.H.; Quirion, J.-C.; Husson, H.-P.; Kondorosi, A.; Ratet, P. Production of Sinorhizobium meliloti nod gene activator and repressor flavonoids from Medicago sativa roots. Mol. Plant Microbe. Interact. 1998, 11, 784–794. [Google Scholar] [CrossRef][Green Version]
  66. Sprent, J.I.; Ardley, J.K.; James, E.K. From North to South: A latitudinal look at legume nodulation processes. S. Afr. J. Bot. 2013, 89, 31–41. [Google Scholar] [CrossRef][Green Version]
  67. Fischer, H.-M. Genetic regulation of nitrogen fixation in rhizobia. Microbiol. Rev. 1994, 58, 352–386. [Google Scholar] [CrossRef] [PubMed]
  68. Ishizuka, J. Trends in biological nitrogen fixation research and application. In Biological Nitrogen Fixation for Sustainable Agriculture; Ladha, J.K., George, T., Bohlool, B.B., Eds.; Developments in Plant and Soil Sciences; Springer: Dordrecht, The Netherlands, 1992; Volume 49, pp. 197–209. [Google Scholar] [CrossRef]
  69. Brockwell, J.; Bottomley, P.J.; Thies, J.E. Manipulation of rhizobia microflora for improving legume productivity and soil fertility: A critical assessment. Plant Soil 1995, 174, 143–180. [Google Scholar] [CrossRef]
  70. Kahindi, J.H.P.; Woomer, P.; George, T.; de Souza Moreira, F.M.; Karanja, N.K.; Giller, K.E. Agricultural intensification, soil biodiversity and ecosystem function in the tropics: The role of nitrogen-fixing bacteria. Appl. Soil Ecol. 1997, 6, 55–76. [Google Scholar] [CrossRef]
  71. Peoples, M.B.; Herridge, D.F.; Ladha, J.K. Biological nitrogen fixation: An efficient source of nitrogen for sustainable agricultural production? In Management of Biological Nitrogen Fixation for the Development of More Productive and Sustainable Agricultural Systems; Springer: Dordrecht, The Netherlands, 1995; pp. 3–28. [Google Scholar]
  72. Muresu, R.; Polone, E.; Sulas, L.; Baldan, B.; Tondello, A.; Delogu, G.; Cappuccinelli, P.; Alberghini, S.; Benhizia, Y.; Benhizia, H. Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol. Ecol. 2008, 63, 383–400. [Google Scholar] [CrossRef] [PubMed][Green Version]
  73. Zhao, K.; Tung, C.-W.; Eizenga, G.C.; Wright, M.H.; Ali, M.L.; Price, A.H.; Norton, G.J.; Islam, M.R.; Reynolds, A.; Mezey, J.; et al. Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat. Commun. 2011, 2, 1–10. [Google Scholar] [CrossRef]
  74. Dudeja, S.S.; Giri, R.; Saini, R.; Suneja-Madan, P.; Kothe, E. Interaction of endophytic microbes with legumes. J. Basic Microbiol. 2012, 52, 248–260. [Google Scholar] [CrossRef]
  75. Carranca, C.; De Varennes, A.; Rolston, D. Biological nitrogen fixation by fababean, pea and chickpea under field conditions estimated by the 15N isotope dilution technique. Eur. J. Agron. 1999, 10, 49–56. [Google Scholar] [CrossRef]
  76. Horn, C.P.; Dalal, R.C.; Birch, C.J.; Doughton, J.A. Nitrogen fixation in chickpea as affected by planting time and tillage practice. In Proceedings of the 8th Australian Agronomy Conference, Queensland, Australia, 29 January–2 February 1996; pp. 1–5. [Google Scholar]
  77. Rao, J.V.D.K.K.; Dart, P.J. Nodulation, nitrogen fixation and nitrogen uptake in pigeonpea (Cajanus cajan (L.) Millsp) of different maturity groups. Plant Soil 1987, 99, 255–266. [Google Scholar] [CrossRef]
  78. Delić, D.; Stajković-Srbinović, O.; Kuzmanović, D.; Rasulić, N.; Mrvić, V.; Andjelović, S.; Knežević-Vukčević, J. Effect of bradyrhizobial inoculation on growth and seed yield of mungbean in Fluvisol and Humofluvisol. Afr. J. Microbiol. Res. 2011, 5, 3946–3957. [Google Scholar]
  79. Kelstrup, L.; Rowarth, J.S.; Williams, P.H.; Ronson, C. Nitrogen fixation in peas (Pisum sativum L.), lupins (Lupinus angustifolius L.) and lentils (Lens culinaris Medik.). Proc. Agron. Soc. N. Z. 1996, 26, 71–74. [Google Scholar]
  80. Bremer, E.; Van Kessel, C.; Nelson, L.; Rennie, R.J.; Rennie, D.A. Selection of Rhizobium leguminosarum strains for lentil (Lens culinaris) under growth room and field conditions. Plant Soil 1990, 121, 47–56. [Google Scholar] [CrossRef]
  81. Usukh, B. The Impact of Lentil and Field Pea Seeding Rates on Dinitrogen Fixation and Subsequent Nitrogen Benefits in an Organic Cropping System. Ph.D. Thesis, University of Saskatchewan, Saskatoon, SK, Canada, 2010. [Google Scholar]
  82. Sparrowl, S.D.; Cochran, L.; Spanow, E.B. Herbage yield and nitrogen accumulation by seven legume crops on acid and neutral soils in a subarctic environment. Can. J. Plant Sci. 1993, 73, 1037–1045. [Google Scholar] [CrossRef]
  83. Valverde, A.; Burgos, A.; Fiscella, T.; Rivas, R.; Velazquez, E.; Rodríguez-Barrueco, C.; Cervantes, E.; Chamber, M.; Igual, J.-M. Differential effects of coinoculations with Pseudomonas jessenii ps06 (a phosphate-solubilizing bacterium) and Mesorhizobium ciceri C-2/2 strains on the growth and seed yield of chickpea under greenhouse and field conditions. In Proceedings of the First International Meeting on Microbial Phosphate Solubilization; Springer: Dordrecht, The Netherlands, 2007; pp. 43–50. [Google Scholar]
  84. Hardarson, G.; Bliss, F.A.; Cigales-Rivero, M.R.; Henson, R.A.; Kipe-Nolt, J.A.; Longeri, L.; Manrique, A.; Pena-Cabriales, J.J.; Pereira, P.A.A.; Sanabria, C.A.; et al. Genotypic variation in biological nitrogen fixation by common bean. Plant Soil 1993, 152, 59–70. [Google Scholar] [CrossRef]
  85. Smith, D.L.; Hume, D.J. Comparison of assay methods for N2 fixation utilizing white bean and soybean. Can. J. Plant Sci. 1987, 67, 11–19. [Google Scholar] [CrossRef]
  86. Moawad, H.; El-din, S.M.S.B.; Khalafallah, M. Quantification of nitrogen fixation by the peanutl Rhizobium symbiotic system in a virgin sandy Soil. J. Plant Nutr. Soil Sci. 1986, 149, 668–673. [Google Scholar] [CrossRef]
  87. Peoples, M.B.; Bell, M.J.; Bushby, H.V.A. Effect of rotation and inoculation with Bradyrhizobium on nitrogen fixation and yield of peanut (Arachis hypogaea L., cv. Virginia Bunch). Aust. J. Agric. Res. 1992, 43, 595–607. [Google Scholar] [CrossRef]
  88. Toomsan, B.; McDonagh, J.F.; Limpinuntana, V.; Giller, K.E. Nitrogen fixation by groundnut and soyabean and residual nitrogen benefits to rice in farmers’ fields in Northeast Thailand. Plant Soil 1995, 175, 45–56. [Google Scholar] [CrossRef]
  89. Olivera, M.; Tejera, N.; Iribarne, C.; Ocana, A.; Lluch, C. Growth, nitrogen fixation and ammonium assimilation in common bean (Phaseolus vulgaris): Effect of phosphorus. Physiol. Plant. 2004, 121, 498–505. [Google Scholar] [CrossRef]
  90. Israel, D.W. Investigation of the role of phosphorus in symbiotic dinitrogen fixation. Plant Physiol. 1987, 84, 835–840. [Google Scholar] [CrossRef][Green Version]
  91. Rudresh, D.L.; Shivaprakash, M.K.; Prasad, R.D. Effect of combined application of Rhizobium, phosphate solubilizing bacterium and Trichoderma spp. on growth, nutrient uptake and yield of chickpea (Cicer aritenium L.). Appl. Soil Ecol. 2005, 28, 139–146. [Google Scholar] [CrossRef]
  92. Swarnalakshmi, K.; Pooniya, V.; Paul, S. Synergistic interaction of Piriformospora indica and microbial inoculants on symbiotic potential, plant nutrition and productivity of chickpea (Cicer arietinum). Indian J. Agron. 2017, 62, 481–488. [Google Scholar]
  93. Vassilev, N.; Someus, E.; Serrano, M.; Bravo, V.; Garcia Roman, M.; Reyes, A.; Vassileva, M. Novel Approaches in Phosphate-Fertilizer Production Based on Wastes Derived from Rock Phosphate Mining and Food Processing Industry; Nova Science Publishers: Hauppauge, NY, USA, 2009; pp. 387–391. [Google Scholar]
  94. Alikhani, H.A.; Saleh-Rastin, N.; Antoun, H. Phosphate solubilization activity of rhizobia native to iranian soils. In Proceedings of the First International Meeting on Microbial Phosphate Solubilization; Springer: Dordrecht, The Netherlands, 2007; pp. 35–41. [Google Scholar]
  95. Miller, S.H.; Browne, P.; Prigent-Combaret, C.; Combes-Meynet, E.; Morrissey, J.P.; O’Gara, F. Biochemical and genomic comparison of inorganic phosphate solubilization in Pseudomonas species. Environ. Microbiol. Rep. 2010, 2, 403–411. [Google Scholar] [CrossRef] [PubMed]
  96. Goldstein, A.H. Recent progress in understanding the molecular genetics and biochemistry of calcium phosphate solubilization by Gram negative bacteria. Biol. Agric. Hortic. 1995, 12, 185–193. [Google Scholar] [CrossRef]
  97. Yazdani, M.; Bahmanyar, M.A.; Pirdashti, H.; Esmaili, M.A. Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of corn (Zea mays L.). World Acad. Sci. Eng. Technol. 2009, 49, 90–92. [Google Scholar]
  98. Gyaneshwar, P.; Kumar, G.N.; Parekh, L.J.; Poole, P.S. Role of soil microorganisms in improving P nutrition of plants. Plant Soil 2002, 245, 83–93. [Google Scholar] [CrossRef]
  99. Feng, G.; Song, Y.C.; Li, X.L.; Christie, P. Contribution of arbuscular mycorrhizal fungi to utilization of organic sources of phosphorus by red clover in a calcareous soil. Appl. Soil Ecol. 2003, 22, 139–148. [Google Scholar] [CrossRef]
  100. Verma, J.P.; Yadav, J.; Tiwari, K.N.; Kumar, A. Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol. Eng. 2013, 51, 282–286. [Google Scholar] [CrossRef]
  101. Moubayidin, L.; Di Mambro, R.; Sabatini, S. Cytokinin-auxin crosstalk. Trends Plant Sci. 2009, 14, 557–562. [Google Scholar] [CrossRef]
  102. Overvoorde, P.; Fukaki, H.; Beeckman, T. Auxin control of root development. Cold Spring. Harb. Perspect. Biol. 2010, 2, a001537. [Google Scholar] [CrossRef][Green Version]
  103. Yaxley, J.R.; Ross, J.J.; Sherriff, L.J.; Reid, J.B. Gibberellin biosynthesis mutations and root development in pea. Plant Physiol. 2001, 125, 627–633. [Google Scholar] [CrossRef][Green Version]
  104. Arshad, M.; Frankenberger, W.T., Jr. Plant growth-regulating substances in the rhizosphere: Microbial production and functions. Adv. Agron. 1997, 62, 45–151. [Google Scholar] [CrossRef]
  105. Hirsch, A.M.; Fang, Y. Plant hormones and nodulation: What’s the connection? Plant Mol. Biol. 1994, 26, 5–9. [Google Scholar] [CrossRef]
  106. Teale, W.D.; Paponov, I.A.; Palme, K. Auxin in action: Signalling, transport and the control of plant growth and development. Nat. Rev. Mol. Cell Biol. 2006, 7, 847–859. [Google Scholar] [CrossRef] [PubMed]
  107. Breakspear, A.; Liu, C.; Roy, S.; Stacey, N.; Rogers, C.; Trick, M.; Morieri, G.; Mysore, K.S.; Wen, J.; Oldroyd, G.E.D. The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 2014, 26, 4680–4701. [Google Scholar] [CrossRef][Green Version]
  108. de Billy, F.; Grosjean, C.; May, S.; Bennett, M.; Cullimore, J.V. Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol. Plant Microbe. Interact. 2001, 14, 267–277. [Google Scholar] [CrossRef][Green Version]
  109. Laplaze, L.; Lucas, M.; Champion, A. Rhizobial root hair infection requires auxin signaling. Trends Plant Sci. 2015, 20, 332–334. [Google Scholar] [CrossRef]
  110. Prinsen, E.; Chauvaux, N.; Schmidt, J.; John, M.; Wieneke, U.; De Greef, J.; Schell, J.; Van Onckelen, H. Stimulation of indole-3-acetic acid production in Rhizobium by flavonoids. FEBS Lett. 1991, 282, 53–55. [Google Scholar] [CrossRef][Green Version]
  111. Spaepen, S.; Vanderleyden, J.; Remans, R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 2007, 31, 425–448. [Google Scholar] [CrossRef][Green Version]
  112. Persello-Cartieaux, F.; David, P.; Sarrobert, C.; Thibaud, M.-C.; Achouak, W.; Robaglia, C.; Nussaume, L. Utilization of mutants to analyze the interaction between Arabidopsis thaliana and its naturally root-associated Pseudomonas. Planta 2001, 212, 190–198. [Google Scholar] [CrossRef]
  113. Bashan, Y.; Holguin, G.; De-Bashan, L.E. Azospirillum-plant relationships: Physiological, molecular, agricultural, and environmental advances (1997–2003). Can. J. Microbiol. 2004, 50, 521–577. [Google Scholar] [CrossRef][Green Version]
  114. Pii, Y.; Crimi, M.; Cremonese, G.; Spena, A.; Pandolfini, T. Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biol. 2007, 7, 1–11. [Google Scholar] [CrossRef] [PubMed][Green Version]
  115. Camerini, S.; Senatore, B.; Lonardo, E.; Imperlini, E.; Bianco, C.; Moschetti, G.; Rotino, G.L.; Campion, B.; Defez, R. Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development. Arch. Microbiol. 2008, 190, 67–77. [Google Scholar] [CrossRef]
  116. Fukuhara, H.; Minakawa, Y.; Akao, S.; Minamisawa, K. The involvement of indole-3-acetic acid produced by Bradyrhizobium elkanii in nodule formation. Plant Cell Physiol. 1994, 35, 1261–1265. [Google Scholar] [CrossRef]
  117. Manulis, S.; Haviv-Chesner, A.; Brandl, M.T.; Lindow, S.E.; Barash, I. Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae. Mol. Plant Microbe. Interact. 1998, 11, 634–642. [Google Scholar] [CrossRef] [PubMed][Green Version]
  118. Nieto, K.F.; Frankenberger, W.T., Jr. Biosynthesis of cytokinins by Azotobacter chroococcum. Soil Biol. Biochem. 1989, 21, 967–972. [Google Scholar] [CrossRef]
  119. Sturtevant, D.B.; Taller, B.J. Cytokinin production by Bradyrhizobium japonicum. Plant Physiol. 1989, 89, 1247–1252. [Google Scholar] [CrossRef] [PubMed][Green Version]
  120. Conrad, K.; Bettin, B.; Neumann, S. The Cytokinin production of Azospirillum and Klebsiella possible ecological effects. In Physiology and Biochemistry of Cytokinins in Plants; Academic Publishing: The Hague, The Netherlands, 1992; Available online: (accessed on 30 May 2014).
  121. Timmusk, S.; Nicander, B.; Granhall, U.; Tillberg, E. Cytokinin production by Paenibacillus polymyxa. Soil Biol. Biochem. 1999, 31, 1847–1852. [Google Scholar] [CrossRef]
  122. García de Salamone, I.E.; Hynes, R.K.; Nelson, L.M. Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can. J. Microbiol. 2001, 47, 404–411. [Google Scholar] [CrossRef]
  123. Arkhipova, T.N.; Veselov, S.U.; Melentiev, A.I.; Martynenko, E.V.; Kudoyarova, G.R. Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 2005, 272, 201–209. [Google Scholar] [CrossRef]
  124. Aloni, R.; Aloni, E.; Langhans, M.; Ullrich, C.I. Role of cytokinin and auxin in shaping root architecture: Regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann. Bot. 2006, 97, 883–893. [Google Scholar] [CrossRef]
  125. Noel, T.C.; Sheng, C.; Yost, C.K.; Pharis, R.P.; Hynes, M.F. Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: Direct growth promotion of canola and lettuce. Can. J. Microbiol. 1996, 42, 279–283. [Google Scholar] [CrossRef]
  126. Frugier, F.; Kosuta, S.; Murray, J.D.; Crespi, M.; Szczyglowski, K. Cytokinin: Secret agent of symbiosis. Trends Plant Sci. 2008, 13, 115–120. [Google Scholar] [CrossRef]
  127. Cooper, J.B.; Long, S.R. Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 1994, 6, 215–225. [Google Scholar] [CrossRef][Green Version]
  128. Kisiala, A.; Laffont, C.; Emery, R.J.N.; Frugier, F. Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonnodulating strains. Mol. Plant Microbe Interact. 2013, 26, 1225–1231. [Google Scholar] [CrossRef][Green Version]
  129. Mens, C.; Li, D.; Haaima, L.E.; Gresshoff, P.M.; Ferguson, B.J. Local and systemic effect of cytokinins on soybean nodulation and regulation of their isopentenyl transferase (IPT) biosynthesis genes following rhizobia inoculation. Front. Plant Sci. 2018, 9, 1150. [Google Scholar] [CrossRef]
  130. Gonzalez-Rizzo, S.; Crespi, M.; Frugier, F. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 2006, 18, 2680–2693. [Google Scholar] [CrossRef][Green Version]
  131. Murray, J.D.; Karas, B.J.; Sato, S.; Tabata, S.; Amyot, L.; Szczyglowski, K. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 2007, 315, 101–104. [Google Scholar] [CrossRef]
  132. Dolgikh, E.A.; Kusakin, P.G.; Kitaeva, A.B.; Tsyganova, A.V.; Kirienko, A.N.; Leppyanen, I.V.; Dolgikh, A.V.; Ilina, E.L.; Demchenko, K.N.; Tikhonovich, I.A.; et al. Mutational analysis idicates that abnormalities in rhizobial infection and subsequent plant cell and bacteroid differentiation in pea (Pisum sativum) nodules coincide with abnormal cytokinin responses and localization. Ann. Bot. 2020, 125, 905–923. [Google Scholar] [CrossRef]
  133. Figueiredo, M.V.B.; Burity, H.A.; Martinez, C.R.; Chanway, C.P. Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl. Soil Ecol. 2008, 40, 182–188. [Google Scholar] [CrossRef]
  134. Cowan, A.K.; Cairns, A.L.; Bartels-Rahm, B. Regulation of abscisic acid metabolism: Towards a metabolic basis for abscisic acid-cytokinin antagonism. J. Exp. Bot. 1999, 50, 595–603. [Google Scholar] [CrossRef]
  135. Cohen, A.C.; Bottini, R.; Piccoli, P.N. Azospirillum brasilense Sp. 245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul. 2008, 54, 97–103. [Google Scholar] [CrossRef]
  136. Kang, S.M.; Radhakrishnan, R.; Khan, A.L.; Kim, M.J.; Park, J.M.; Kim, B.R.; Shin, D.H.; Lee, I.J. Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol. Biochem. 2014, 84, 115–124. [Google Scholar] [CrossRef]
  137. Tominaga, A.; Nagata, M.; Futsuki, K.; Abe, H.; Uchiumi, T.; Abe, M.; Kucho, K.; Hashiguchi, M.; Akashi, R.; Hirsch, A.M. Enhanced nodulation and nitrogen fixation in the abscisic acid low-sensitive mutant enhanced nitrogen fixation1 of Lotus japonicus. Plant Physiol. 2009, 151, 1965–1976. [Google Scholar] [CrossRef][Green Version]
  138. Suzuki, A.; Akune, M.; Kogiso, M.; Imagama, Y.; Osuki, K.; Uchiumi, T.; Higashi, S.; Han, S.-Y.; Yoshida, S.; Asami, T. Control of nodule number by the phytohormone abscisic acid in the roots of two leguminous species. Plant Cell Physiol. 2004, 45, 914–922. [Google Scholar] [CrossRef][Green Version]
  139. Van de Velde, W.; Guerra, J.C.P.; De Keyser, A.; De Rycke, R.; Rombauts, S.; Maunoury, N.; Mergaert, P.; Kondorosi, E.; Holsters, M.; Goormachtig, S. Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol. 2006, 141, 711–720. [Google Scholar] [CrossRef][Green Version]
  140. Serova, T.A.; Tikhonovich, I.A.; Tsyganov, V.E. Analysis of nodule senescence in pea (Pisum sativum L.) using laser microdissection, real-time PCR, and ACC immunolocalization. J. Plant Physiol. 2017, 212, 29–44. [Google Scholar] [CrossRef] [PubMed]
  141. Yamaguchi, S. Gibberellin metabolism and its regulation. Annu. Rev. Plant Biol. 2008, 59, 225–251. [Google Scholar] [CrossRef]
  142. Gutiérrez-Mañero, F.J.; Ramos-Solano, B.; Probanza, A.N.; Mehouachi, J.; Tadeo, F.R.; Talon, M. The plant-growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol. Plant. 2001, 111, 206–211. [Google Scholar] [CrossRef]
  143. Bottini, R.; Cassán, F.; Piccoli, P. Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biotechnol. 2004, 65, 497–503. [Google Scholar] [CrossRef] [PubMed]
  144. Dodd, I.C.; Zinovkina, N.Y.; Safronova, V.I.; Belimov, A.A. Rhizobacterial mediation of plant hormone status. Ann. Appl. Biol. 2010, 157, 361–379. [Google Scholar] [CrossRef]
  145. Salazear-Cerezo, S.; Martinez-Montiel, N.; Garcia –Sanchez, J.; Perezy-Terron, R.; Martinez-Contreras, D. Gibberellin biosynthesis and metabolism: A convergent route for plants, fungi and bacteria. Microbiol. Res. 2018, 208, 85–98. [Google Scholar] [CrossRef] [PubMed]
  146. Cassan, F.; Bottini, R.; Schneider, G.; Piccoli, P. Azospirillum brasilense and Azospirillum lipoferum hydrolyze conjugates of GA20 and metabolize the resultant aglycones to GA1 in seedlings of rice dwarf mutants. Plant Physiol. 2001, 125, 2053–2058. [Google Scholar] [CrossRef] [PubMed][Green Version]
  147. Cassan, F.D.; Lucangeli, C.D.; Bottini, R.; Piccoli, P.N. Azospirillum spp. metabolize (17, 17–2H2) gibberellin A20 to (17, 17–2H2) gibberellin A1 in vivo in dy rice mutant seedlings. Plant Cell Physiol. 2001, 42, 763–767. [Google Scholar] [CrossRef][Green Version]
  148. Freiberg, C.; Fellay, R.; Bairoch, A.; Broughton, W.J.; Rosenthal, A.; Perret, X. Molecular basis of symbiosis between Rhizobium and legumes. Nature 1997, 387, 394–401. [Google Scholar] [CrossRef] [PubMed]
  149. Tully, R.E.; Keister, D.L. Cloning and mutagenesis of a cytochrome P-450 locus from Bradyrhizobium japonicum that is expressed anaerobically and symbiotically. Appl. Environ. Microbiol. 1993, 59, 4136–4142. [Google Scholar] [CrossRef][Green Version]
  150. Kaneko, T.; Nakamura, Y.; Sato, S.; Minamisawa, K.; Uchiumi, T.; Sasamoto, S.; Watanabe, A.; Idesawa, K.; Iriguchi, M.; Kawashima, K. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 2002, 9, 189–197. [Google Scholar] [CrossRef]
  151. Tatsukami, Y.; Ueda, M. Rhizobial gibberellin negatively regulates host nodule number. Sci. Rep. 2016, 6, 27998. [Google Scholar] [CrossRef][Green Version]
  152. Ferguson, B.J.; Ross, J.J.; Reid, J.B. Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiol. 2005, 138, 2396–2405. [Google Scholar] [CrossRef][Green Version]
  153. McAdam, E.L.; Reid, J.B.; Foo, E. Gibberellins promote nodule organogenesis but inhibit the infection stages of nodulation. J. Exp. Bot. 2018, 69, 2117–2130. [Google Scholar] [CrossRef]
  154. Maekawa, T.; Maekawa-Yoshikawa, M.; Takeda, N.; Imaizumi-Anraku, H.; Murooka, Y.; Hayashi, M. Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J. 2009, 58, 183–194. [Google Scholar] [CrossRef]
  155. Fonouni-Farde, C.; Tan, S.; Baudin, M.; Brault, M.; Wen, J.; Mysore, K.S.; Niebel, A.; Frugier, F.; Diet, A. DELLA-mediated gibberellin signalling regulates Nod factor signalling and rhizobial infection. Nat. Commun. 2016, 7, 1–13. [Google Scholar] [CrossRef] [PubMed]
  156. Jin, Y.; Liu, H.; Luo, D.; Yu, N.; Dong, W.; Wang, C.; Zhang, X.; Dai, H.; Yang, J.; Wang, E. DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nat. Commun. 2016, 7, 1–14. [Google Scholar] [CrossRef] [PubMed]
  157. Stracke, S.; Kistner, C.; Yoshida, S.; Mulder, L.; Sato, S.; Kaneko, T.; Tabata, S.; Sandal, N.; Stougaard, J.; Szczyglowski, K. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 2002, 417, 959–962. [Google Scholar] [CrossRef]
  158. Serova, T.A.; Tsyganova, A.V.; Tikhonovich, I.A.; Tsyganov, V.E. Gibberellins inhibit nodule senescence and stimulate nodule meristem bifurcation in pea (Pisum sativum L.). Front. Plant Sci. 2019, 10, 285. [Google Scholar] [CrossRef] [PubMed][Green Version]
  159. Guinel, F.C.; LaRue, T.A. Ethylene inhibitors partly restore nodulation to pea mutant E107 (brz). Plant Physiol. 1992, 99, 515–518. [Google Scholar] [CrossRef] [PubMed][Green Version]
  160. Nukui, N.; Ezura, H.; Minamisawa, K. Transgenic Lotus japonicus with an ethylene receptor gene Cm-ERS1/H70A enhances formation of infection threads and nodule primordia. Plant Cell Physiol. 2004, 45, 427–435. [Google Scholar] [CrossRef][Green Version]
  161. Shah, S.; Li, J.; Moffatt, B.A.; Glick, B.R. Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria. Can. J. Microbiol. 1998, 44, 833–843. [Google Scholar] [CrossRef]
  162. Ma, W.; Guinel, F.C.; Glick, B.R. Rhizobium leguminosarum biovar viciae 1-aminocyclopropane-1-carboxylate deaminase promotes nodulation of pea plants. Appl. Environ. Microbiol. 2003, 69, 4396–4402. [Google Scholar] [CrossRef][Green Version]
  163. Tittabutr, P.; Awaya, J.D.; Li, Q.X.; Borthakur, D. The cloned 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene from Sinorhizobium sp. strain BL3 in Rhizobium sp. strain TAL1145 promotes nodulation and growth of Leucaena leucocephala. Syst. Appl. Microbiol. 2008, 31, 141–150. [Google Scholar] [CrossRef]
  164. Nascimento, F.X.; Brígido, C.; Glick, B.R.; Oliveira, S.; Alho, L. Mesorhizobium ciceri LMS-1 expressing an exogenous 1-aminocyclopropane-1-carboxylate (ACC) deaminase increases its nodulation abilities and chickpea plant resistance to soil constraints. Lett. Appl. Microbiol. 2012, 55, 15–21. [Google Scholar] [CrossRef]
  165. Uchiumi, T.; Ohwada, T.; Itakura, M.; Mitsui, H.; Nukui, N.; Dawadi, P.; Kaneko, T.; Tabata, S.; Yokoyama, T.; Tejima, K. Expression islands clustered on the symbiosis island of the Mesorhizobium loti genome. J. Bacteriol. 2004, 186, 2439–2448. [Google Scholar] [CrossRef] [PubMed][Green Version]
  166. Nandasena, K.; Yates, R.; Tiwari, R.; O’Hara, G.; Howieson, J.; Ninawi, M.; Chertkov, O.; Detter, C.; Tapia, R.; Han, S.; et al. Complete genome sequence of Mesorhizobium ciceri bv. biserrulae type strain (WSM1271 T). Stand. Genom. Sci. 2014, 9, 462–472. [Google Scholar] [CrossRef][Green Version]
  167. Nukui, N.; Minamisawa, K.; Ayabe, S.-I.; Aoki, T. Expression of the 1-aminocyclopropane-1-carboxylic acid deaminase gene requires symbiotic nitrogen-fixing regulator gene nifA2 in Mesorhizobium loti MAFF303099. Appl. Environ. Microbiol. 2006, 72, 4964–4969. [Google Scholar] [CrossRef] [PubMed][Green Version]
  168. Pieterse, C.M.J.; Leon-Reyes, A.; Van der Ent, S.; Van Wees, S.C.M. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 2009, 5, 308–316. [Google Scholar] [CrossRef][Green Version]
  169. Shahzad, S.M.; Khalid, A.; Arshad, M.; Tahir, J.; Mahmood, T. Improving nodulation, growth and yield of Cicer arietinum L. through bacterial ACC-deaminase induced changes in root architecture. Eur. J. Soil Biol. 2010, 46, 342–347. [Google Scholar] [CrossRef]
  170. Chaudhary, D.; Sindhu, S. Inducing salinity tolerance in chickpea (Cicer arietinum L.) by inoculation of 1-aminocyclopropane-1-carboxylic acid deaminase-containing Mesorhizobium strains. Afr. J. Microbiol. Res. 2015, 9, 117–124. [Google Scholar] [CrossRef][Green Version]
  171. Sharma, P.; Khanna, V.; Kumari, S. Potential of ACC-deaminase producing plant growth promoting rhizobacteria on water stress mitigation in lentil (Lens culinaris L. Medikus) under axenic conditions. Int. J. Adv. Res. 2015, 3, 59–67. [Google Scholar]
  172. Shaharoona, B.; Arshad, M.; Zahir, Z.A. Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Lett. Appl. Microbiol. 2006, 42, 155–159. [Google Scholar] [CrossRef]
  173. Ahmad, M.; Zahir, Z.A.; Asghar, H.N.; Asghar, M. Inducing salt tolerance in mung bean through coinoculation with rhizobia and plant-growth-promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase. Can. J. Microbiol. 2011, 57, 578–589. [Google Scholar] [CrossRef]
  174. Barnawal, D.; Bharti, N.; Maji, D.; Chanotiya, C.S.; Kalra, A. ACC deaminase-containing Arthrobacter protophormiae induces NaCl stress tolerance through reduced ACC oxidase activity and ethylene production resulting in improved nodulation and mycorrhization in Pisum sativum. J. Plant Physiol. 2014, 171, 884–894. [Google Scholar] [CrossRef]
  175. Safronova, V.I.; Stepanok, V.V.; Engqvist, G.L.; Alekseyev, Y.V.; Belimov, A.A. Root-associated bacteria containing 1-aminocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol. Fertil. Soils 2006, 42, 267–272. [Google Scholar] [CrossRef]
  176. Arshad, M.; Shaharoona, B.; Mahmood, T. Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield, and ripening of pea (Pisum sativum L.). Pedosphere 2008, 18, 611–620. [Google Scholar] [CrossRef]
  177. Belimov, A.A.; Dodd, I.C.; Hontzeas, N.; Theobald, J.C.; Safronova, V.I.; Davies, W.J. Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol. 2009, 181, 413–423. [Google Scholar] [CrossRef] [PubMed]
  178. Husen, E.; Wahyudi, A.T.; Suwanto, A. Growth enhancement and disease reduction of soybean by 1-aminocyclopropane-1-carboxylate deaminase-producing Pseudomonas. Am. J. Appl. Sci. 2011, 8, 1073–1080. [Google Scholar] [CrossRef][Green Version]
  179. Saravanakumar, D.; Samiyappan, R. ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J. Appl. Microbiol. 2007, 10, 1283–1292. [Google Scholar] [CrossRef] [PubMed]
  180. Khandelwal, A.; Sindhu, S.S. ACC deaminase containing rhizobacteria enhance nodulation and plant growth in cluster bean (Cyamopsis tetragonoloba L.). J. Microbiol. Res. 2013, 3, 117–123. [Google Scholar] [CrossRef]
  181. Trung, N.T.; Thuam, N.H. Screening of strong 1-aminocyclopropane-1-carboxylate deaminase producing bacteria for improving the salinity tolerance of cowpea. Appl. Microbiol. 2016, 2, 1000111. [Google Scholar] [CrossRef]
  182. Silva, E.R.; Zoz, J.; Oliveira, C.E.S.; Zuffo, A.M.; Steiner, F.; Zoz, T.; Vendruscolo, E.P. Can co-inoculation of Bradyrhizobium and Azospirillum alleviate adverse effects of drought stress on soybean (Glycine max L. Merrill.)? Arch. Microbiol. 2019, 201, 325–335. [Google Scholar] [CrossRef]
  183. Sondergaard, T.E.; Schulz, A.; Palmgren, M.G. Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol. 2004, 136, 2475–2482. [Google Scholar] [CrossRef][Green Version]
  184. Karlidag, H.; Esitken, A.; Turan, M.; Sahin, F. Effects of root inoculation of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient element contents of leaves of apple. Sci. Hortic. 2007, 114, 16–20. [Google Scholar] [CrossRef]
  185. German, M.A.; Burdman, S.; Okon, Y.; Kigel, J. Effects of Azospirillum brasilense on root morphology of common bean (Phaseolus vulgaris L.) under different water regimes. Biol. Fertil. Soils 2000, 32, 259–264. [Google Scholar] [CrossRef]
  186. Saikia, S.P.; Dutta, S.P.; Goswami, A.; Bhau, B.S.; Kanjilal, P.B. Role of Azospirillum in the Improvement of Legumes. In Microbes for Legume Improvement; Khan, M.S., Musarrat, J., Zaidi, A., Eds.; Springer: Berlin/Heidelberg, Germany, 2010; pp. 389–408. [Google Scholar] [CrossRef]
  187. dos Santos Lima Fagotti, D.; Abrantes, J.L.F.; Cerezini, P.; Fukami, J.; Nogueira, M.A.; del Cerro, P.; Valderrama-Fernández, R.; Ollero, F.J.; Megías, M.; Hungria, M. Quorum sensing communication: Bradyrhizobium-Azospirillum interaction via N-acyl-homoserine lactones in the promotion of soybean symbiosis. J. Basic Microbiol. 2019, 59, 38–53. [Google Scholar] [CrossRef][Green Version]
  188. Barnawal, D.; Bharti, N.; Pandey, S.S.; Pandey, A.; Chanotiya, C.S.; Kalra, A. Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol. Plant. 2017, 161, 502–514. [Google Scholar] [CrossRef][Green Version]
  189. Sakamoto, K.; Ogiwara, N.; Kaji, T.; Sugimoto, Y.; Ueno, M.; Sonoda, M.; Matsui, A.; Ishida, J.; Tanaka, M.; Totoki, Y. Transcriptome analysis of soybean (Glycine max) root genes differentially expressed in rhizobial, arbuscular mycorrhizal, and dual symbiosis. J. Plant Res. 2019, 132, 541–568. [Google Scholar] [CrossRef] [PubMed]
  190. Sreevidya, M.; Gopalakrishnan, S.; Kudapa, H.; Varshney, R.K. Exploring plant growth-promotion actinomycetes from vermicompost and rhizosphere soil for yield enhancement in chickpea. Braz. J. Microbiol. 2016, 47, 85–95. [Google Scholar] [CrossRef][Green Version]
  191. Tokala, R.K.; Strap, J.L.; Jung, C.M.; Crawford, D.L.; Salove, M.H.; Deobald, L.A.; Bailey, J.F.; Morra, M.J. Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl. Environ. Microbiol. 2002, 68, 2161–2171. [Google Scholar] [CrossRef] [PubMed][Green Version]
  192. Khanna, V.; Sharma, P. Potential for enhancing lentil (Lens culinaris) productivity by co-inoculation with PSB, plant growth-promoting rhizobacteria and Rhizobium. Indian J. Agric. Sci. 2011, 81, 932. [Google Scholar]
  193. Bansal, R.K. Synergistic effect of Rhizobium, PSB and PGPR on nodulation and grain yield of mungbean. J. Food Legum. 2009, 22, 37–39. [Google Scholar]
  194. Bhattacharjya, S.; Chandra, R. Effect of inoculation methods of Mesorhizobium ciceri and PGPR in chickpea (Cicer areietinum L.) on symbiotic traits, yields, nutrient uptake and soil properties. Legum. Res. Int. J. 2013, 36, 331–337. [Google Scholar]
  195. Badawi, F.S.F.; Biomy, A.M.M.; Desoky, A.H. Peanut plant growth and yield as influenced by co-inoculation with Bradyrhizobium and some rhizo-microorganisms under sandy loam soil conditions. Ann. Agric. Sci. 2011, 56, 17–25. [Google Scholar] [CrossRef][Green Version]
  196. Tilak, K.V.B.R.; Ranganayaki, N.; Manoharachari, C. Synergistic effects of plant-growth promoting rhizobacteria and Rhizobium on nodulation and nitrogen fixation by pigeonpea (Cajanus cajan). Eur. J. Soil Sci. 2006, 57, 67–71. [Google Scholar] [CrossRef]
  197. Bhattacharjee, S.; Sharma, G.D. Effect of dual inoculation of arbuscular mycorrhiza and Rhizobium on the chlorophyll, nitrogen and phosphorus contents of pigeon pea (Cajanus cajan L.). Adv. Microbiol. 2012, 2, 25945. [Google Scholar] [CrossRef][Green Version]
  198. Haskett, T.; Wang, P.; Ramsay, J.; O’Hara, G.; Reeve, W.; Howieson, J.; Terpolilli, J. Complete genome sequence of Mesorhizobium ciceri strain CC1192, an efficient nitrogen-fixing microsymbiont of Cicer arietinum. Genome Announc. 2016, 4, e00516-16. [Google Scholar] [CrossRef][Green Version]
  199. Weiss, V.A.; Faoro, H.; Tadra-Sfeir, M.Z.; Raittz, R.T.; de Souza, E.M.; Monteiro, R.A.; Cardoso, R.L.A.; Wassem, R.; Chubatsu, L.S.; Huergo, L.F. Draft genome sequence of Herbaspirillum lusitanum P6-12, an endophyte isolated from root nodules of Phaseolus vulgaris. J. Bacteriol. 2012, 194, 4136–4137. [Google Scholar] [CrossRef][Green Version]
  200. Simões-Araújo, J.L.; Leite, J.; Passos, S.R.; Xavier, G.R.; Rumjanek, N.G.; Zilli, J.É. Draft genome sequence of Bradyrhizobium sp. strain BR 3267, an elite strain recommended for cowpea inoculation in Brazil. Braz. J. Microbiol. 2016, 47, 781–782. [Google Scholar] [CrossRef][Green Version]
  201. Schuldes, J.; Orbegoso, M.R.; Schmeisser, C.; Krishnan, H.B.; Daniel, R.; Streit, W.R. Complete genome sequence of the broad-host-range strain Sinorhizobium fredii USDA257. J. Bacteriol. 2012, 194, 4483. [Google Scholar] [CrossRef] [PubMed][Green Version]
  202. Siqueira, A.F.; Ormeño-Orrillo, E.; Souza, R.C.; Rodrigues, E.P.; Almeida, L.G.P.; Barcellos, F.G.; Batista, J.S.S.; Nakatani, A.S.; Martínez-Romero, E.; Vasconcelos, A.T.R. Comparative genomics of Bradyrhizobium japonicum CPAC 15 and Bradyrhizobium diazoefficiens CPAC 7: Elite model strains for understanding symbiotic performance with soybean. BMC Genom. 2014, 15, 1–21. [Google Scholar] [CrossRef] [PubMed][Green Version]
  203. Zhu, B.; Liu, H.; Tian, W.-X.; Fan, X.-Y.; Li, B.; Zhou, X.-P.; Jin, G.-L.; Xie, G.-L. Genome sequence of Stenotrophomonas maltophilia RR-10, isolated as an endophyte from rice root. Genome Announc. 2012, 194, 1280–1281. [Google Scholar] [CrossRef] [PubMed][Green Version]
  204. Mathimaran, N.; Srivastava, R.; Wiemken, A.; Sharma, A.K.; Boller, T. Genome sequences of two plant growth-promoting fluorescent Pseudomonas strains, R62 and R81. J. Bacteriol. 2012, 194, 3272–3273. [Google Scholar] [CrossRef][Green Version]
  205. Gamez, R.M.; Rodríguez, F.; Bernal, J.F.; Agarwala, R.; Landsman, D.; Mariño-Ramírez, L. Genome sequence of the banana plant growth-promoting rhizobacterium Bacillus amyloliquefaciens BS006. Genome Announc. 2015, 3, e01391-15. [Google Scholar] [CrossRef][Green Version]
  206. Wisniewski-Dyé, F.; Lozano, L.; Acosta-Cruz, E.; Borland, S.; Drogue, B.; Prigent-Combaret, C.; Rouy, Z.; Barbe, V.; Herrera, A.M.; González, V. Genome sequence of Azospirillum brasilense CBG497 and comparative analyses of Azospirillum core and accessory genomes provide insight into niche adaptation. Genes 2012, 3, 576–602. [Google Scholar] [CrossRef] [PubMed]
  207. Christensen, H.; Kuhnert, P.; Olsen, J.E.; Bisgaard, M. Comparative phylogenies of the housekeeping genes atpD, infB and rpoB and the 16S rRNA gene within the Pasteurellaceae. Int. J. Syst. Evol. Microbiol. 2004, 54 Pt 5, 1601–1609. [Google Scholar] [CrossRef][Green Version]
  208. Rivas, R.; Martens, M.; De Lajudie, P.; Willems, A. Multilocus sequence analysis of the genus Bradyrhizobium. Syst. Appl. Microbiol. 2009, 32, 101–110. [Google Scholar] [CrossRef]
  209. Edwards, U.; Rogall, T.; Blöcker, H.; Emde, M.; Böttger, E.C. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 1989, 17, 7843–7853. [Google Scholar] [CrossRef] [PubMed][Green Version]
  210. Tan, H.W.; Weir, B.S.; Carter, N.; Heenan, P.B.; Ridgway, H.J.; James, E.K.; Sprent, J.I.; Young, J.P.W.; Andrews, M. Rhizobia with 16S rRNA and nifH similar to Mesorhizobium huakuii but novel recA, glnII, nodA and nodC genes are symbionts of New Zealand Carmichaelinae. PLoS ONE 2012, 7, e47677. [Google Scholar] [CrossRef] [PubMed][Green Version]
  211. Venkadesaperumal, G.; Amaresan, N.; Kumar, K. Plant growth promoting capability and genetic diversity of bacteria isolated from mud volcano and lime cave of Andaman and Nicobar Islands. Braz. J. Microbiol. 2014, 45, 1271–1281. [Google Scholar] [CrossRef] [PubMed][Green Version]
  212. Naveed, M.; Mubeen, S.; Ahmed, I.; Khalid, N.; Suleria, H.A.R.; Bano, A.; Mumtaz, A.S. Identification and characterization of rhizospheric microbial diversity by 16S ribosomal RNA gene sequencing. Braz. J. Microbiol. 2014, 45, 985–993. [Google Scholar] [CrossRef] [PubMed][Green Version]
  213. Laguerre, G.; Mavingui, P.; Allard, M.-R.; Charnay, M.-P.; Louvrier, P.; Mazurier, S.-I.; Rigottier-Gois, L.; Amarger, N. Typing of rhizobia by PCR DNA fingerprinting and PCR-restriction fragment length polymorphism analysis of chromosomal and symbiotic gene regions: Application to Rhizobium leguminosarum and its different biovars. Appl. Environ. Microbiol. 1996, 62, 2029–2036. [Google Scholar] [CrossRef][Green Version]
  214. Zhang, J.J.; Liu, T.Y.; Chen, W.F.; Wang, E.T.; Sui, X.H.; Zhang, X.X.; Li, Y.; Li, Y.; Chen, W.X. Mesorhizobium muleiense sp. nov., nodulating with Cicer arietinum L. Int. J. Syst. Evol. Microbiol. 2012, 62, 2737–2742. [Google Scholar] [CrossRef][Green Version]
  215. Diouf, F.; Diouf, D.; Klonowska, A.; Le Queré, A.; Bakhoum, N.; Fall, D.; Neyra, M.; Parrinello, H.; Diouf, M.; Ndoye, I. Genetic and genomic diversity studies of Acacia symbionts in Senegal reveal new species of Mesorhizobium with a putative geographical pattern. PLoS ONE 2015, 10, e0117667. [Google Scholar] [CrossRef]
  216. De Bruijn, F.J. Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl. Environ. Microbiol. 1992, 58, 2180–2187. [Google Scholar] [CrossRef] [PubMed][Green Version]
  217. De Meyer, S.E.; Van Hoorde, K.; Vekeman, B.; Braeckman, T.; Willems, A. Genetic diversity of rhizobia associated with indigenous legumes in different regions of Flanders (Belgium). Soil Biol. Biochem. 2011, 43, 2384–2396. [Google Scholar] [CrossRef]
  218. Kaschuk, G.; Hungria, M.; Andrade, D.S.; Campo, R.J. Genetic diversity of rhizobia associated with common bean (Phaseolus vulgaris L.) grown under no-tillage and conventional systems in Southern Brazil. Appl. Soil Ecol. 2006, 32, 210–220. [Google Scholar] [CrossRef]
  219. Gaunt, M.W.; Turner, S.L.; Rigottier-Gois, L.; Lloyd-Macgilp, S.A.; Young, J.P. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int. J. Syst. Evol. Microbiol. 2001, 51, 2037–2048. [Google Scholar] [CrossRef] [PubMed][Green Version]
  220. Kim, D.H.; Kaashyap, M.; Rathore, A.; Das, R.R.; Parupalli, S.; Upadhyaya, H.D.; Gopalakrishnan, S.; Gaur, P.M.; Singh, S.; Kaur, J. Phylogenetic diversity of Mesorhizobium in chickpea. J. Biosci. 2014, 39, 513–517. [Google Scholar] [CrossRef] [PubMed][Green Version]
  221. Payne, G.W.; Vandamme, P.; Morgan, S.H.; LiPuma, J.J.; Coenye, T.; Weightman, A.J.; Jones, T.H.; Mahenthiralingam, E. Development of a recA gene-based identification approach for the entire Burkholderia genus. Appl. Environ. Microbiol. 2005, 71, 3917–3927. [Google Scholar] [CrossRef] [PubMed][Green Version]
  222. Blažinkov, M.; Sikora, S.; Uher, D.; Mačešić, D.; Redžepović, S. Genotypic characterisation of indigenous Rhizobium leguminosarum bv. viciae field population in Croatia. Agric. Conspec. Sci. 2007, 72, 153–158. [Google Scholar]
  223. Marinković, J.; Đorđević, V.; Balešević-Tubić, S.; Bjelić, D.; Vucelić-Radović, B.; Jošić, D. Osmotic stress tolerance, PGP traits and RAPD analysis of Bradyrhizobium japonicum strains. Genetika 2013, 45, 75–86. [Google Scholar] [CrossRef]
  224. Kasa, P.; Modugapalem, H.; Battini, K. Isolation, screening, and molecular characterization of plant growth promoting rhizobacteria isolates of Azotobacter and Trichoderma and their beneficial activities. J. Nat. Sci. Biol. Med. 2015, 6, 360–363. [Google Scholar] [CrossRef][Green Version]
  225. Lerner, A.; Herschkovitz, Y.; Baudoin, E.; Nazaret, S.; Moenne-Loccoz, Y.; Okon, Y.; Jurkevitch, E. Effect of Azospirillum brasilense inoculation on rhizobacterial communities analyzed by denaturing gradient gel electrophoresis and automated ribosomal intergenic spacer analysis. Soil Biol. Biochem. 2006, 38, 1212–1218. [Google Scholar] [CrossRef]
  226. Sachdev, D.; Nema, P.; Dhakephalkar, P.; Zinjarde, S.; Chopade, B. Assessment of 16S rRNA gene-based phylogenetic diversity and promising plant growth-promoting traits of Acinetobacter community from the rhizosphere of wheat. Microbiol. Res. 2010, 165, 627–638. [Google Scholar] [CrossRef]
  227. Sharma, R.; Pooniya, V.; Bisaria, V.S.; Swarnalakshmi, K.; Sharma, S. Bioinoculants play a significant role in shaping the rhizospheric microbial community: A field study with Cajanus cajan. World J. Microbiol. Biotechnol. 2020, 36, 1–17. [Google Scholar] [CrossRef]
  228. Sharma, S.B.; Sayyed, R.Z.; Trivedi, M.H.; Gobi, T.A. Phosphate solubilizing microbes: Sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus 2013, 2, 587. [Google Scholar] [CrossRef][Green Version]
  229. Ding, Y.; Wang, J.; Liu, Y.; Chen, S. Isolation and identification of nitrogen-fixing bacilli from plant rhizospheres in Beijing region. J. Appl. Microbiol. 2005, 99, 1271–1281. [Google Scholar] [CrossRef]
  230. Ashraf, M.A.; Rasool, M.; Mirza, M.S. Nitrogen fixation and indole acetic acid production potential of bacteria isolated from rhizosphere of sugarcane (Saccharum officinarum L.). Adv. Biol. Res. 2011, 5, 348–355. [Google Scholar]
  231. Jha, Y.; Subramanian, R.B. Characterization of root-associated bacteria from paddy and its growth-promotion efficacy. 3 Biotech 2014, 4, 325–330. [Google Scholar] [CrossRef] [PubMed][Green Version]
  232. Naveed, M.; Sohail, Y.; Khalid, N.; Ahmed, I.; Mumtaz, A.S. Evaluation of glucose dehydrogenase and pyrroloquinoline quinine (pqq) mutagenesis that renders functional inadequacies in host plants. J. Microbiol. Biotechnol. 2015, 25, 1349–1360. [Google Scholar] [CrossRef]
  233. Ovaa, W.; Bitter, W.; Weisbeek, P.; Koster, M. Multiple outer membrane receptors for uptake of ferric pseudobactins in Pseudomonas putida WCS358. Mol. Gen. Genet. 1995, 248, 735–743. [Google Scholar] [CrossRef]
  234. Woo, S.M.; Lim, J.H.; Jeong, H.Y.; Kim, S.D. Genetic monitoring of plant growth promoting rhizobacterium (PGPR), Bacillus subtilis AH18 using multiplex PCR in field soil. Microbiol. Biotechnol. Lett. 2009, 37, 1–9. [Google Scholar]
  235. Lim, J.H.; Ahn, C.H.; Jeong, H.Y.; Kim, Y.H.; Kim, S.D. Genetic monitoring of multi-functional plant growth promoting rhizobacteria Bacillus subtilis AH18 and Bacillus licheniformis K11 by multiplex and real-time polymerase chain reaction in a pepper farming field. J. Korean Soc. Appl. Biol. Chem. 2011, 54, 221–228. [Google Scholar] [CrossRef]
  236. Patten, C.L.; Glick, B.R. Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl. Environ. Microbiol. 2002, 68, 3795–3801. [Google Scholar] [CrossRef] [PubMed][Green Version]
  237. Brandao, P.F.B.; Clapp, J.P.; Bull, A.T. Diversity of nitrile hydratase and amidase enzyme genes in Rhodococcus erythropolis recovered from geographically distinct habitats. Appl. Environ. Microbiol. 2003, 69, 5754–5766. [Google Scholar] [CrossRef] [PubMed][Green Version]
Figure 1. Biotic and abiotic factors influencing plant– plant growth promoting rhizobacteria (PGPR) interactions in the rhizosphere.
Figure 1. Biotic and abiotic factors influencing plant– plant growth promoting rhizobacteria (PGPR) interactions in the rhizosphere.
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Table 1. Influence of plant growth promoting rhizobacteria on growth of legume crops.
Table 1. Influence of plant growth promoting rhizobacteria on growth of legume crops.
CropMicrobesBeneficial EffectsReferences
Cicer arietinum (Chickpea)Pseudomonas aeruginosa,
Pseudomonas alcaligenes,
Pseudomonas fluorescens BHUPSB06, Pseudomonas jessenii PS06
Enhanced acquisition of P and Fe, effective symbiosis with Mesohizobium[23,24,25]
Pseudomonas alcaligenes,
Bacillus pumilus
Increase in shoot dry mass, pod number, nodulation, chlorophyll content, N, P and K content[24,25]
Azospirillum lipoferum FK1,
Azospirillum brasilense
Improved nodulation and growth[19,26]
AzotobacterIncrease in plant–rhizobial symbiosis, biomass, grain yield, N content[27]
Lens culinaris
Bacillus megaterium
Kurthia sp. LK786,
Pseudomonas diminuta LK884
Enhanced symbiotic effect of Rhizobium leguminosarum and improved plant growth[28,29]
Pseudomonas sp.Enhanced symbiotic effect of Rhizobium leguminosarum and improved plant growth[30]
Proteus vulgarisIncreased nodulation potential when given in combination with Rhizobium leguminosarum L-12-8[31]
Vigna radiata (Green gram)Bacillus subtilis,
Bacillus megaterium
Increase in dry matter and N and P uptake[32,33]
Pseudomonas putida GRP3AStimulated iron uptake[34]
Pseudomonas sp.Increase in plant height and improved root development[34,35,36]
Cajanus cajan (Pigeonpea)Bacillus subtilis AF1,
Bacillus cereus BS03
Increase in shoot, root length, nodulation and biomass[37,38]
Pseudomonas spp.,
Pseudomonas aeruginosa RRLJ
Significant increase in plant growth and nodulation occupancy of Rhizobium[38,39]
Azotobacter chroococcum A41,
Bacillus megaterium MTCC 453,
Pseudomonas fluorescens MTCC9768.
Improved plant growth and yield[40]
Arachis hypogaea
Pseudomonas fluorescens
Enhanced synergistic activity of rhizobia for nutrient uptake and plant growth[41,42]
Glycine max
Bacillus amyloliquefaciens LL2012, Bacillus subtilisEnhanced symbiotic capacity of Bradyrhizobium japonicum[31,43]
Azospirillum brasilense Sp7,
Azospirillum lipoferum CCM3863
Efficient symbiosis with Bradyrhizobium japonicum and enhancement in root growth and shoot dry matter[44]
Pseudomonas cepaciaEnhanced synergistic activity with Bradyrhizobium japonicum TAL-378 resulted in overall improved plant growth[45,46]
Phaseolus vulgaris
(Common bean)
Bacillus megateriumIncreased nodulation, shoot dry weight, nodule dry weight and chlorophyll content[47]
Paenibacillus polymyxa DSM 36 and Loutit (L)Increased symbiotic efficiency of Rhizobium tropici[48]
Azospirillum brasilense,
Azospirillum lipoferum S21
Enhancement of nodulation and N2 fixation activity of Rhizobium[49,50]
Pseudomonas monteilii,
Pseudomonas fluorescens P93
Synergistic effect of Rhizobium pisi leading to increased nodulation[48,51]
Vicia faba
(Faba bean)
Azospirillum brasilense, Azospirillum lipoferum SM1, Azospirillum brasilenseIncrease in growth of root, shoot and improved nodulation[26,52]
Azotobacter chroococcum H23,
Azotobacter vinelandii ATCC12837 and Dv42
Increased nodulation, dry mater and total N content[53]
Pseudomonas aeruginosa,
Pseudomonas putida TK3,
Serratia marcescens BM1
Serratia liquefaciens BM4,
Xanthobacter autotrophicus BM3
Increase in the phytoremediation potential
Increase in shoot dry weight, number of pods per plant and nodule dry weight
Pseudomonas fluorescens,
Pseudomonas alcaligenes PsA15, Pseudomonas denitrificans PsD6
Increase in fresh and dry weight, root and shoot length, number of leaves per plant[55,56]
Bacillus polymyxa BcP26,
Mycobacterium phlei MbP18,
Cellulomonas sp. 32
Increase in root and shoot growth, nodulation, increase in N and P content[55]
Phaseolus vulgaris
(French bean)
Pseudomonas lurida NPRp15, Pseudomonas putida PGRs4Increased root and shoot dry weight, nodulation, nutrient uptake, pod yield[57]
Vigna unguiculata (Cowpea)Pontibacter niistensis NII-0905Increase in root number, root length, shoot length and dry biomass[58]
Table 2. Range of nitrogen fixed by associations of important legume crops with rhizobia.
Table 2. Range of nitrogen fixed by associations of important legume crops with rhizobia.
Legume CropAssociated Rhizobial StrainsAmount of N Fixed (kg ha−1)Method of EstimationReference
Cicer arietinumBradyrhizobium ciceri bvs. CP31, CP3619–2415N isotope dilution[75]
Rhizobium sp.15–3215N natural abundance[76]
Cajanus cajanRhizobium sp. IHP11413–69N Difference[77]
Vigna radiataBradyrhizobium japonicum 542116N Difference[78]
Lens culinarisRhizobium leguminosarum bv. viciae su3912515N isotope dilution[79]
Rhizobium leguminosarum0–10515N isotope dilution[80]
Rhizobium sp.37–5515N natural abundance[81]
Bradyrhizobium sp.82N Difference[82]
Phaseolus vulgarisRhizobium leguminosarum bv. phaseoli24–3915N isotope dilution[83]
Rhizobium leguminosarum bv. phaseoli11–16515N isotope dilution[84]
Phaseolus vulgarisRhizobium phaseoli78.715N isotope dilution[85]
Vicia fabaRhizobium leguminosarum bv. viciae76–12515N isotope dilution[75]
Bradyrhizobium sp.210N Difference[82]
Rhizobium phaseoli3.8acetylene reduction[85]
Pisum sativumRhizobium leguminosarum bv. viciae su-39134–11215N isotope dilution[79]
Bradyrhizobium sp.128N Difference[82]
Rhizobium leguminosarum bv. viciae31–10715N isotope dilution[75]
Arachis hypogaeaRhizobium sp.186N Difference[86]
Bradyrhizobium sp.150–20015N isotope dilution[87,88]
Glycine maxBradyrhizobium japonicum102.915N isotope dilution[85]
Bradyrhizobium japonicum25.6acetylene reduction[85]
Bradyrhizobium sp.108–15215N isotope dilution[88]
Table 3. P nutrition of legume crops mediated by plant growth-promoting rhizobacteria.
Table 3. P nutrition of legume crops mediated by plant growth-promoting rhizobacteria.
Pseudomonas aeruginosaCicer arietinum[100]
Pseudomonas alcaligenes, Bacillus pumilusCicer arietinum[24]
Bacillus megateriumLens culinaris[28]
Bacillus megateriumPhaseolus vulgaris[47]
Pseudomonas fluorescensArachis hypogaea[41]
Pseudomonas lurida-NPRp15 and Pseudomonas putida-PGRs4Phaseolus vulgaris[57]
Bacillus subtilisVigna radiata[32]
Table 4. ACC-deaminase producing PGPR strains promoting growth and stress alleviation in legume crops.
Table 4. ACC-deaminase producing PGPR strains promoting growth and stress alleviation in legume crops.
Legume CropAssociated PGPREffectReference
Cicer arietinumSerratia proteamaculans J119Improved root and shoot growth, nodulation, grain yield[169]
Mesorhizobium ciceri LMS1Increase in nodulation and plant growth[164]
MesorhizobiumImproved plant growth under salinity stress[170]
Lens culinarisBacillus cereus,
Pseudomonas sp.
Promoted plant growth under axenic conditions[171]
Vigna radiataPseudomonas putida,
Pseudomonas fluorescens, Bradyrhizobium japonicum
Root elongation, increase in nodule number, nodule fresh and dry weight[172]
Pseudomonas fluorescens,
Pseudomonas syringae,
Rhizobium phaseoli
Significantly reduced salinity stress and increase plant growth[173]
Pisum sativumRhizobium leguminosarum
bv. viciae 128C53K
Increased nodulation[162]
Arthrobacter protophormiaeIncreased plant tolerance to salt stress and improved plant growth[174]
Pseudomonas brassicacearum Am3,
Pseudomonas marginalis Dp1,
Enhanced nutrient uptake[175]
Pseudomonas fluorescens, Pseudomonas putida,Reduced drought stress on plant[176]
Variovorax paradoxus 5C2Improved growth, yield and water use efficiency of drought stressed plants[177]
Glycine maxPseudomonas sp.Increased plant growth and reduced plant fungal disease[178]
Arachis hypogaeaPseudomonas sp.Enhanced growth, yield and nutrient uptake[41]
Pseudomonas fluorescens TDK1Enhanced resistance to saline stress[179]
Cyamopsis tetragonoloba (Cluster bean)Pseudomonas sp.Improved nodulation and plant growth[180]
Vigna unguiculataPseudomonas sp.Improved plant growth under salt stress[181]
Table 5. Effect of co-inoculation on plant growth and development.
Table 5. Effect of co-inoculation on plant growth and development.
Co-Inoculated StrainsLegume PlantPositive Effects on Plant Growth ParametersReference
Rhizobium leguminosarum bv. viciae, Pseudomonas sp. (PSB), Pseudomonas sp. (PGPR)Lens culinaris81% increase in nodule number, 57% increase in nodule dry weight and 15% improvement in grain yield *[192]
Rhizobium CRM 6,
Bacillus polymyxa (PSB),
PGPR (KB 133)
Vigna radiata110% increase in nodule number, 121% increase in nodule weight and 44% increase in grain yield *[193]
Bacillus amyloliquefaciens LL2012,
Bradyrhizobium japonicum
Glycine max50% increase in shoot dry weight and 40% increase in root dry weight #[43]
Mesorhizobium ciceri CH-1233, Pseudomonas sp. LK884Cicer arietinum56% increase in nodule number, 100% increase in nodule dry weight, and 15% increase in grain yield *[194]
Bradyrhizobium sp.,
Serratia marcescens, Trichoderma harzianum
Arachis hypogaea115% increase in nodule number, 94% increase in nodule dry weight and 41% increase in grain yield *[195]
Azotobacter chroococcum
Cajanus cajan248% increase in nodule number, 100% increase in nodule dry weight and 92% increase in N fixation, and 19% increase in grain yield #[196]
Pseudomonas fluorescens
Cajanus cajan388% increase in nodule number, 267% increase in nodule dry weight and 134% increase in N fixation and 66% increase in grain yield #[196]
Bacillus cereus
Cajanus cajan382% increase in nodule number, 196% increase in nodule dry weight and 116% increase in N fixation and 54% increase in grain yield #[196]
Glomus fasciculatum (VAM), RhizobiumCajanus cajan19% increase in chlorophyll content, 10% increase in N content and 114% increase in P content #[197]
* Study performed in field; # Study carried out in pot conditions.
Table 6. Whole genome data of PGPR available in worldwide web.
Table 6. Whole genome data of PGPR available in worldwide web.
PGPRHost PlantGenome Size (Mb)Reference
Mesorhizobium ciceri CC1192Cicer arietinum6.94[198]
Herbaspirillum lusitanum P6-12Phaseolus vulgaris4.46[199]
Bradyrhizobium yuanmingense BR 3267Vigna unguiculata7.90[200]
Sinorhizobium fredii USDA257Glycine max6.47[201]
Bradyrhizobium japonicum CPAC 15, Bradyrhizobium diazoefficiens CPAC 7Glycine max9.58[202]
Stenotrophomonas maltophilia RR-10Oryza sativa (Rice)4.66[203]
Pseudomonas strain R62 and R81Triticum sp. (Wheat)6.00[204]
Bacillus amyloliquefaciens BS006Musa sp. (Banana)4.17[205]
Azospirillum brasilense CBG497Zea mays (Maize)6.50[206]
Table 7. Commonly employed molecular techniques to profile the PGPR diversity.
Table 7. Commonly employed molecular techniques to profile the PGPR diversity.
MethodPGPR Community/Source PlantReference
16S rDNA sequencingRhizobia, Pantoea agglomerans, Exiguobacterium, Ensifer, Bacillus sp., Pseudomonas and Leclercia[209,210,211,212]
16S-23S IGS sequencingRhizobium leguminosarum bv. viciae, trifolii, and phaseoli, Mesorhizobium populations[213,214]
REP-PCR, ERIC-PCR DNA fingerprintingMesorhizobia sp.[215]
Rhizobium meliloti solates[216]
Rhizobia associated with Belgium legumes[217]
Box PCRMesorhizobium populations associated from Chickpea[214]
Rhizobia associated with common bean[218]
ARDRAMesorhizobium, common bean rhizobia[214,218]
MLSAgyrB (DNA gyrase), rpoD (RNA polymerase) of Pseudomonas[217]
atpD (ATP synthase)[219]
gyrB, nifK and nod genes of Mesorhizobium,[220]
recA of Burkholderia sp.[221]
RAPD-PCRRhizobium leguminosarum bv. viciae strains, Azotobacter and Trichoderma strains,
Bradyrhizobium japonicum strains
DGGEAzospirillum brasilense in maize[225]
Acinetobacter community from wheat
Rhizospheric microbial community in pigeonpea
Table 8. Genes activated during direct mode of action of PGPR.
Table 8. Genes activated during direct mode of action of PGPR.
PGP TraitRelated GenesPGPR StrainsReferences
Nitrogen fixationnifH, nifD, nifK
(nitrogenase iron protein)
Paenibacillus sp., Klebsiella sp., Azospirillum sp., Burkholderia sp., Bacillus sp., Mesorhizobium sp.[229,230,231]
Phosphate solubilizationpqqC, pqqBCD,
pqqAB, pqqE, pqqF (Pyrrolo Quinoline Quinone Synthase)
gdh (Glucose Dehydrogenase, cofactor for pqq genes)
Pseudomonas sp.,
Pseudomonas fluorescens QAU67,
Pseudomonas putida QAU90,
Bacillus sp.
Siderophores productionpupa (siderophore transporter),
sid (siderophore synthesis),
dhbF (2,3-Dihydroxy Benzoate synthesis gene)
Pseudomonas putida
Bacillus subtilis AH18
Bacillus licheniformis K11
IAA synthesisnhase (nitrile hydratase),
amd (amidase),
ipdC (indole-3-pyruvate decarboxylase),
aec (auxin efflux carrier protein)
Rhodococcus erythropolis,
Pseudomonas putida
Bacillus subtilis AH18
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Swarnalakshmi, K.; Yadav, V.; Tyagi, D.; Dhar, D.W.; Kannepalli, A.; Kumar, S. Significance of Plant Growth Promoting Rhizobacteria in Grain Legumes: Growth Promotion and Crop Production. Plants 2020, 9, 1596.

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Swarnalakshmi K, Yadav V, Tyagi D, Dhar DW, Kannepalli A, Kumar S. Significance of Plant Growth Promoting Rhizobacteria in Grain Legumes: Growth Promotion and Crop Production. Plants. 2020; 9(11):1596.

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Swarnalakshmi, Karivaradharajan, Vandana Yadav, Deepti Tyagi, Dolly Wattal Dhar, Annapurna Kannepalli, and Shiv Kumar. 2020. "Significance of Plant Growth Promoting Rhizobacteria in Grain Legumes: Growth Promotion and Crop Production" Plants 9, no. 11: 1596.

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