Microbiome in Crops: Diversity, Distribution, and ...

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15 Microbiome in Crops: Diversity, Distribution, and Potential Role in Crop Improvement Ajar N. Yadav⁎, Vinod Kumar⁎, Harcharan S. Dhaliwal⁎, Ram Prasad†, Anil K. Saxena‡ ⁎

Eternal University, Sirmour, India †Amity University, Noida, India ‡ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, India

1 INTRODUCTION The global necessity to increase agricultural production from a steadily decreasing and degrading land resource base has placed considerable strain on the fragile agroecosystems. Microbial diversity in soil is considered important for maintaining the sustainability of agriculture production systems. There are many links between microbial diversity and ecosystem processes. A microbe helps plant for growth, yield, and adaptation. Microbes associated with crops could be classified into three groups, for example, rhizospheric, phyllospheric, and endophytic. Region of contact between root and soil where soil is affected by roots is designated as “rhizosphere.” Microbes associated with rhizosphere of any plant are said as rhizospheric microbes. The rhizosphere is the zone of soil influenced by roots through the release of substrates that affect microbial activity. A number of microbial species have been reported associated with the plant rhizosphere belonging to genera Azospirillum, Alcaligenes, Arthrobacter, Acinetobacter, Bacillus, Paenibacillus, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Methylobacterium, Pseudomonas, Rhizobium, and Serratia (Xie et al., 1996; Lavania et al., 2006; Chaiharn and Lumyong, 2011; Yadav et al., 2011, 2014, 2016a; Meena et al., 2012; Kumar et al., 2016; Shah et al., 2017; Suman et al., 2016a). The endophytic microbes are referred to those microorganisms that colonizes in the interior of the plant parts, namely, root, stem, or seeds without causing any harmful effect on host plant. The word endophyte means “in the plant” and is derived of the Greek words endon (within) and phyton (plant). Endophytes inside a plant may either become localized at the point of entry or spread throughout the plant.

Crop Improvement through Microbial Biotechnology https://doi.org/10.1016/B978-0-444-63987-5.00015-3

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These microorganisms can reside within cells (Jacobs et al., 1985), in the intercellular spaces (Patriquin and Döbereiner, 1978), or in the vascular system (Bell et al., 1995). Endophytic microbes enter plants mainly through wounds, naturally occurring as a result of plant growth or through root hairs and at epidermal conjunctions. Besides providing entry avenues, wounds also create favorable conditions for the bacteria by allowing leakage of plant exudates that serve as a nutrient source for the bacteria (Quadt-Hallmann et al., 1997). Endophytic microbes live in plant tissues without causing substantive harm to the host. They exist within the living tissues of most plant species in the form of symbiotic association to slightly pathogenic. These bacteria have been isolated from a variety of plants including wheat (Coombs and Franco, 2003; Jha and Kumar, 2009; Verma et al., 2014a, 2015a, 2016a), rice (Mano and Morisaki, 2007; Naik et al., 2009; Piromyou et al., 2015), maize (Araújo et al., 2000; Montanez et al., 2012; Thanh and Diep, 2014), soybean (Hung and Annapurna, 2004; Mingma et al., 2014), pea (Narula et al., 2013; Tariq et al., 2014), common bean (Suyal et al., 2015), chickpea (Saini et al., 2015), and pearl millet (Beatriz Sánchez et al., 2014). A large number of endophytic bacterial species belonging to different genera including Achromobacter, Azoarcus, Burkholderia, Enterobacter, Gluconacetobacter, Herbaspirillum, Klebsiella, Microbiospora, Micromonospora, Nocardioides, Pantoea, Planomonospora, Pseudomonas, Serratia, Streptomyces, and Thermomonospora (Verma et al., 2014a, 2015a; Ryan et al., 2008; Hallmann et al., 1997) have been sorted out from different host plants. The phyllosphere is common niche for synergism between bacteria and plant. Microbes on leaf surface are most adapted microbes as they tolerate high temperature (40–55°C) and UV radiation. Many bacteria such as Agrobacterium, Methylobacterium, Pantoea, and Pseudomonas have been reported in the phyllosphere (Yadav, 2009; Verma et al., 2014a, 2015a, 2016a,b). Microbes associated with crops are able to promote the plant growth. Several microbes have been reported that they can promote plant growth either directly or indirectly. The plant microbiomes (Epiphytic, endophytic, and rhizospheric) have been shown to promote plant growth directly, for example, by fixation of atmospheric nitrogen; solubilization of minerals such as phosphorus, potassium, and zinc; and production of siderophores and plant growth hormones such cytokinin, auxin, and gibberellins (Prasad et al., 2015). Several microbes support plant growth indirectly, via production of antagonistic substances by inducing resistance against plant pathogens (Glick et al., 1999; Tilak et al., 2005; Verma et al., 2017b; Yadav, 2017; Yadav et al., 2017c). Many microbes support plant growth indirectly, by production of antagonistic molecules by inducing resistance against plant pathogens. Plant growth-promoting microbes (PGPMs) are used as biological control agents for the suppression of soilborne pathogens. These PGPMs may promote plant growth in terms of increased germination rates; biomass; leaf area; chlorophyll content; nitrogen content; protein content; hydraulic activity; root and shoot length; yield; and tolerance to abiotic stresses like drought, temperature, flood, and salinity. The PGPMs may be use as bioinoculants so that it fits into a long-term sustainable agricultural systems. Among different cereal crops, leguminous crops (chickpea, pea, soybean, and common bean) and nonleguminous crops (wheat, rice, maize, and millet) are the major grain that sustains humanity. Wheat grows in temperate climate, and it is staple food for 35% of world's population. On other hand, it provides more calories and protein in the diet than any other crops. To provide food security to the ever-increasing population, greater agriculture production is a pressing need in 21st century. The increasing demand for a steady and healthy food supply by a burgeoning human population will require efficient management practices along

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with controlling disease that reduce crop yield. During the last couple decades, agricultural production has increased due to the use of high-yielding varieties and enhanced consumption of chemicals, which are used both as fertilizers to provide nutrition and as protection agents to control the damage caused by phytopathogens. Excessive use of chemicals and change in traditional cultivation practices have resulted in the deterioration of physical, chemical, and biological health of the cultivable soil. An understanding of microbial diversity perspectives in agricultural context is important and useful to arrive at measures that can act as indicator of soil quality and plant productivity. The present book chapter describes the different types of association between microbes and plants. The method of isolation of different groups of microbes associated with plant and role of microbes in crop improvement have been discussed here.

2 ISOLATION AND CHARACTERIZATION OF CROP MICROBIOMES Microbiome of crops is largely influenced by the environmental circumstances surrounding the host plants such as the type and pH of soil, content in soil, rainfall, salinity of soil, and temperatures. To know the diversity and distribution among different groups of microbes associated with different crops in the form of epiphytic, endophytic, and rhizospheric should be isolated using culturable and unculturable techniques. For isolation of endophytes, attention needs to be paid to avoid contamination with undesirable epiphytic microbes. It is recommended to first sterilize the entire surface of the samples, followed by cutting their organs and tissues into pieces with a sterilized knife, if necessary. Sodium hypochlorite is the most commonly used disinfectant. Plant samples usually are sterilized by sequential immersion in 70% ethanol for 1–3 min and 1%–3% sodium hypochlorite for 3–5 min, followed by repeated rinsing in sterile water to remove residual sodium hypochlorite (Suman et al., 2016b). Double or triple surface sterilization with a combination of ethanol and other disinfectants is also recommended to eliminate epiphytic microbes. Sample for isolation of endophytic microbes is macerated independently with 10 mL sterile 0.85% NaCl using a mortar and pestle and further homogenized by vortexing for 60 s at high speed. The solutions are then used for further isolation of microbes (Fig. 1). Epiphytic microbes should be isolated using standard method of imprinting, whereas rhizospheric microbes should be isolated using serial dilution method followed by spread or pour-plate methods. Different specific mediums can be used for isolation of archaea, eubacteria, and fungi (Suman et al., 2016b). The different specific growth medium were used to isolate the maximum possible culturable morphotypes of different groups of microbes such as heterotrophic microbes (nutrient agar), pseudomonads (King's B agar), Arthrobacter (trypticase soy agar), soil-specific microbes (soil-extract agar), Bacillus and Bacillus-derived genera (BBDG) (T3A with heat treatment methods), archaea (chemically defined and complex medium), and fungi (rose bengal and potato dextrose agar) (Verma et al., 2015a; Yadav et al., 2017e,h). To isolate different groups of microbes, all medium and conditions can be used such as for halophilic (with 5%–20% NaCl concentration), drought-tolerant (7%–10% polyethylene glycol), acidophilic (pH 3–5), alkaliphilic (pH 8–11), psychrophilic (incubation at >5°C temperature), and thermophilic (incubation at >45°C temperature) (Fig. 1). The microbes can be further screened for tolerance to temperature, salt (NaCl concentration), drought, and pH according to the method described earlier (Yadav et al., 2015a).

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FIG. 1 A schematic representation of the isolation, characterization, identification, and potential application of culturable and unculturable microbiome of crops.

For identification of microbes, genomic DNA can be isolated using Zymo Research Fungal/ Bacterial DNA MicroPrep following the standard protocol prescribed by the manufacturer. Different primers can be used for amplification of 16S rRNA gene for archaea and bacteria while 18S rRNA gene for fungi. PCR-amplified 16S/18S rRNA genes have to be purified and sequenced. The partial 16S or 18S rRNA gene sequences should be compared with sequences available in the NCBI database. The phylogenetic tree can be constructed on aligned data sets using the neighbor-joining (NJ) method and the program MEGA 4.0.2 (Fig. 2). For characterization of unculturable microbes, cell lysis and DNA extraction of plant roots and rhizospheric soil should be done with a direct DNA extraction procedure. For this, shoot/ root material (15 mL) should be combined in a 30 mL centrifuge tube with 0.25 g SDS, 2 mL of

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FIG. 2 Phylogenetic tree showed the relationship among different groups of microorganisms isolated from 15 different plants.

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1M phosphate buffer, pH 7, and 3 g each glass beads. After shaking in beat beater for 1 min, sample should be centrifuged for 10 min at 10,000×g. The supernatant should be precipitated for 2 h at −20°C with 1 volume of isopropanol, 0.3 M sodium acetate, and pH 5.2. The DNA pellet should be collected by centrifugation at 10,000×g for 10 min, vacuum dried, and resuspended in 5 mL water. DNA purification should be accomplished with the DNA purification system. The resulting purified extract should be dissolved in 50 μL MQ water. The basic steps involved in constructing and exploiting a metagenomic library have been given in Fig. 1. The isolated DNA is called metagenome. This metagenome either can be used directly for sequencing (using specific primer of archaea/bacterial/fungi) or can be cloned into suitable vector to generate the metagenomic library or can be amplified by using universal primers to generate 16S/18S rRNA gene library. For cloning, the most frequently used vectors are the plasmids, but for large gene clusters, other vectors such as bacterial artificial chromosome (BAC), cosmid, and fosmid should be used. The library should be then transferred to Escherichia coli. These clones should be then used for sequencing or screening for gene/ allele, secondary metabolite, or bioactive molecules synthesized by the DNA fragment from samples. The simplified diagrammatic scheme has been presented in Fig. 1 to show steps of isolation, screening, and identification of culturable and unculturable microbes.

3 DIVERSITY AND DISTRIBUTION OF CROP MICROBIOMES The different groups of microbes have been reported as epiphytic, endophytic, and rhizospheric such as archaea, eubacteria, and fungi, which included different phylum mainly Acidobacteria, Actinobacteria, Ascomycota, Bacteroidetes, Basidiomycota, DeinococcusThermus, Euryarchaeota, Firmicutes, and Proteobacteria (Fig. 2). The Proteobacteria were further grouped as α-, β-, γ-, and δ-Proteobacteria. Overall, the distribution of microbes varied in all bacterial phyla; Proteobacteria were most dominant followed by Actinobacteria. Least number of microbes was reported from phylum Deinococcus-Thermus and Acidobacteria followed by Bacteroidetes (Fig. 3). On review of different groups of microbes reported from leguminous and nonleguminous crops, it was found that Acidobacteria, Basidiomycota, Euryarchaeota, and δ-Proteobacteria may not be reported from leguminous crops (Fig. 3). Many novel microbes have been sorted out from leguminous crops including Rhizobium ciceri, Rhizobium mediterraneum, Ochrobactrum ciceri, Rhizobium pusense, Mesorhizobium muleiense, and Ciceribacter lividus from chickpea (Nour et al., 1994, 1995; Imran et al., 2010; Panday et al., 2011; Zhang et al., 2012a; Kathiravan et al., 2013); Rhizobium tropici, Rhizobium gallicum, Rhizobium giardinii, Herbaspirillum lusitanum, Rhizobium lusitanum, Rhizobium freirei, Rhizobium paranaense, Rhizobium azibense, and Rhizobium ecuadorense from common bean (Martínez-Romero et al., 1991; Amarger et al., 1997; Valverde et al., 2003, 2006; Dall'Agnol et al., 2013, 2014; Ribeiro et al., 2015; Mnasri et al., 2014); Paenibacillus mendelii from pea (Šmerda et al., 2005); and Bradyrhizobium pachyrhizi, Flavobacterium glycines, Bradyrhizobium huanghuaihaiense, Streptomyces heilongjiangensis, Bradyrhizobium ottawaense, Sphingobacterium yanglingense, and Plantactinospora soyae from soybean (Ramírez-Bahena et al., 2009; Madhaiyan et al., 2010; Zhang et al., 2012b; Liu et al., 2013; Yu et al., 2014; Peng et al., 2014; Guo et al., 2016). The novel species of different microbes have been isolated from nonleguminous crops worldwide and reported from different domain archaea, bacteria, and

3 DIVERSITY AND DISTRIBUTION OF CROP MICROBIOMES

FIG. 3

Abundance of microbiome belonging diverse phylum and groups reported different crops.

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eukarya such as Acidovorax radicis, Herbaspirillum hiltneri, Saccharopolyspora shandongensis, and Paenibacillus hispanicus from wheat (Li et al., 2011; Rothballer et al., 2006; Zhang et al., 2008; Menéndez et al., 2016; Yadav et al., 2017b,g); Ochrobactrum oryzae, Paenibacillus hunanensis, Methylogaea oryzae, Methylophilus glucosoxydans, Flavobacterium aquaticum, Spirosoma oryzae, Rhizobium rhizoryzae, Paenibacillus rhizoryzae, Rhizobium oryzicola, Clostridium oryzae, Roseomonas oryzicola, Rhizobium oryziradicis, Chromobacterium rhizoryzae, and Bacillus oryzisoli from rice (Tripathi et al., 2006; Liu et al., 2010; Geymonat et al., 2011; Doronina et al., 2012; Subhash et al., 2013; Ahn et al., 2014; Zhang et al., 2014; Zhang et al., 2015a,b; Horino et al., 2015; Chung et al., 2015; Zhao et al., 2016; Zhou et al., 2016; Zhang et al., 2016); and Paenibacillus brasilensis, Pediococcus stilesii, Microbacterium neimengense, Paenibacillus zeae, Chryseobacterium endophyticum, Dyadobacter endophyticus, and Nocardioides zeicaulis from maize (von der Weid et al., 2002; Franz et al., 2006; Gao et al., 2013, 2016; Liu et al., 2015; Lin et al., 2016; Kämpfer et al., 2016). Microbes have been reported as both culture-dependent and culture-independent approach. It is possible to assess only a small fraction of the microbial diversity associated with plants using the isolation methods described above because few microbial species can be cultivated using traditional laboratory methods. The sizes of microbial communities as determined using culture-independent methods might be 100- to 1000-fold larger than communities uncovered via traditional isolation. Archaea were also reported as associated with maize and rice using unculturable method only. There was the first report on archaea that to be identified as endophytes associated with rice by the culture-independent approach. Methanospirillum sp. and Candidatus. Methanoregula boonei have been reported as endophytic archaea from rice (Sun et al., 2008). The archaea that has been isolated from phylum Euryarchaeota belonged to different genera such as Haloferax, Methanobacterium, Methanosaeta, Methanospirillum, and Thermoplasma (Chelius and Triplett, 2001). On review of different eight crops, it was found that microbes that were most predominant and studied belong to six major phyla Actinobacteria, Ascomycota, Bacteroidetes, Deinococcus-Thermus, Firmicutes, and Proteobacteria (Table 1). Among 116 reported genera from eight cereal crops, 40 microbes were reported as most predominant, namely, Achromobacter, Acidovorax, Acinetobacter, Acremonium, Agrobacterium, Alcaligenes, Aspergillus, Azoarcus, Azospirillum, Azotobacter, Bacillus, Bradyrhizobium, Brevundimonas, Burkholderia, Chaetomium, Cladosporium, Deinococcus, Delftia, Enterobacter, Erwinia, Flavobacterium, Herbaspirillum, Klebsiella, Methanospirillum, Methylobacterium, Microbacterium, Microbispora, Nocardioides, Ochrobactrum, Paecilomyces, Paenibacillus, Pantoea, Penicillium, Pseudomonas, Rhizobium, Serratia, Sphingomonas, Staphylococcus, Stenotrophomonas, and Streptomyces (Table 1). Among 40 genera (most predominant), Achromobacter, Agrobacterium, Alcaligenes, Aspergillus, Azospirillum, Azotobacter, Bacillus, Bradyrhizobium, Enterobacter, Herbaspirillum, Microbacterium, Paenibacillus, Penicillium, Pseudomonas, Rhizobium, Serratia, Staphylococcus, and Streptomyces were most dominant and reported from more than four associated crops (Table 1). Most studies on the occurrence of microbes have been performed using culture-dependent approaches. The member Bacillus and Bacillus-derived genera (BBDG) are associated with different plant and show different plant growth-promoting attributes such as solubilization of phosphorus, potassium, and zinc and production of phytohormones and biocontrol against different pathogens. BBDG has been consistently described as culturable bacteria that can colonize wheat (Verma et al., 2014a, 2015a, 2016b), rice (Sun et al., 2008), maize (Liu et al., 2015;

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TABLE 1 Diversity and Distribution of Microbiome of Leguminous and Nonleguminous Crops

Chickpea

Common Bean

β-Proteobacteria β-Proteobacteria γ-Proteobacteria Ascomycota α-Proteobacteria β-Proteobacteria Ascomycota β-Proteobacteria α-Proteobacteria γ-Proteobacteria Firmicutes α-Proteobacteria α-Proteobacteria β-Proteobacteria Ascomycota Ascomycota Deinococcus-Thermus β-Proteobacteria γ-Proteobacteria γ-Proteobacteria Bacteroidetes β-Proteobacteria γ-Proteobacteria Euryarchaeota α-Proteobacteria Actinobacteria Actinobacteria Actinobacteria α-Proteobacteria Ascomycota Firmicutes γ-Proteobacteria Ascomycota γ-Proteobacteria α-Proteobacteria γ-Proteobacteria α-Proteobacteria Firmicutes γ-Proteobacteria Actinobacteria

Pea

Achromobacter Acidovorax Acinetobacter Acremonium Agrobacterium Alcaligenes Aspergillus Azoarcus Azospirillum Azotobacter Bacillus Bradyrhizobium Brevundimonas Burkholderia Chaetomium Cladosporium Deinococcus Delftia Enterobacter Erwinia Flavobacterium Herbaspirillum Klebsiella Methanospirillum Methylobacterium Microbacterium Microbispora Nocardioides Ochrobactrum Paecilomyces Paenibacillus Pantoea Penicillium Pseudomonas Rhizobium Serratia Sphingomonas Staphylococcus Stenotrophomonas Streptomyces

Soybean

1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30. 31. 32. 33. 34. 35. 36. 37. 38. 39. 40.

Leguminous

Millet

Taxonomical Affiliation Maize

Plant Associated Microbes

Wheat

S. No.

Rice

Nonleguminous

see the legend on next page

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Kämpfer et al., 2016), pea (Šmerda et al., 2005), soybean (Hung and Annapurna, 2004), common bean (Figueiredo et al., 2008), and chickpea (Saini et al., 2015). The members of Enterobacter bacteria have been reported from different plants such as wheat (Verma et al., 2014a), rice (Piromyou et al., 2015), maize (Montanez et al., 2012), and pea (Tariq et al., 2014). The genus Burkholderia has been reported in different plants such as rice (Govindarajan et al., 2008; Rangjaroen et al., 2014) and maize (Bevivino et al., 1998). Pseudomonas are ubiquitous in nature, is a member of γ-Proteobacteria, and has been also reported from different plant tissues such as wheat (Verma et al., 2014a), rice (Sun et al., 2008), maize (Thanh and Diep, 2014; Szilagyi-Zecchin et al., 2014), and millet (Gupta et al., 2013). The pink-pigmented facultative methylotrophs (PPFMs) have been reported from diverse host plants such as wheat (Yadav, 2009; Verma et al., 2015a), rice (Dourado et al., 2015), and common bean (de Oliveira Costa et al., 2012). In plant colonization, the frequency and distribution may be influenced by plant genotype or by interactions with other associated microorganisms, which may result in increasing plant fitness. The different species of Pantoea have been described as cosmopolitan found associated with wheat (Verma et al., 2014b), rice (Rangjaroen et al., 2014), and maize (Ikeda et al., 2013). Members of Pantoea are ubiquitous in plant tissue; they are able to influence plant growth through the production of auxins or cytokinins and induce systemic resistance against diseases (Fig. 4). There were many microbes found to be common in more than three associated crops. Along with common microbial genera, there were many niche-specific microbial genera that have been reported from all eight crops such as Micrococcus, Micromonospora, Planobispora, Planomonospora, Rhodococcus, Saccharopolyspora, and Thermomonospora from wheat; Alkanindiges, Caulobacter, Chromobacterium, Comamonas, Cryptococcus, Curvibacter, Cytophagales, Gallionella, Holophaga, Humicola, Hydrogenophaga, Kaistina, Methylogaea, Methylophaga, Methylophilus, Mitsuaria, Novosphingobium, Phialophora, Rhodopseudomonas, Rhodosporidium, Roseomonas, Sinorhizobium, Speiropsis, Spirosoma, Stemphylium, and Torulaspora from rice; Corynebacterium, Streptosporangium, Dyadobacter, Pedobacter, Haloferax, Methanobacterium, Methanosaeta, Thermoplasma, Pediococcus, Gluconacetobacter, and Rhanella from maize; Clavibacter, Plantactinospora, Tsukamurella, Alternaria, Colletotrichum, Curvularia, Drechslera, Scopulariopsis, Niabella, Sphingobacterium, Leuconostoc, and Rhodanobacter from soybean; and Lysinibacillus, Ciceribacter, Ensifer, Mesorhizobium, and Janthinobacterium from chickpea (Fig. 5). There are very few reports for niche-/crop-specific microbes from crops system, but there were many reports on niche specificity of microbes from different extreme habitats (Kumar et al., 2014a,b; Pandey et al., 2013; Yadav et al., 2015b, 2016b, 2017f; Saxena et al., 2016). Wheat (Triticum aestivum) (Coombs and Franco, 2003; Jha and Kumar, 2009; Verma et al., 2014a, 2015a, 2016a,b; Li et al., 2011; Rothballer et al., 2006; Zhang et al., 2008; Menéndez et al., 2016), rice (Oryza sativa) (Mano and Morisaki, 2007; Naik et al., 2009; Piromyou et al., 2015; Zhou et al., 2016; Sun et al., 2008; Rangjaroen et al., 2014; Tian et al., 2007; Govindarajan et al., 2008; Elbeltagy et al., 2000; Krause et al., 2006; Ji et al., 2014), maize (Zea mays) (Montanez et al., 2012; Thanh and Diep, 2014; Hallmann et al., 1997; Kämpfer et al., 2016; Chelius and Triplett, 2001; Mcinroy and Kloepper, 1995; Araújo et al., 2000; Rawat and Mushtaq, 2016), pearl millet (Pennisetum glaucum) (Beatriz Sánchez et al., 2014; Hallmann et al., 1997; Gupta et al., 2013; Rosenblueth and MartínezRomero, 2006; Ezekiel et al., 2014; Rafi et al., 2012), soybean (Glycine max) (Hung and Annapurna, 2004; Guo et al., 2016; Pimentel et al., 2006; Okubo et al., 2009; Selvakumar et al., 2013; Subramanian et al., 2014; Mingma et al., 2014), common bean (Phaseolus vulgaris) (Suyal et al., 2015; Martínez-Romero et al., 1991; Ribeiro et al., 2015; de Oliveira Costa et al., 2012; Sánchez et al., 2014), pea (Pisum sativum) (Narula et al., 2013; Tariq et al., 2014; Šmerda et al., 2005; Hynes et al., 2008), and chickpea (Cicer arietinum) (Saini et al., 2015; Panday et al., 2011; Kathiravan et al., 2013; Hynes et al., 2008; Nadwani and Dudeja, 2013; Dudeja, 2013; Joseph et al., 2012; Valverde et al., 2007; Küçük and Kivanc, 2008; Kundu et al., 2009; Yadav et al., 2010; Singh et al., 2013; Kaur and Sharma, 2013; Zaheer et al., 2016; Zhang et al., 2017).

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100%

90%

80%

Relative distributions

70%

60%

50%

40%

30%

20%

10%

a pe C hi ck

C

om

m

on

be

an

Pe a

n So yb

ea

t ille M

ai ze M

R ic e

W

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at

0%

Achromobacter Actinoallomurus Alkanindiges Azospirillum Brevundimonas Chaetomium Clavibacter Enterobacter Fusarium Janthinobacterium Methanobacterium Methylogaea Micromonospora Paenibacillus Planobispora Rhizoctonia Roseomonas Speiropsis Staphylococcus

FIG. 4

Acidovorax Aeromonas Alternaria Azotobacter Burkholderia Chryseobacterium Deinococcus Erwinia Gluconacetobacter Klebsiella Methanosaeta Microbacterium Nocardioides Pantoea Planomonospora Rhodanobacter Scopulariopsis Sphingobacterium Stenotrophomonas

Acinetobacter Agrobacterium Aspergillus Bacillus Candidatus Ciceribacter Delftia Exiguobacterium Haloferax Lysinibacillus Methanospirillum Microbispora Ochrobactrum Paracoccus Pseudomonas Rhodopseudomonas Serratia Sphingomonas Streptomyces

Diversity and distribution of microbiome of different crops.

Acremonium Alcaligenes Azoarcus Bradyrhizobium Caulobacter Cladosporium Ensifer Flavobacterium Herbaspirillum Mesorhizobium Methylobacterium Micrococcus Paecilomyces Penicillium Rhizobium Rhodosporidium Sinorhizobium Spirosoma Thermomonospora

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FIG. 5 Venn diagram showing niche-specific microbes reported from leguminous and nonleguminous crops.

4 BENEFICIAL ROLE OF MICROBES IN CROP IMPROVEMENT Plants play an important role in selecting and enriching the types of bacteria by the constituents of their root exudates. Thus, depending on the nature and concentrations of organic constituents of exudate and the corresponding ability of the microbes to utilize these as sources of energy, the microbial community develops in the interaction as epiphytic/endophytic/rhizospheric. There is a continuum of the microbial presence in phyllosphere, rhizosphere, and internal plant tissues. Microbes associated with crops are of agriculturally important as they can enhance plant growth and improve plant nutrition through biological N2 fixation and other mechanisms (Yadav et al., 2017e). Microbes may increase crop yields, remove contaminants, inhibit pathogens, and produce fixed nitrogen or novel substances (Quadt-Hallmann et al., 1997). The growth stimulation by microbes can be a consequence of biological N2-fixation (de Bruijn et al., 1997; Suman et al., 2001; Iniguez et al., 2004; Taulé et al., 2012; Pankievicz et al., 2015); production of phytohormones, such as IAA and cytokinins (Verma et al., 2015a; Lin and Xu, 2013; Rashid et al., 2012); biocontrol of phytopathogens through the production of antifungal or antibacterial agents (Raaijmakers et al., 2002; Errakhi et al., 2016); siderophores production (Leong, 1986; Ellis, 2017); nutrient competition (Bach et al., 2016); and induction of acquired host resistance (Pal and Gardener, 2006; Van Loon et al., 1998), enhancing the bioavailability of minerals (Haas and Défago, 2005). Sustainable agriculture requires the use of strategies to increase or maintain the current rate of food production while reducing damage to the environment and human health (Yadav et al., 2017a). The use of microbial plant growth promoters is an alternative to conventional agricultural technologies (Kour et al., 2017a; Yadav et al., 2017c,j). Plant growth-promoting microbes can affect plant growth directly or indirectly. The direct promotion of plant growth by PGP microbes, for the most part, entails providing the plant with a compound that is synthesized by the bacterium or facilitating the uptake of certain nutrients from the environment. The indirect promotion of plant growth occurs when PGP microbes decrease or prevent the deleterious effects of one or more phytopathogenic organisms.

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4.1 Phytohormones Production Plant-associated microbes typically produced plant growth hormones such as auxins and gibberellins. The gibberellin production is most typical for the root-associated microbes, and auxin production is common to all plant-associated microbes. Auxins are a group of indole derivatives that have various growth-promoting functions in plants, such as promotion of root formation; regulation of fruit ripening; and stimulation of cell division, extension, and differentiation. Indoleacetic acid (IAA) is the most well-known auxin. Auxins can promote the growth of roots and stems quickly (by increasing cell elongation) or slowly (through cell division and differentiation). The production of such growth regulators by microbes provides numerous benefits to the host plant including the facilitation of root system expansion, which enhances the absorption of water and nutrients and improves plant survival. The ability to synthesize these phytohormones is widely distributed among plant-associated microbes, and IAA may potentially be used to promote plant growth or suppress weed growth. Diverse microbial species possess the ability to produce the auxin phytohormone IAA. Different biosynthesis pathways have been identified, and redundancy for IAA biosynthesis is widespread among plant-associated bacteria. Interactions between IAA-producing bacteria and plants lead to diverse outcomes on the plant side, varying from pathogenesis to phytostimulation. Reviewing the role of bacterial IAA in different microorganism-plant interactions highlights the fact that bacteria use this phytohormone to interact with plants as part of their colonization strategy, including phytostimulation and circumvention of basal plant defense mechanisms. Isolates producing IAA have stimulatory effect on the plant growth. Egamberdieva (2009), reported that IAA-producing bacterial strains such as Pseudomonas aurantiaca TSAU22, Pseudomonas extremorientalis TSAU6, and Pseudomonas extremorientalis TSAU20 significantly increased seedling root growth up to 25% in nonsalinated conditions and up to 52% at 100 mM NaCl, compared with control plants. The action of phytohormoneproducing bacteria and plant growth regulators on germination and seedling growth of wheat under saline conditions were studied. Seed dormancy enforced by salinity (100 mM NaCl) was substantially alleviated, and the germination was promoted by gibberellin, auxin, zeatin, and ethephon from 54% to 97%. Thanh and Diep (2014) reported 301 endophytic bacteria in maize plant cultivated on acrisols of the eastern of South Vietnam. Isolates were sort out, and all of them have the ability of nitrogen fixation and phosphate solubilization together with IAA biosynthesis, but there were 30 isolates having the best characteristics, and they were identified as maize endophytes and nifH gene owners. Endophytic bacteria were identified as Bacillus, Azotobacter, and Enterobacter. Cytokinins are a group of compound with the backbone of adenine having a substitution at the N-6 atom of the purine ring. These compounds are important in many steps of plant development, as they stimulate plant cell division, induce germination of seeds, activate dormant buds, and play a role in apical dominance. Cytokinins also induce the biosynthesis of chlorophyll, nucleic acids, and chloroplast proteins at the early stages of leaf development. Both pathogenic and beneficial plant-associated bacterial species are capable of synthesizing cytokinins. Among plant-associated methylotrophs, species such as Methylovorusmays and Methylobacterium mesophilicum JCM2829 synthesize and excrete cytokinins (Ivanova et al., 2001, 2008).

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Verma et al. (2014a) have isolated wheat-associated bacteria (epiphytic, endophytic, and rhizospheric) from five locations in central zone (one of the wheat agroecological zones) in India. A total of 222 rhizospheric bacteria were isolated, belonging to 12 genera, namely, Acinetobacter, Bacillus, Duganella, Exiguobacterium, Kocuria, Lysinibacillus, Micrococcus, Paenibacillus, Pantoea, Pseudomonas, Serratia, and Stenotrophomonas. From the phyllosphere, a total of 89 bacteria were isolated belonging to different genera of Arthrobacter, Bacillus, Corynebacterium, Methylobacterium, Paenibacillus, Pseudomonas, and Psychrobacter; and 37 endophytic bacteria were isolated and identified belonging to genera of Delftia, Micrococcus, Pseudomonas, and Stenotrophomonas. Among the total isolates, 12% isolates produced IAA. According to Verma et al. (2015a), the biodiversity of wheat-associated bacteria from the northern hills zone of India was deciphered. A total of 247 bacteria were isolated from five different sites. Analysis of these bacteria by amplified ribosomal DNA restriction analysis (ARDRA) using three restriction enzymes, AluI, MspI, and HaeIII, led to the grouping of these isolates into 19–33 clusters for the different sites at 75% similarity index. Among all isolated bacteria, 14% showed IAA production in which strain IARI-HHS1-3 showed highest IAA production (70.8 ± 1.5 μg mg−1 protein day−1) followed by IARI-HHS1-8 (69.1 ± 0.5 μg mg−1 protein day−1). Tabatabaei et al. (2016) have reported Pseudomonas isolated from wheat. An in vitro experiment was conducted to observe the effect of the inoculation of four indole-3-acetic acid (IAA)-producing Pseudomonas isolates and exogenous IAA on seed germination traits and α-amylase activity of durum wheat. The results showed inoculation with all bacterial isolates led to a decrease in the germination percent, although the extent of the depression varied with the isolate. A significant relationship between concentrations of bacterial IAA and the germination inhibition percent in durum wheat seeds by different bacterial strains was observed.

4.2 Solubilization of Phosphorus, Potassium, and Zinc Phosphorus (P) is major essential macronutrients for biological growth and development. Microorganisms offer a biological rescue system capable of solubilizing the insoluble inorganic P of soil and make it available to the plants. The ability of some microorganisms to convert insoluble phosphorus (P) to an accessible form, like orthophosphate, is an important trait in PGP microbes for increasing plant yields. The rhizospheric phosphate utilizing bacteria could be a promising source for plant growth-promoting agent in agriculture. Phosphate solubilization is a common trait among microbes associated with different crops. For instance, the majority of microbial populations from wheat, rice, maize, and legumes were able to solubilize mineral phosphates in plate assays, and a vast number of PGP microbes with phosphate-solubilizing property have been reported that include members belonging to Burkholderia, Enterobacter, Halolamina, Pantoea, Pseudomonas, Citrobacter, and Azotobacter (Verma et al., 2014a, 2015a, 2016a; Forchetti et al., 2007; Kumar et al., 2017; Yadav et al., 2016c, 2017c,i; Singh et al., 2016; Gaba et al., 2017). Possible mechanisms for solubilization from organic bound phosphate involve either of three enzymes, namely, C-P lyase, nonspecific phosphatases, and phytases. However, most of the bacterial genera solubilize phosphate through the production of organic acids such as gluconate, ketogluconate, acetate, lactate, oxalate, tartarate, succinate, citrate, and glycolate (Khan et al., 2009; Stella and Halimi, 2015; Yadav, 2015). Type of organic acid produced for P solubilization may depend upon the carbon source utilized as substrate. Highest P solubilization has been observed when glucose,


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sucrose, or galactose has been used as sole carbon source in the medium (Khan et al., 2009; Vyas and Gulati, 2009; Park et al., 2010). According to Yadav et al. (2015c), archaea are unique microorganisms that are present in ecological niches of high temperature, pH, and salinity. A total of 157 archaea were obtained from 13 sediment, water, and rhizospheric soil samples collected from Rann of Kutch, Gujarat, India. With an aim to screen phosphate-solubilizing archaea, a new medium was designed as Haloarchaea P Solubilization (HPS) medium. The medium supported the growth and P solubilization activity of archaea. Employing the HPS medium, 20 isolates showed the P solubilization. Phosphate-solubilizing archaea were identified as 17 distinct species of 11 genera, namely, Haloarcula, Halobacterium, Halococcus, Haloferax, Halolamina, Halosarcina, Halostagnicola, Haloterrigena, Natrialba, Natrinema, and Natronoarchaeum. Natrinema sp. strain IARI-WRAB2 was identified as the most efficient P solubilizer (134.61 mg L−1) followed by Halococcus hamelinensis strain IARI-SNS2 (112.56 mg L−1). Saxena et al. (2015) reported that archaeal isolates exhibited phosphate solubilization both in plates and broth. Clear halo zones were observed around the colonies of isolates that showed P solubilization. All isolates positive for P solubilization in plate assay also exhibited P solubilization. A significant decline in pH of the culture medium was observed during phosphate solubilization. HPLC analysis detected seven different kinds of organic acids, namely, citric acid, formic acid, fumaric acid, succinic acid, malic acid, propionic acid, and tartaric acid from the cultures of these isolates. In addition, seven isolates could solubilize potassium. Seven isolates were able to produce IAA and zeatin, while only two isolates showed siderophore production. The isolates positive for two or more plant growth-promoting traits were further tested for seed germination assay using wheat as the test crop. Sixteen isolates that enhanced germination and seedling growth were evaluated in a greenhouse experiment, and eight archaea were selected that could improve the dry weight of root and shoot over uninoculated control in saline soils (ECe 6.2 dS m−1). A preliminary investigation suggests the role of archaea in supporting the growth of plants in saline soils. The potassium-solubilizing microbes (KSMs) solubilized the insoluble potassium (K) to soluble forms of K for plant growth and yield. K solubilization is carried out by a large number of bacteria (Bacillus mucilaginosus, Bacillus edaphicus, Bacillus circulans, Acidithiobacillus ferrooxidans, and Paenibacillus spp.) and fungal strains (Aspergillus spp. and Aspergillus terreus). Major amounts of K-containing minerals (muscovite, orthoclase, biotite, feldspar, illite, and mica) are present in the soil as a fixed form that is not directly taken up by the plant. The main mechanism of KSMs is acidolysis, chelation, exchange reactions, complexolysis, and production of organic acid. Soil microbes have been reported to play a key role in the natural K cycle, and therefore, potassium-solubilizing microorganisms present in the soil could provide an alternative technology to make potassium available for uptake by plants. Microbes require various nutrients for their growth and metabolism. Among the nutrients, zinc is an element present in the enzyme system as cofactor and metal activator of many enzymes. The role of zinc in the nutrition and physiology of both eukaryotic and prokaryotic organisms is widely studied, especially its importance for activity of many enzymes. Exogenous application of soluble zinc sources, similar to fertilizer application, has been advocated to various crops. This causes transformation of about 96%–99% of applied available zinc to various unavailable forms. The zinc thus made unavailable can be reverted back to available form by inoculating a bacterial strain capable of solubilizing it. Zinc is a nutrient at low concentration but toxic

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at higher concentration. Zinc solubilization by bacteria has an immense importance in zinc nutrition to plants. K-solubilizing bacteria (KSB) were found to resolve potassium, silicon, and aluminum from insoluble minerals. BBDG were best characterized for K solubilization (Sheng et al., 2008; Verma et al., 2015b). The K-solubilizing bacteria may have use in the amelioration of K-deficient soil in agriculture. There are only few reports on K solubilization by endophytic bacteria isolated from wheat (Verma et al., 2014a, 2015a, 2016a). Verma et al. (2016a) have reported 395 bacilli from wheat, and these bacteria have been screened for direct and indirect PGP traits, and results have been represented by 55 representative bacilli. Of 55 representatives, 39, 18, and 40 strains exhibited solubilization of phosphorus, potassium, and zinc, respectively. Among P, K, and Zn solubilizers, Paenibacillus polymyxa BNW6 solubilized highest amount of phosphorus (95.6 ± 1.0 mg L−1) followed by Sporosarcina sp. BNW4 (75.6 ± 1.0 mg L−1). Planococcus salinarum BSH13 (46.9 ± 1.2 mg L−1) and Bacillus pumilus BCZ15 (7.5 ± 0.5 mg L−1) solubilized highest amount of potassium and zinc, respectively. Among plant growth-promoting activities, ammonia-producing bacilli were highest (79.0%), when compared with P solubilizer (73.9%), Zn solubilizers (67.1%), protease producers (56.7%), IAA producers (55.2%), siderophore producers (49.1%), biocontrol activity (47.8%), K solubilizers (39.2%), N2 fixers (31.4%), HCN producers (27.3%), and gibberellic acid producers (24.8%).

4.3 Biological N2-Fixation Nitrogen is the major limiting factor for plant growth; the application of N2-fixing microbes as biofertilizer has emerged as one of the most efficient and environmentally sustainable methods for increasing the growth and yield of crop plants. Biological nitrogen fixation (BNF) is one of the possible biological alternatives to N fertilizers and could lead to more productive and sustainable agriculture without harming the environment. Many associative and endophytic bacteria are now known to fix atmospheric nitrogen and supply it to the associated host plants. A variety of nitrogen-fixing microbes like Arthrobacter, Azoarcus, Azospirillum, Azotobacter, Bacillus, Enterobacter, Gluconacetobacter, Herbaspirillum, Klebsiella, Pseudomonas, and Serratia have been isolated from the rhizosphere of various crops, which contribute fixed nitrogen to the associated plants (Suman et al., 2016b; Giller, 2001; Elbeltagy et al., 2001; Boddey et al., 2003; Wei et al., 2014; Reis and Teixeira, 2015). In recent years, application of microbial inoculants supplying N requirement efficiently to the various host plants including cereal crops has drawn attention for increasing plant yield in sustainable manner. The concept of BNF by endophytes (Dobereiner, 1992) has led to investigations on the potential uses of endophytic nitrogen-fixing bacteria that colonize graminaceous plants. Burkholderia, Herbaspirillum, Azospirillum, and Rhizobium leguminosarum bv. Trifolii are contributor of endophytic BNF in rice (Govindarajan et al., 2008; Biswas et al., 2000; Baldani and Baldani, 2005; Isawa et al., 2009; Doty, 2011; Estrada et al., 2013; Choudhury et al., 2014; Aon et al., 2015; Yadav et al., 2017d). Choudhury and Kennedy (2004) reported that that the Azolla and cyanobacteria can supplement the nitrogen requirements of plants, replacing 30%–50% of the required urea-N in rice production. BNF by Azotobacter, Clostridium, Azospirillum, Herbaspirillum, and Burkholderia can substitute for urea-N, while Rhizobium can promote the growth physiology or improve the root morphology of the rice plant. Green manure crops can also fix substantial amounts of


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atmospheric N. Among the green manure crops, Sesbania rostrata has the highest atmospheric N2-fixing potential, and it has the potential to completely substitute for urea-N in rice cultivation. Pham et al. (2017) have isolated from rice rhizosphere and endosphere, nitrogen-fixing Pseudomonas stutzeri A15, unequivocal evidence of the plant growth-promoting effect, and the potential contribution of biological nitrogen fixation. The use of plant growth-promoting rhizobacteria as a sustainable alternative for chemical nitrogen fertilizers has been explored for many economically important crops. Pseudomonas stutzeri A15 induced significant growth promotion compared with uninoculated rice seedlings. Furthermore, inoculation with strain A15 performed significantly better than chemical nitrogen fertilization, clearly pointing to the potential of this bacterium as biofertilizer.

4.4 ACC-Deaminase Activity Ethylene is a stress-induced plant hormone that can inhibit plant growth. Some microbes can lower the level of ethylene in the plant by cleaving the plant-produced ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC). Inoculation of such microbes can mitigate the effect of various stressors by sustaining plant growth in the face of ethylene. ACC-deaminase-producing microbes may play a role in regulating ethylene levels after such bursts, ensuring that ethylene levels stay below the point where growth is impaired (Glick, 1995). Ethylene is a key regulator of the colonization of plant tissue by bacteria that in turn suggests that the ethylene inhibiting effects of ACC deaminase may be a microbial colonization strategy. Generally, ethylene is an essential metabolite for the normal growth and development of plants (Khalid et al., 2004, 2006). This plant growth hormone is produced endogenously by approximately all plants and is also produced by different biotic and abiotic processes in soils and is important in inducing multifarious physiological changes in plants. Apart from being a plant growth regulator, ethylene has also been established as a stress hormone. Under stress conditions like those generated by salinity, drought, waterlogging, heavy metals, and pathogenicity, the endogenous level of ethylene is significantly increased that negatively affects the overall plant growth. PGP microbes that possess the enzyme, ACC deaminase, facilitate plant growth and development by decreasing ethylene levels, inducing salt tolerance, and reducing drought stress in plants (Kour et al., 2017b; Verma et al., 2017b; Yadav and Saxena, 2018). Microbial strains exhibiting ACC deaminase activity have been identified in a wide range of genera such as Acinetobacter, Achromobacter, Agrobacterium, Alcaligenes, Azospirillum, Bacillus, Burkholderia, Enterobacter, Pseudomonas, Ralstonia, Serratia, and Rhizobium (Verma et al., 2015a, 2016a; Khalid et al., 2006; Xu et al., 2014; Srivastava et al., 2014). Verma et al. (2014a, 2015a) reported psychrotolerant and drought-tolerant microbes from wheat showing ACC deaminase activity by different genera of Arthrobacter, Flavobacterium, Bacillus, Methylobacterium, Providencia, Pseudomonas, Stenotrophomonas, and Enterobacter. These bacteria also possess solubilization of phosphorus, potassium, and zinc; produced IAA, siderophore, HCN, and ammonia; and showed antifungal activity against plant pathogens.

4.5 Biocontrol The indirect mechanism of plant growth occurs when bacteria lessen or prevent the detrimental effects of pathogens on plants by production of inhibitory substances or by increasing the natural resistance of the host. Phytopathogenic microbes can control by releasing siderophores,

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chitinases, antibiotics, and fluorescent pigment or by cyanide production. Biocontrol systems are eco-friendly and cost-efficient and involved in improving the soil consistency and maintenance of natural soil flora. To act efficiently, the biocontrol agent should remain active under large range of conditions, namely, varying pH, temperature, and concentrations of different ions. Biocontrol agents limit the growth of pathogen and few nematodes and insects (Verma et al., 2017a). Biocontrol microbes can limit pathogens directly by producing antagonistic substances, competition for iron, detoxification, or degradation of virulence factors or indirectly by inducing systemic resistance (ISR) in plants against certain diseases; signal interference; competition for nutrients and niches; and interference with activity, survival, germination, and sporulation of the pathogen. Recent studies have indicated that biological control of bacterial wilt disease could be achieved using antagonistic bacteria. Different bacterial species, namely, Alcaligenes, Bacillus, Clavibacter, Curtobacterium, Flavobacterium, Kluyvera, Microbacterium, and Pseudomonas, have been reported as inhibitory to plant pathogens (Verma et al., 2015a,c; Inderiati and Franco, 2008; Ramesh et al., 2009; Nagendran et al., 2013; Gholami et al., 2014; Purnawati, 2014). Iron is a necessary cofactor for many enzymatic reactions and is an essential nutrient for virtually all organisms. In aerobic conditions, iron exists predominantly in its ferric state (Fe3+) and reacts to form highly insoluble hydroxides and oxyhydroxides that are largely unavailable to plants and microorganisms. To acquire sufficient iron, siderophores produced by bacteria can bind Fe3+ with a high affinity to solubilize this metal for its efficient uptake. Bacterial siderophores are low-molecular-weight compounds with high Fe3+ chelating affinities responsible for the solubilization and transport of this element into bacterial cells. Some bacteria produce hydroxamate-type siderophores, and others produce catecholate-type siderophores. In a state of iron limitation, the siderophore-producing microorganisms are also able to bind and transport the iron-siderophore complex by the expression of specific proteins. The production of siderophores by microorganisms is beneficial to plants because it can inhibit the growth of plant pathogens. Siderophores have been implicated for both direct and indirect enhancement of plant growth by plant growth-promoting microbes.

5 CONCLUSION AND FUTURE SCOPE The need of today's world is high output yield and enhanced production of the crop and fertility of soil to get in an eco-friendly manner. Hence, the research has to be focused on the new concept of microbial (endophytic, epiphytic, and rhizospheric) engineering based on favorable partitioning of the exotic biomolecules, which create a unique setting for the interaction between plant and microbes. Future research in microbes will rely on the development of molecular and biotechnological approaches to increase our knowledge of microbes and to achieve an integrated management of microbial populations of endophytic, epiphytic, and rhizospheric microbes. In the course of the past few decades, the human population has doubled. Food production has similarly increased. Use of man-made fertilizers has enabled much of the increase in the crop production. Concurrent with the escalating use of commercial fertilizers, the intensity of agricultural practices has increased, and a wide variety of fungicides, bactericides, and pesticides are utilized in large-scale crop production. Because of their close interaction with plants, attention has been focused on microbes and their potential use in sustainable agriculture.

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