Cronicon · Priyanka Verma1,2* and Archna Suman2 Among cereal crops, wheat (Triticum aestivum L.) is the most important cereal crop which is contributes almost one-third to the total

CroniconO P E N A C C E S S EC MICROBIOLOGY

Review Article

Wheat Microbiomes: Ecological Significances, Molecular Diversity and Potential Bioresources for Sustainable Agriculture

1Department of Microbiology, Akal College of Basic Science, Eternal University, Sirmour, India2Division of Microbiology, Indian Agricultural Research Institute, New Delhi, India

*Corresponding Author: Priyanka Verma, Department of Microbiology Akal College of Basic Science Eternal University, Sirmour, India.

Citation: Priyanka Verma and Archna Suman. “Wheat Microbiomes: Ecological Significances, Molecular Diversity and Potential Biore-sources for Sustainable Agriculture”. EC Microbiology 14.9 (2018): 641-665.

Received: April 25, 2018; Published: August 31, 2018

Abstract

Keywords: Agro-ecological Zones; Biodiversity; Biofertilizers; Bioresources; Microbiomes; Plant Growth Promotion; Wheat

Priyanka Verma1,2* and Archna Suman2

Among cereal crops, wheat (Triticum aestivum L.) is the most important cereal crop which is contributes almost one-third to the total food grain in world. Wheat cultivation in world differs considerably with respect to harsh environments (temperatures, pH, salinity and drought) and distinct geographic distribution of soil types. There are six mega environmental agro-ecological zones in India on the basis of climatic conditions. Diverse agro-ecological zones represent a unique ecosystem and may have novel microbiomes such as acidophiles, alkaliphiles, halophiles, psychrophiles, thermophiles and xerophiles. Microbes grow across a broad range of temperature, pH, salinity, water deficient and oxygen and play an indispensable role in maintaining the biosphere and improving plant growth for sustainable agriculture. The wheat microbiomes can be source of novel biomolecules, genes and alleles. Wheat microbiome mainly belongs to different phyla namely Actinobacteria, Bacteroidetes, Firmicutes, Gemmatimonadetes and Proteobacteria. Wheat microbiomes (phyllospheric, endophytic and rhizospheric) such as Azotobacter, Achromobacter, Alcaligenes, Azospirillum, Enterobacter, Herbaspirillum, Methanospirillum, Klebsiella, Pantoea, Burkholderia, Bacillus, Paenibacillus, Lysinibacillus, Methylobacterium, Pseudomonas, Rhodosporidium, Serratia, Staphylococcus, Penicillium, Streptomyces and Thermomonospora have been isolated and characterized for plant growth promotion (PGP) under the diverse harsh environments. The microbiomes of wheat play important role in plant growth, soil health and fertility as well as in amelioration of diverse abiotic stresses by directly, e.g. via N2-fixation, production of siderophore, phytohormones (auxin, cytokinin and gibberellins) and solubilization of potassium, phosphorus and zinc or indirectly via production of ammonia, hydrogen cyanide, iron chelating compounds, hydrolytic enzymes, antibiotics and antagonistic molecules for suppression of soil borne pathogens. The ecological significances, molecular diversity, PGP attributes of wheat microbiomes and its potential roles in mitigation of different abiotic stress in plants have been discussed in present review. This is first critical review on microbiomes of wheat and its potential role in crop improvements under the diverse harsh environments.

IntroductionAmong cereal crops, wheat (Triticum aestivum L.) is contributing more than 45% of digestible energy and 30% of total protein in hu-

man diet, as well as a substantial contribution to feeding livestock. Wheat shares 35.5% of total food grain production, next to rice. The annual demand of wheat in developed countries is 3%, on the basis of survey and reports but the yield increase is less than 1% annually. Wheat is the main staple food of Asia and major staple cereal crop for more than 1/3rd total population in world. Wheat cultivation in world differs considerably with respect to harsh environments (temperatures, pH, salinity and drought) and distinct geographic distri-

642



bution of soil types. During last two decades the production of wheat increased due to use of high yielding phytopathogenic resistance dwarf varieties and India ranked 2nd in production of wheat (12.05%). Wheat cultivation in India differs considerably in respect to harsh environmental conditions (pH, salinity, high temperatures, low temperatures and water deficient) and diverse types of soils. On the basis of climatic conditions, there are six mega agro-ecological climatic zones in India e.g. Low temperature conditions (Northern hills zone), acidic soil (Southern hills zone), alkaline soil (North eastern plain zone and North western plain zone), drought and heat stress conditions (Central zone), and high temperature condition (Peninsular zone).

Among six zone, two zone namely North eastern and North western plain zones are optimally irrigated, fertilized yielding maximum (85%), whereas Central zone is low yielding (10%) due to high temperature and less water availability [1]. Grain yield per hectare (ha) has not significantly increased in last 10 years while we should have 93 Mt/year required by 2020. Northern hills zone is predominantly rain fed wheat growing area of 0.8 mha with 16.64 q ha-1 average wheat production. North western plain zone with 9.5 mha with 39.4 q ha-1 average wheat production and this zone is impaction with weed infestation particularly Phalaris minor, yellow and brown rusts. Central zone has half area of wheat cultivation in comparison of North western plain zone and average wheat productivity of 24.1 q ha-

1. This zone has major constraints are leaf and stem rust, termites and prevalent rainfed conditions. From the Peninsular zone, average wheat productivity of 29.8 q ha-1 in 1.5 mha of wheat growing area. The major constraints are leaf and brown rust, attack of aphids and heat stress. Southern hills zone having major constraints are termites, black rust and low pH stress. This zone has lowest average wheat production of 10 q ha-1 in wheat cultivation area of 0.2 mha [1].

The development of the predictive understanding between soil biology, agronomy and crop performance could be an important step to achieve high yields and it will also affect global production. Further, plants microbiomes have received a global attention in this context to achieve plant growth, high yields, soil health and soil fertility. These PGP microbes can either be associated to roots (rhizospheric) present inside tissues (endophytic) and on the surface of phyllosphere (epiphytic) [2] The microbiomes of plants play important role in PGP and amelioration of different abiotic stresses by various direct or indirect mechanisms. The plant microbiomes (phyllospheric, en-dophytic and rhizospheric) have been shown to promote plant growth directly, e.g. via N2-fixation, production of siderophore, phytohor-mones (auxin, cytokinin and gibberellins) and solubilization of potassium, phosphorus and zinc or indirectly via production of ammonia, hydrogen cyanide, iron chelating compounds, hydrolytic enzymes, antibiotics and antagonistic molecules for suppression of soil borne pathogens [3-6]. The Plant microbiomes with multifarious PGP attributes could be used as bio-inoculations or biofertilizers for sustain-able agricultural system.

The epiphytic microbes present on phyllosphere, which is a common niche for extremophilic microbes. The microbes on phyllosphere can categorize as thermophilic microbes as they can tolerate high temperatures and UV radiation. The plant part, leaves, stems and other areal parts of plants are exposed air and dust which results the attachments of typical and novel microbes on surface due to secretion of waxes and cuticles and which finally help in the waterfront of phyllospheric microbiomes. The phyllospheric microbiomes may survive or proliferates on leaves depending on extent of influences of material in leaf diffusates or exudates. The leaf diffusates contains the principal nutrients factors (amino acids, glucose, fructose and sucrose), and such specialized habitats may provide niche for nitrogen fixation and secretions of substances capable of promoting the growth of plants. Many microbes such as Achromobacter, Agrobacterium, Alcaligenes, Arthrobacter, Azotobacter, Bacillus, Brevundimonas, Corynebacterium, Enterobacter, Haemophilus, Lysinibacillus, Methylobacterium, Micro-coccus, Micromomospora, Paenibacillus, Pantoea, Pseudomonas, Psychrobacter, Stenotrophomonas and Streptomyces have been reported in the phyllosphere of wheat [3,4,7-13].

The microbiomes of interior of the plant parts (root, stem or seeds) are referred as endophytes and these microbes may be does not causing advised effect of plant part where they are present. Endophytic microbiomes (in the plant) enter in host plants through wounds and root hairs. The plant tissue may be penetrating by soil microbiomes by producing extracellular hydrolytic enzymes (pectinase and cellulase). Endophytic microbiomes transmitted from parent to offspring or among individuals. Endophytic microbiomes of host plants

643



can be modified by phase of plant growth, plant physiological state and different environmental factor. Endophytic microbiome belongs to phylum Actinobacteria, Acidobacteria, Ascomycota, Bacteroidetes, Basidiomycota, Deinococcus-Thermus Euryarchaeota, Firmicutes and Proteobacteria have been reported from different cereal, leguminous, non-leguminous crops, woody and medicinal plant such as bean, citrus, chilli, cotton, chickpea, maize, mustard, pea, potato, pearl millet, rice, sugarcane, soybean, sunflower strawberry, and tomato [14]. There are many such reports on endophytic microbiomes from wheat and microbes belong to different genera such as Achromobacter, Bacillus, Burkholderia,Micromomospora, Microbiospora, Nocardioides, Planomonospora, Pseudomonas, Pantoea, Piriformospora, Strepto-myces and Thermomonospora [4,7,15-17].

The microbiomes in rhizosphere are most dominant in nature, which have been attracted by plant by releasing of different types of substrates by root exudates. Rhizospheric zone is characterized as hot spot of microbial diversity than other microbiomes as phyllo-spheric and endophytic. The rhizospheric microbiomes plays important role in plant growth and nutrient uptake because these microbes are closed attached between roots and soils. Among plant microbiomes, the rhizospheric microbes have been more affected from several factors e.g. soil moisture, soil types, pH and micronutrients present in soil. In comparison among epiphytic, endophytic and rhizospheric microbiomes of plants, the microbiomes in rhizosphere are most dominant and belong to different genera namely: Acidobacteria, Actino-bacteria, Aquificae, Armatimonadetes, Bacteroidetes, Caldiserica, Chlamydiae, Chlorobi, Chloroflexi, Chrysiogenetes, Cyanobacteria, Defer-ribacteres, Deinococcus–Thermus, Dictyoglomi, Elusimicrobia, Fibrobacteres, Firmicutes, Fusobacteria, Gemmatimonadetes, Lentisphaerae, Nitrospirae, Planctomycetes, Proteobacteria, Spirochaetes, Synergistetes, Tenericutes, Thermodesulfobacteria, Thermomicrobia, Thermoto-gae and Verrucomicrobia in which three phyla Actinobacteria, Firmicutes and Proteobacteria have been well characterized and reported as rhizospheric microbiomes. The rhizospheric microbiomes have been well characterized and reported from all study plants. The wheat rhizospheric microbiomes belong to different genera such Arthrobacter, Azospirillum, Alcaligenes, Acinetobacter, Bacillus, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Lysinibacillus, Methylobacterium, Paenibacillus, Pseudomonas, Rhizobium and Serratia [3,4,10-13,18-20].

The use of PGP microbiome facilitates wheat growth and as eco-friendly and have no adverse effects on soil and agro-ecosystems. The use of microbiomes of multifarious PGP attributes as biofertilizers for sustainable agriculture increased worldwide [8,21-24]. There are many reports on growth and yield of several crops by used to different PGP microbes [4,7,9,11,13-15,17,25-48]. Application of bio-inoculants containing microbes with multifunctional PGP attributes may be a suitable alternative for reduction of the chemical fertilizers inputs as well as to enhance the productivity and soil fertility. Therefore, isolation, screening, characterization, identification and selection of effective microbes with multifarious PGP attributes and their eco-friendly application as bio-inoculants/biofertilizers is of great impor-tance for enhancing the growth, yield, adaptation and soil health for maintaining sustainability of agro-ecosystems. The present review revealed about biodiversity of wheat microbiomes and its ecological significances and potential bioresources in crops improvements for sustainable agriculture.

Wheat Cultivation

Wheat cultivation in India started 5000 years ago. Today, India ranks second in wheat production with a harvest of 95.38 million ton during the season 2013 - 2014 (http://www.icar.org.in/en/node/7665). Breeding programs are traditionally empirical, that is selection is generally based on yield only which has limitations under stressful environment. To meet the increasing demand of wheat production without increasing area, there is need to incorporate new physiological tools, which will help for the improvement of breeding program under abiotic stress environment. If specific physiological trait associated with yield could be identified under stress environment, selec-tion efficiency could be increased. Among different staple food crops, wheat is most important and grown over 200 mha worldwide and cultivated in diverse environmental conditions. It is a valued grain in the subcontinent Asia. Due to increasing populations, the agriculture sector is expected to move towards environmentally sustainable development for future generations. To counteract the dark side of heavy input of chemical fertilizers and pesticides, plateauing crop productivity, the global interest should be shifted towards microbiomes with multifarious PGP attributes from natural agro ecosystems contributing to plant growth, productivity and soil fertility.

644



On the basis of agro climatic conditions wheat cultivation in India has been divided into six mega environmental agro-ecological zones (Figure 1). Wheat is grown in all the states in India except southern and north eastern states. Uttar Pradesh, Haryana, Punjab, Rajasthan are the major wheat producing states accounting for almost 80% of total production in India. Major rain fed wheat areas are in Madhya Pradesh, Gujarat, Maharashtra, West Bengal and Karnataka. Only 1/3 of wheat growing region in India receives desired irrigation, while the remaining area has limited irrigation availability (http://agropedia.iitk.ac.in/content/cultivation-wheat). Breeding programmers are generally aimed for rain fed and irrigated environments and there is need to develop varieties which are responsive to limited irrigation conditions [49]. Thus, to increase the productivity of region receiving limited irrigation, different physiological techniques which should be adopted for tolerant to water and heat stress [50].

Figure 1: Wheat production worldwide and six diverse agro-ecological zones in India.

Isolation, enumeration and molecular characterization of wheat microbiomes

Wheat microbiomes are being largely influenced by the environmental conditions temperature, pH, nutrient contains in soil, salinity and water contain in soil. To know the diversity and distribution among different groups of microbes associated with wheat crops (epi-phytic, endophytic and rhizospheric microbes). Wheat associated microbes may be characterized using culturable and un-culturable tech-niques. The endophytic and rhizospheric microbes associated with wheat could be isolated using surface sterilization, serial dilution and

645



spread/pour plate techniques [16,51]. The epiphytic microbes should be isolated using standard method of imprinting as well as using serial dilution method followed by spread or pour plate methods. For isolation of different groups of microbes (archaea, eubacteria and fungi), different specific and selective medium would be used e.g. Heterotrophic microbes (nutrient agar); Pseudomonads (King’s B agar), Arthrobacter (trypticase soy agar); soil-specific microbes (soil extract agar), Bacillus and Bacillus derived genera (T3A with heat treat-ment methods); archaea (chemically defined and complex medium); fungi (rose Bengal and potato dextrose agar) (Table 1 and Figure 2).

Media and composition per literRhizospheric microbes

1. Nutrient agar (NA): 5 g peptone; 5 g NaCl; 3 g beef extract; 18 g agar; pH-3-6 ±0.22. T3 agar: 3 g tryptone; 2 g tryptose; 1.5 g yeast extract; 0.005 g MnCl2; 0.05 g sodium phosphate; 18 g agar; pH-3-6±0.2.3. Soil extract agar (SEA): 2 g glucose; 1 g yeast extract; 0.5 g K2HPO4; 100 mL soil extract (250 g soil from sampling site + 1L H2O;

autoclave and filter); 18 g agar; pH-3-6±0.2.4. Tryptic soy agar (TSA): 17 g tryptone; 3 g soya meal; 2.5 g dextrose; 5 g NaCl; 2.5 g K2HPO4; 18 g agar; pH-3-6±0.2.5. King’s B agar (KB): 20 g protease peptone; 1.5 g K2HPO4; 1.5 g MgSO4.7H2O; 10 mL glycerol; 18 g agar; pH 3-6±0.2.6. Jensen’s agar (JA): 20 g sucrose; 1 g K2HPO4; 0.5 g Mg2SO4; 0.5 g NaCl; 0.001 g Na2MoO4; 0.01 g FeSO4; 2 g CaCO3; 18 g agar; pH

3-6±0.27. R2A agar: 0.5 g protease peptone; 0.5 g casamino acids; 0.5 g yeast extract; 0.5 g dextrose; 0.5 g

8. soluble starch; 0.3 g dipotassium phosphate; 0.05 g magnesium sulphate 7H2O; 0.3 g sodium pyruvate; agar 20 g agar; pH 3-6±0.2.9. Nutrient agar10. Tryptic soy agar11. King’s B agar12. Ammonium minerals salt (AMS) medium: 0.70 g K2HPO4; 0.54 g KH2PO4; 1.00 g MgSO47H2O; 0.20 g CaCl2.2H2O; 4.00 mg

FeSO4.7H2O; 0.50 g NH4Cl; 100 µg ZnSO4.7H2O; 30 µg MnCl2.4H2O; 300 µg H3BO3; 10 µg CuCl2.2H2O; 200 µg CoCl2.6H2O; 20 µg NiCl2 .6H2O; 60 µg Na2MoO4.2H2O; 18 g agar; pH-3-6±0.2.

Endophytic microbes13. Luria Bertani medium (LB): 10 g casein acid hydralysate; 5 g yeast extract; 10 g NaCl; 18 g agar; pH-3-6±0.214. Modified Dobereiner medium (MDM): 10 g sucrose; 5 g malic acid; 0.2 g K2HPO4.H2O; 0.4 g KH2PO4.H2O; 0.1 g NaCl; 0.01 g FeCl3;

0.002 g Na2MoO4; 0.2 g MgSO4.7H2O; 0.02 g CaCl2.H2O; 18 g agar; pH 3-6±0.2.15. Yeast extract mannitol agar (YEMA): 1 g yeast extract; 10 g mannitol 0.5 g K2HPO4.H2O; 0.002 g MgSO4.7H2O; 0.1 g NaCl; 18 g

agar; pH 3-6±0.2.

Table 1: The different growth media used for isolation and enumeration of microbiomes of wheat.

Figure 2: A schematic representation of the isolation, identification of microbes of wheat (Triticum aestivum L).

646



The isolated microbiomes from wheat may be screened for different abiotic stresses of temperatures, pH, drought and salinity using method described by Yadav Verma., et al [51].

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. For characterization of un-culturable microbes, metagenomic DNA should be isolated using Zymo Research metagenomic Fungal/Bacterial DNA MicroPrep™ following the standard protocol prescribed by the manufacturer. 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 metagenomics library have been given in figure 2. The isolated DNA is called metagenome. This metagenome can be either used directly for sequencing (using specific primer of archaea/bacterial/fungi). The simplified diagrammatic scheme has been presented in figure 2 to show steps of isolation and identification of culturable and un-culturable microbes. After sequencing the sequences should be compared with sequences available in the NCBI database. The phylogenetic tree can be constructed on aligned data sets using the Maximum Likehood method and the program MEGA 4.0.2 to know the taxonomical affiliations of all microbes [52,53] (Figure 3).

Biodiversity of wheat microbiomes

Microbial biodiversity includes the diversity of different groups of microbes such as archaea bacteria, fungi, cyanobacteria and protozoa. Microbes are ubiquitous in nature and have been reported from extreme environments and associated with all living species. The plant microbiomes included epiphytic, endophytic and rhizospheric microbes which are associated with plant and helps in growth and also adaptation in harsh environments. Scientists have reported more than 1.7 million living species on our planet, only 1 - 10% bacterial species among 5000 identified species of prokaryotes. Overall it said be that there is small idea about true diversity of all living microbiomes [54,55]. The microbiomes provide huge reservoirs of bioresources which can be used in agriculture, industry and medical processes. The plant microbiomes are essential to a sustainable biosphere as it plays important roles in plant growth, productivity and soil health.

Biodiversity is an important constituent of environmental conservation and is central to agriculture production. The culturable microbiomes are only small fraction of the soil microbiomes. Hence there are other techniques to study the biodiversity such as phospholipid fatty acids analysis- enables to estimate the structure of the living microbial community; Whole soil fatty acid methyl ester analysis- enables to examine the microbial community structure by assessing the lipid components from live and dead microorganisms and Cloning and sequencing of the bacterial 16S ribosomal DNA can allow to assess the bacterial diversity in the soil with a high degree of discrimination. Molecular finger printing techniques have been developed to permit the simultaneous analysis of numerous samples. Among these techniques, denaturing gradient gel electrophoresis (DGGE) analysis of the 16S rDNA gene permits finger printing of the dominant bacteria. The DGGE patterns represent the relative abundance of the detectable bacterial populations and can release to the biological structure of the bacterial community.

There are three types of RNAs found in the microbial ribosome’s, 5S rRNA, 16S rRNA and 23S rRNA. The first attempt to characterize microbes by studying rRNA began by extracting the 5S rRNA molecules directly from the cells. However, the information content in approximately 120 bp long molecule is relatively small and was abandoned to the benefit of the 1,500 bp long 16S rRNA gene and to a lesser extent to the 3,000 bp long 23S rRNA. The 16S rRNA molecule has several advantages. Some regions of the gene are universally conserved and suitable for phylogenetic studies of distantly related organisms. Other regions are semi-conserved and more useful for the analysis of phylogenetic relationship between phyla and families; variable and hyper-variable regions in the 16S rRNA gene enable to discriminate between organisms belonging to the same genus or even between species, although not between strain within the same species [56]. The length of the gene is convenient, so PCR and sequencing are easy. Furthermore, the ends of the gene are highly conserved

647



across all bacterial and archaeal domains; therefore, almost the entire gene can be amplified by PCR [57], have compared bacteria using on other hand the classical phenotypic characterization including morphological studies, Gram staining, enzyme activities, utilization of different organic substrates such as carbon and energy sources as well as molecular analyses. It has been found that the phylogenetic analysis of small subunit rRNA gene sequences is more efficient for the identification of microbial strains because misidentification of microbes is less with the molecular methods. Application of genotypic and molecular analysis has advanced microbial identification and it has led to the discovery of a number of possibly new species [58].

Microbial diversity can be defined in terms of functional and genetic diversity. On the basis of different reports, wheat microbiome mainly belongs to different phyla namely Actinobacteria, Bacteroidetes, Firmicutes, Proteobacteria etc. (Figure 3 and 4) [3,7,9,11-17,25-48]. In general, there are three kinds of plant-microbe-interactions are considered i.e. epiphytic, endophytic and rhizospheric. On the basis of different reports on microbes interaction with wheat plants, it was found that there are some common and niche-specific microbes from epiphytic, endophytic and rhizospheric communities such as Arthrobacter nicotianae, Bacillus amyloliquefaciens, Bacillus megaterium, Bacillus sphaericus, Bacillus subtilis, Micrococcus luteus, Paenibacillus amylolyticus, Paenibacillus polymyxa, Pseudomonas aeruginosa, Pseudomonas azotoformans, Pseudomonas chlororaphis, Pseudomonas fluorescens, Pseudomonas rhodesiae and Stenotrophomonas maltophilia were common and most pre-dominant species reported from phyllosphere, internal tissues and rhizosphere; along with common and pre-dominants species of different genera, many niche-specific species have been reported e.g. Alcaligenes faecalis, Arthrobacter methylotrophus, Brevundimonas diminuta, Corynebacterium callunae, Enterobacter aerogenes, Methylobacterium phyllosphaerae, Microbacterium phyllosphaerae, Pseudomonas fuscovaginae, Pseudomonas geniculata, Pseudomonas mosselii and Pseudomonas plecoglossicida as epiphytic; Achromobacter piechaudii, Achromobacter xylosoxidans, Acinetobacter lwoffii, Delftia acidovorans, Delftia lacustris, Ochrobactrum intermedium, Pantoea dispersa, Pantoea eucalypti, Pseudomonas monteilii, Staphylococcus epidermidis and Variovorax soli as endophytic and Arthrobacter nicotinovorans,Azotobacter tropicalis, Bacillus atrophaeus, Bacillus horikoshii, Bacillus mojavensis, Bacillus siamensis, Bacillus thuringiensis, Enterobacter asburiae, Exiguobacterium acetylicum, Gluconacetobacter xylinus, Klebsiella oxytoca, Kocuria kristinae, Lysinibacillus fusiformis, Paenibacillus alvei, Pantoea ananatis, Planococcus rifietoensis, Planomicrobium okeanokoites, Pseudomonas extremorientalis, Pseudomonas rhizosphaerae, Rhodobacter capsulatus, Rhodobacter sphaeroides and Serratia marcescens as rhizospheric microbes. Microbes reported as common niches as well as niche specific, there are some microbes reported from one or more common host [3,7,9,11-17,25-48] (Figure 5). Venn diagram represented the common as well as niche–specific site for survival and growth (Figure 6) [3,7,9,11-17,25-48].

Figure 3: Abundance of wheat microbiomes belonging diverse phylum and groups.

648



Figure 4: Phylogenetic tree showed the relationship among different groups of microorganisms associated with wheat (Triticum aestivum L).

649



Figure 5: Relative distribution among different microbes isolated from phyllosphere, endophytic and rhizospheric sample of wheat (Triticum aestivum L.). [3,7,9,11-17,25-48].

650



Figure 6: Venn diagram showing niche-specific microbes reported from wheat (Triticum aestivum L).

Mechanisms of plant growth promotion

Plant growth promoting endophytic, epiphytic and rhizospheric microbes are associated with plant and stimulates plant growth directly or indirectly. Microbes hold different types of mechanisms to stimulate plants growth direct by the fixed atmospheric nitrogen, iron that has been sequestered by microbial siderophores, synthesizing phytohormones including auxins, cytokinins and gibberellins; solubilizing minerals such as phosphorous and synthesizing different enzymes. Indirect stimulation of plant growth includes preventing phytopathogens (biocontrol) through production of antibiotics, siderophores and hydrogen cyanide. Among rhizospheric microbes there is a gradient of root proximity and intimacy as follows: (i) microbes living in the soil near roots, utilizing metabolites leaked from roots as C and N sources, (ii) microbes colonizing the rhizoplane (root surface), microbes residing in root tissue, inhabiting spaces between cortical cells and lastly (iv) microbes living inside cells in specialized root structures, or nodules. These are discussed in order of intimacy with the associated plant, from almost casual, to extremely regulated and housed in specialized structures. Within this classification, various mechanisms of plant growth promoting effects have been established; with the greatest understanding being of the rhizobia legume symbiosis (Table 2). The application of PGP microbes is a promising agricultural approach that plays a vital role in crop protection, growth promotion or biological disease control and sustained soil fertility [16,19,59-62]. In the last decade, a number of PGP microbes associated

651



with wheat and different cereals crops have been identified including Acinetobacter, Arthrobacter, Azospirillum, Azotobacter, Bacillus, Burkholderia, Citricoccus, Kocuria, Lysinibacillus, Methylobacterium, Paenibacillus, Providencia, Pseudomonas and Serratia [13,18,63-65]. The rhizosphere can be defined as any volume of soil specifically influenced by plant roots and/or in association with roots and hairs. This space includes soil bound by plant roots, often extending a few mm from the root surface. Plant exudates in the rhizosphere, such as amino acids, fatty acids, nucleotides, organic acids, phenolics, plant growth regulators, putrescine, sterols, sugars, and vitamins, provide a rich source of energy and nutrients for bacteria, resulting in bacterial populations greater in this area than outside the rhizosphere. Most rhizosphere organisms occur within 50 mm of root surface and populations within 10 mm of root surface.

Abiotic Stress and PGP Microbes Response ReferenceCold stress

Arthrobacter methylotrophus IARI-HHS1-25 Growth, Alleviate cold [12]Arthrobacter sulfonivorans IARI-L-16 Growth and alleviation [47]

Azospirillum brasilense Sp245 Affected dry weight [46]Bacillus altitudinis IARI-HHS2-2 Growth and yield [13]

Bacillus amyloliquefaciens IARI-HHS2-30 Growth and alleviation [124]Bacillus aryabhattai BNH5 Growth, Alleviate cold [3,4]

Bacillus cereus AS4 Growth and yield [44]Bacillus megaterium AS15 Growth and yield [44]Bacillus megaterium AS8 Growth and yield [44]Bacillus megaterium M3 Affected dry weight [46]Bacillus muralis BNH12 Growth, Alleviate cold [3,4]Bacillus subtilis OSU142 Affected dry weight [46]

Bacillus thuringiensis BNH2 Growth, Alleviate cold [3,4]Bordetella bronchiseptica IARI-HHS2-29 Growth, Alleviate cold [12]

Cellulomonas turbata AS1 Growth and yield [44]Enterobacter cloacae AS6 Growth and yield [44]

Flavobacterium psychrophilum HHS2-37 Growth and yield [13]Kocuria kristinae IARI-HHS2-64 Growth, Alleviate cold [11]

Methylobacterium phyllosphaerae IARI-HHS2-67 Growth and yield [13]Mycobacterium phlei MbP18 Growth, root and shoot [33]

Mycobacterium sp. 44 higher N, P, and K contents [33]Mycoplana bullata MpB46 Growth, root and shoot [33]

Paenibacillus polymyxa BNH18 Growth, Alleviate cold [3,4]Pantoea agglomerans 050309 higher N, P, and K contents [33]

Pseudomonas extremorientalis IARI-HHS2-1 Growth, Alleviate cold [11]Pseudomonas fluorescens PPRs4 Alleviating cold stress [39]Pseudomonas fluorescens PsIA12 higher N, P, and K contents [33]

Pseudomonas jessani PGRs1 Alleviating cold stress [39]Pseudomonas koreensis PBRs7 Alleviating cold stress [39]

Pseudomonas lurida M2RH3 Growth and nutrient uptake [43]Pseudomonas lurida NPRs3 Alleviating cold stress [39]

Pseudomonas putida AS3 Growth and yield [44]Pseudomonas putida PGRs4 Alleviating cold stress [39]

Pseudomonas sp. NARs9 Germination, root lengths [119]Sporosarcina sp. BNH20 Growth, Alleviate cold [3,4]

Drought and heat stressAchromobacter spanius IARI-NIAW2-15 Growth, Alleviate high temp [11]Achromobacter spanius IARI-NIAW2-15 Growth, yield [4]

Alcaligenes faecalis IARI-NIAW1-6 Growth, Alleviate high temp [11]Azospirillum brasilense NO40 Improved homeostatic [36]

Azospirillum brasilense Sp245 Coleoptiles growth [27]Azospirillum brasilense Sp245 Grain yield, mineral quality [32]

Azospirillumlipoferum AZ1, AZ9, AZ45 Alleviate the drought stress [28]Bacillus alcalophilus BCZ14 Growth, yield, stress [3]

Bacillus altitudinis BPZ4 Growth, yield [3]Bacillus amyloliquefaciens 5113 Improved homeostatic [36]

Bacillus aryabhattai BCZ17 Growth, yield, stress [3]Bacillus licheniformis BPZ5 Growth, yield [3]

Bacillus mojavensis IARI-NIAW2-23 Growth, yield [4]Bacillus safensis W10 Plant growth and yield [31]

Bacillus tequilensis BCZ6 Growth, yield, stress [3]Burkholderia phytofirmans PsJN Growth and grain yield [40]

Delftia acidovorans IARI-NIAW1-20 Growth, yield [4]Delftia lacustris IARI-NIAW1-34 Growth, Alleviate high temp [11]

Duganella violaceusniger IARI-IIWP-23 Growth, Alleviate heat stress [11]Exiguobacterium acetylicum BPZ8 Growth, yield [3]

Glomus mosseae (AMF) Enhance its defence system [37]Kocuria sp. IARI-IHD-9 Growth, Alleviate heat stress [11]

Methylobacterium mesophilicum IARI-NIAW1-41 Growth, yield [4]Micrococcus sp. IARI-IIWP-20 Growth, Alleviate heat stress [11]

Ochrobactrum pseudogregnonense IP8 Plant growth and yield [31]Paenibacillus amylolyticus BPZ10 Growth, yield [3]Paenibacillus dendritiformis BCZ2 Growth, yield, stress [3]

Paenibacillus dendritiformis IARI-IIWP-4 Growth, Alleviate drought [11]Paenibacillus tundrae BCZ3 Growth, yield, stress [3]Piriformospora indica (Pi) drought resistance, growth [48]

Planococcus salinarum BCZ23 Growth, yield, stress [3]Pseudomonas poae IARI-NIAW2-1 Growth, Alleviate heat stress [11]Pseudomonas poae IARI-NIAW2-1 Growth, yield [4]

Pseudomonas putida AKMP7 Growth, Alleviate heat stress [26]Psychrobacter fozii IARI-IIWP-12 Growth, Alleviate heat stress [11]

Rhodobacter sphaeroides IARI-NIAW1-7 Growth, Alleviate heat stress [11]Rhodobacter sphaeroides IARI-NIAW1-7 Growth, yield [4]

Pantoea theicola NBRC 110557T Alleviate drought stress [102]Pantoea intestinalis DSM 28113T Alleviate drought stress [102]

Salinity stressAchromobacter xylosoxidans 249 Growth and SOD activity [30]Aeromonas hydrophila MAS-765 Alleviate salinity, growth [29]

Aeromonas vaga BAM-77 Growth and Yield [35]Arthrobacter nicotianae IARI-BHD-1 Growth and Alleviate salinity [11]

Bacillus amyloliquefaciens BNE12 Growth and Alleviate salinity [3]Bacillus insolitus MAS17 Alleviate salinity, growth [29]

Bacil lus l icheniformis HSW-16 Growth and Productivity [45]Bacillus methylotrophicus BNE2 Growth and Alleviate salinity [3]Bacillus sp. MAS617/620/820 Alleviate salinity, growth [29]

Brachybacterium nesterenkovii IARI-BHI-4 Growth and Alleviate salinity [11]Cellulosimicrobium cellulans IARI-BHI-13 Growth and Alleviate salinity [11]

Enterobacter sp. 12 Growth and SOD activity [30]Klebsiella sp. SBP-8 Plant growth and yield [41]

Microbacterium phyllosphaerae IARI-BHI-1 Growth and Alleviate salinity [11]Paenibacillus xylanexedens BNE18 Growth and Alleviate salinity [3]

Planomicrobium okeanokoites BNE8 Growth and Alleviate salinity [4]Planomicrobium okeanokoites IARI-BHI-16 Growth and Alleviate salinity [11]

Pseudomonas aurantiaca TSAU22 Growth and salinity tolerate [104]Pseudomonas chlororaphis TSAU13 Growth and salinity tolerate [104]

Pseudomonas extremorientalis TSAU20 Growth and salinity tolerate [104]Pseudomonas extremorientalis TSAU6 Growth and salinity tolerate [104]

Pseudomonas fluorescens 153 Salinity stress, growth [25]Pseudomonas putida 108 Salinity stress, growth [25]

Pseudomonas putida TSAU1 Growth and salinity tolerate [104]Pseudomonas sp. 33 Growth and SOD activity [30]

Serratia marcescens 73 Growth and SOD activity [30]Acidic and Alkalinity stress

Aeromonas vaga BAM-77 Growth and Yield [35]Bacillus aerophilus BSH15 Growth and Alleviate acidity [3]Bacillus altitudinis BNW15 Growth and Alleviate alkalinity [3]

Bacillus circulans BSH11 Growth and Alleviate acidity [3]Bacillus endophyticus BNW9 Growth and Alleviate alkalinity [3]

Bacillus nanhaiensis BSH7 Growth and Alleviate acidity [3]Bacillus nanhaiensis IARI-THD-20 Growth and alleviation [9]

Bacillus nealsonii IARI-THD-30 Growth and Yield [11]Bacillus rigui IARI-THD-6 Growth and alleviation [11]

Lysinibacillus fusiformis IARI-THD-4 Growth and Yield [9]Lysinibacillus sphaericus BNW22 Growth and Alleviate alkalinity [3]

Lysinibacillus sphaericus BSH6 Growth and Alleviate acidity [3]Micrococcus roseus SW1 Growth and Yield [34]

Paenibacillus lautus IARI-DV-77 Growth and alleviation [11]Paenibacillus xylanexedens BNW24 Growth and Alleviate alkalinity [3]

Planococcus salinarum BNW25 Growth and Alleviate alkalinity [3]Planococcus salinarum BSH13 Growth and Alleviate acidity [3]

Planomicrobium sp. BSH14 Growth and Alleviate acidity [3]Pseudomonas argentinensis IARI-DHD-5 Growth and alleviation [11]

Pseudomonas flavescens IARI-DHD-6 Growth and Yield [11]Pseudomonas plecoglossicida IARI-DV-5 Growth and alleviation [11]Pseudomonas rhizosphaerae IARI-DV-26 Growth and alleviation [11]

Staphylococcus arlettae BNW27 Growth and Alleviate alkalinity [3]Staphylococcus epidermidis IARI-THW-28 Growth and Yield [9]

Table 2: Response of plant growth promotion of microbes on growth of wheat.

652



The phyllosphere is common niche for synergism between bacteria and plant. Microorganisms on leaf surfaces are said to be extremophiles as they tolerate high temperature (40 - 55°C) and UV radiation in day time while cool temperatures (5 - 10°C) in night. Many bacteria such as Pseudomonas and Methylobacterium have been reported in the phyllosphere [8,66-69]. The endophytes are ubiquitous and have been found in all the species of plants studied to date; however, most of these endophytes/plant relationships are not well understood. Endophytes may benefit host plants by preventing pathogenic organisms from colonizing them Endophytes may also produce chemicals which inhibit the growth of competitors, including pathogenic organisms. Some bacterial endophytes have proven to increase plant growth. The presence of fungal endophytes can cause higher rates of water loss in leaves. However, certain fungal endophytes help plants survive drought and heat. Fungal endophytes-related host benefits are common phenomena, and have been the focus of much research, particularly among the grass endophytes. Endophytic bacteria live in plant tissues without causing substantive harm to the host. Bacterial endophytes have been recovered from a variety of plants including: sugarcane, pine tree, rice, eucalyptus tree, sunflower, potato. The endophytes reported from wheat were Achromobacter, Microbiospora, Micrococcus, Pantoea, Planobispora, Planomonospora, Planomonospora, Pseudomonas, Rhodococcus, Stenotrophomonoas, Streptomyces and Thermomonospora [14,16].

The wheat microbiomes enhance growth through numerous mechanisms viz. The biological nitrogen fixation (BNF; solubilization of phosphorus, potassium and zinc; Secretion of hormones such as auxins, indole acetic acid (IAA), cytokinins, gibberellins and ethylene; Facilitating the uptake of essential nutrients (N, P, Fe, Zn, etc.) from the atmospheric air and soil; Fe solubilization and mineralization; Induction of systemic resistance; Production of 1-aminocyclopropane-1-carboxylate deaminase (ACC; Quorum sensing (QS) signal interference and inhibition of biofilm formation; Promoting beneficial plant-microbe symbioses; Exhibiting antifungal activity, exhibition of antagonistic activity against phytopathogenic microorganisms by producing siderophores, b-1,3-glucanase, chitinases and antibiotics etc.

Phosphate solubilization and mineralization

Phosphorus is an important plant nutrient, next only to nitrogen and classed along nitrogen and potassium as a major plant nutrient element. Microorganisms are involved in a range of processes that effect the transformation of soil phosphorus (P) and are thus an integral component of soil P cycle. However, a large proportion of soluble inorganic phosphate added to the soil is rapidly fixed a s insoluble forms soon after the application and become unavailable to the plants [47,70,71]. The phenomenon of fixation and precipitation of P in soil is pH dependent; Al and Fe phosphate are formed in acidic soil while in calcareous soils high concentration of Ca results in pH precipitation. Microorganisms are critical for the transfer of P from the poorly available soil pools [20,72-75].

Several soil microbes possess the ability to change insoluble forms by secreting organic acids such as formic, acetic, propionic, lactic, glycolic, fumaric and succinic acid. Plants utilize only inorganic P; organic P compounds must first be hydrolyzed by the phosphatase enzyme, which mostly originate from plant roots, through the action of bacteria [47,76]. Since then it has been established that there are specific groups of soil microorganisms which increase the availability of phosphates to the plants, not only by mineralizing organic phosphorus compounds but also rendering inorganic phosphorus compounds more available to them [5,47,61,76]. The efficacy of various phosphate solubilizing bacteria (PSB) in dissolving insoluble phosphates such as suspension, agar, soil, bone meal, hydroxyapatite, and rock phosphate has received considerable attention during last two decades [3,47,62,77,78].

Mineralization of most organic phosphorous compounds is carried out by means of phosphatase enzymes. The conversion of insoluble inorganic P to a form accessible by plants is achieved by PSB via organic acids, chelation and exchange reactions [47,61]. However, organic P forms, particularly phytates, are predominant in most soils (10 - 50% of total P) and must be mineralized by phytases (myo-inositol hexakisphosphate phosphohydrolases) to be available P for plants. There are many reports which have shown that Bacillus sp., Providencia sp., Brevundimonas and Alcaligenes were recorded positive for P solubilization. The role of PGP microbes in production of phosphatase, β-gluconase, dehydrogenase, antibiotic, solubilization of phosphates and other nutrients, stabilization of soil aggregates, improved soil structure and organic matter contents has been recognized.

653



Potassium solubilization and immobilization

Potassium is an essential macronutrient and most abundantly absorbed cation that play an important role in the growth, metabolism and development of plants. Without adequate potassium, the plants will have poorly developed roots, grow slowly, produce small seeds and have lower yields. Although, potassium constitutes about 2.5 per cent of the lithosphere but actual soil concentrations of this nutrient vary widely ranging from 0.04 to 3.0 per cent [79]. Plants absorb potassium only from the soil and its availability in soil is dependent upon the K dynamics as well as on total K content. Out of the three forms of potassium found in the soil, soil minerals make up more than 90 to 98% of soil potassium and most of it is unavailable for plant uptake. The second non-exchangeable form of potassium makes up approximately 1 to 10 per cent of soil potassium and consists predominantly of interlayer K of non-expanded clay minerals such as illite and lattice K in K-feldspars, which contribute significantly to the plant uptake [80,81]. Release of non-exchangeable K to the third exchangeable form occurs when level of exchangeable and solution K is decreased by crop removal, runoff, erosion and/or leaching [82]. With the introduction of high yielding crop varieties/hybrids and the progressive intensification of agriculture, the soils are getting depleted in potassium reserve at a faster rate. Moreover, due to imbalanced fertilizer application, potassium deficiency is becoming one of the major constraints in crop production. This emphasized the search to find an alternative indigenous source of K for plant uptake and to maintain K status in soils for sustaining crop production [12,13,83] evaluated forty-one endophytic bacteria were isolated from surface-sterilized roots and culms of wheat var. HS507, growing in NW Indian Himalayas. These bacteria were screened in vitro for multifarious plant growth promoting attributes such as solubilization of phosphorus, potassium, zinc; production of indole acetic acids, hydrogen cyanide, gibberellic acid, siderophore and activities of nitrogen fixation, ACC deaminase and biocontrol against Rhizoctonia solani and Macrophomina phaseolina at low temperature (4°C). One isolate IARI-HHS2-30, showed appreciable level of potassium solubilization was further characterized in vivo at control condition of low temperature. Based on 16S rDNA sequence analysis, this isolate was identified as Bacillus amyloliquefaciens assigned accession number KF054757. Analysis of the phylogenetic characterization showed close homology with typical psychrotolerant bacteria Bacillus amyloliquefaciens, Bacillus methylotrophicus, Bacillus polyfermenticus, Bacillus siamensis, Bacillus subtilis, and Bacillus vallismortis. Endophytic nature and plant growth promoting ability of IARI-HHS2-30 was tested by qualitatively and followed by inoculation onto wheat seedlings in low temperature conditions. At 30 days after inoculation, Bacillus amyloliquefaciens IARI-HHS2-30 to wheat plants resulted in significant increase in root/shoot length, fresh weight, and chlorophyll a content. Plant growth promoting features coupled with psychrophilic ability suggest that this endophytic bacterium may be exploited as bio-inoculants for various crops in low temperature and high-altitude condition.

Zinc solubilization

Zinc, a transition metal, is essentially required by plants for their growth and development. It plays a vital role in photosynthesis, membrane integrity, protein synthesis, pollen formation and immunity system. It is also an important component of nucleic acids and Zn-binding proteins. It is documented that about 3,000 proteins of higher plants contain Zn prosthetic groups. Moreover, Zn is required as a co-factor for the activity of more than 300 enzymes and enhances the level of antioxidants within plant tissues. Furthermore, Zn plays a critical role in hormonal regulation in plants. In addition, Zn is critical for the synthesis of phytohormones such as auxin, abscisic acid, gibberellins and cytokinins. Its deficiency reduces level of these phytohormones in plant tissues resulting in an impairment of cell growth. Thus, its deficiency in plant tissues adversely affects various vital processes occurring within plant body. Although Zn is required by the plant in microconcentration, its bio-available fraction in soil is very low due to various soil factors [84]. Some soils, despite having fair quantity of Zn cannot support plant growth because of poor bioavailable Zn. It is further documented that around 30% of the world’s soils are Zn deficient [85]. The bioavailable content of Zn in soil can be increased using both chemical and biological approaches. Mineral fertilizers are considered a good source of Zn but it gets fixed quickly on soil matrix, resulting in poor availability to plants [86]. It has been estimated that about 90% of the total soil Zn exist in residual fraction, having no relevance to bioavailable fraction [87]. It is crucial to increase bioavailability of Zn to plants by solubilizing fixed Zn and/or by reducing fixation of the applied Zn fertilizers. This can be achieved either by using organic amendments or potential Zn solubilizing bioinoculants. Organic amendments improve bioavailability of

654



Zn by increasing microbial biomass, which not only enhance the rate of decomposition of organic matter (source of Zn), but also enhance the bioavailability of indigenous Zn by lowering the soil pH and by releasing chelating agents. Similarly, exogenous application of some potential Zn solubilizing microflora has shown huge capability to improve bioavailable Zn content in soil and its uptake by plant roots [11,71].

The zinc solubilizing bacteria (ZSB) associated with wheat growing in central zone of India has been reported by [11,12]. On the basis of amplified ribosomal DNA restriction analysis (ARDRA) and 16S rRNA gene sequencing zinc solubilizing bacteria were identified as Arthrobacter Humicola, Bacillus alcalophilus, Bacillus barbaricus, Bacillus megaterium, Bacillus thuringiensis, Corynebacterium callunae, Exiguobacterium acetylicum, Lysinibacillus xylanilyticus, Paenibacillus dendritiformis, Paenibacillus tundra, Pantoea ananatis, Pseudomonas fuscovaginae, Pseudomonas lini, Pseudomonas monteilii, Pseudomonas stutzeri, Pseudomonas thivervalensis and Psychrobacter fozii. Among different groups of ZSB, Isolate Paenibacillus dendritiformis IARI-IIWP-4 show highest zinc solubilization (9.8 ± 1.5 mm). These promising isolates showing a range of useful plant growth promoting attributes insist to be explored for agricultural applications. In another study, ZSB with potential PGP attributes under different abiotic stress condition have been reported e.g. acidotolerant, alkalitolerant, psychrotrophic and thermophilic ZSB [3,4,12,49].

Biofortification is a novel approach which leads to the development of micronutrient dense staple crops. Among widely cultivated food crops, wheat plays a particularly important role in daily energy intake, especially in the developing world. Widely cultivated modern wheat cultivars with a high-yield capacity are poor sources of micronutrients, especially Fe and Zn, for meeting daily requirements of humans. In addition, wheat is rich in antinutritional compounds such as phytic acid and phenolic compounds that reduce biological availability of Fe and Zn in the human digestive tract. Presently, bio-fortification approach is getting much attention to increase the availability of micronutrients especially Fe and Zn in the major food crops. Use of plant growth promoting bacteria is becoming an effective approach to substitute synthetic fertilizers, pesticides, and supplements. The selected efficient plant growth promoting bacteria mobilize the nutrients by various mechanisms such as acidification, chelation, exchange reactions, and release of organic acids [62].

Biological nitrogen fixation

Nitrogen (N2) is essential element for growth in the entire living organism. Although dinitrogen is the major component of air, most living forms, excepting certain microorganisms, fulfil their needs for nitrogen by using combined forms of nitrogen. Nitrogen is abundant on the earth and composes 78% of the atmosphere but is unavailable to plants. It needs to be converted into ammonia, a form available to plants and other eukaryotes. Atmospheric nitrogen is converted into forms utilized by plants by three different processes: (i) Conversion of atmospheric nitrogen into oxides of nitrogen in the atmosphere. (ii) Industrial nitrogen fixation uses catalysts and high temperature (300 - 500°C) to convert nitrogen to ammonia. Biological nitrogen fixation involves the conversion of nitrogen to ammonia by microorganisms using a complex enzyme system identified as nitrogenase.

Biological nitrogen fixation, fixes about 60% of the earth’s available nitrogen and represents an economically beneficial and environmentally sound alternative to chemical fertilizers [88]. PGP microbes that fix nitrogen in non-leguminous plants are diazotrophs which form a non-obligate interaction with host. The process of nitrogen fixation is carried out by the nitrogenase enzyme coded by nif genes. One of the best studied diazotrophs for nitrogen fixation is Azospirillum sp. isolated from nitrogen poor soils. Members of these bacterial genera are capable of fixing atmospheric nitrogen and of promoting plant growth. In modern agriculture, the natural processes for replenishing nitrogen used up by crops are too slow to sustain the productivity needed. Major contributors of fixed N in the soil are the N fixing microbes and chemical fertilizers. Microbial system can siphon out appreciable amounts of N from the atmospheric reservoir and enrich soil with this important but scare nutrient [89]. Microbial groups that affect plants by supplying combined nitrogen include: (i) symbiotic N2-fixing Rhizobium which are obligate symbionts of the legumes, and others like Azospirillum which colonize root zones and fix N2 in loose associations with the plants, (ii) Actinomycetes in non-leguminous trees, and free living N2-fixers as blue green algae, Acetobacter, Azotobacter, Bacillus, Klebsiella and Pseudomonas [90].

655



Production of phytohormones

One of the direct mechanism by which PGP microbes can promote plant growth is by production of plant growth regulators or phytohormones [91,92]. Plant growth regulators (PGRs) are the organic substances that influence physiologically processes of the plant at very low concentration. Phytohormones include bacterial metabolites that effect plant growth; examples of phytohormones or their derivatives produced by bacteria, such as Azotobacter, Azospirillum, Bacillus and Pseudomonas. Beneficial effects of these PGRs include the promotion and proliferation of root development, which results in efficient uptake of water and nutrients [93]. observed production of PGP substances, by N2-fixing Azospirillum brasilense, in liquid culture medium. This bacterium produced small amount of IAA, gibberellins and cytokinin like substances. Auxin regulates shoot elongation and other physiological plant processes. Indole 3- acetic acid is a naturally occurring auxin. Many PGP microbial strains e.g. Azospirillum, Bacillus and Pseudomonas produce auxin and promote root development in plants [3,6]. The root growth promoting hormone auxin, as present in root exudates, is usually synthesized from the exudates amino acid tryptophan. The tryptophan concentration in exudates differs strongly among plants. Although it is relatively easy to measure the concentration of IAA produced in the laboratory, but it is difficult to assess and determine the levels of IAA produced in rhizosphere as expression of IAA genes is controlled by both genetic and environmental factors. Moreover, five different pathways are identified in bacteria for biosynthesis of IAA [91]. Inoculation of seeds with the auxin-generating Pseudomonas fluorescens WCS 365 did not result in an increase in the root or shoot weight of cucumber, sweet pepper, or tomato, but led to a significant increase in the root weight of radish, which produces at least nine times more tryptophan in its exudates per seedling than cucumber, sweet pepper, or tomato. Bacterial plant growth promotion is a well-established and complex phenomenon and is often achieved by the activities of more than one plant growth promoting trait that is exhibited by plant-associated bacteria. The presence of IAA and related compounds could be demonstrated for many diazotrophs, for example, Acetobacter diazotrophicus, Azospirillum, Azotobacter, Paenibacillus and Polymyxa sp. [94-96].

Indole acetic acid concentration was evaluated in indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan [97,98] described the interaction of Azospirillum strain and roots of cereal crop by applying an approach based on differential fluorescence induction (DFI) promoter trapping to identify genes of Azospirillum brasilense Sp-245 which were induced in the presence of spring wheat seed extracts. Production of plant growth promoting hormone IAA and other attributes such as P solubilization, hydrogen cyanide production, and ammonia production by plant growth promoting bacteria such as: Bacillus thuringiensis, Enterobacter asburiae and Serratia marcescens were studied under in vitro conditions by G Selvakumar., et al [99].

One of the mechanisms that a number of PGP microbes uses to facilitate plant growth and development is the lowering of plant ethylene concentration through the action of the enzyme ACC deaminase [100]. Pseudomonas putida GR 12-2 promoted growth of canola seedling and elongation of its root; but mutants of Pseudomonas putida GR 12-2 lacking ACC deaminase activity were unable to promote the growth of canola seedling roots under gnotobiotic conditions implicating the role of ACC deaminase in plant growth promotion. PGP microbes having ACC deaminase activity could be helpful in sustaining plant growth and development under stress condition by reducing stress induced ethylene production. Lately, efforts have been made to introduce ACC deaminase genes into plants to regulate ethylene level in plants for optimum growth particularly under stressed conditions like flooding, presence of organic toxicants, metals, drought, salt and flower wilting [101]. ACC deaminase has been widely reported in numerous microbial species of gram negative and positive bacteria, Rhizobia, endophytes and fungi [91,102-107].

Production of siderophores

Plants commonly excrete a soluble organic compound (chelators and phytosiderophores) which bind Fe3+ and helps to maintain it in solution. Chelators deliver the Fe3+ to the root surface where it is reduced to Fe2+ and immediately absorbed. The predominant form of iron in aerated soils is ferric ion, which is sparingly soluble. The concentration of iron is rather low, and insufficient to support microbial growth. To survive in such an environment, organisms were found to secrete Fe binding ligands called siderophore having higher affinity

656



(KD = 10-20 to 10-50) to sequester iron from the microenvironment [108]. Siderophore production is beneficial to plants by solubilizing iron formerly unavailable to the plant. It has also some biocontrol properties because it helps a particular microorganism to compete effectively against other organisms for available iron, especially pathogenic fungi [109].

Siderophores are ferric ion specific ligands of low molecular weight. Therefore, through production and secretion of siderophore, PGPR can prevent the proliferation of phytopathogens and thereby facilitating plant growth. The secreted siderophore molecules find most of the ferric ion that is available in the rhizosphere; and as a result, effectively prevent any pathogen in its immediate vicinity from proliferating because of lack of iron. It should be noted that the plant host is unaffected by depletion of iron caused by PGP Microbes. Plants are able to grow at much lower iron concentration (~1000 fold) than microbial phytopathogens [92]. Recently, wheat associated Bacilli have been isolated and characterized for direct and indirect PGP traits by [3]. 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 to 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%), gibberellic acid producers (24.8%).

Biological control

Three classical categories of antagonism are: antibiosis, competition and exploitation. Antibiosis refers to the production of metabolic agents by the organisms which have harmful effects on the others [110]. Competition is the active demand in excess of immediate supply of material or condition and exploitation is either predation or direct parasitism. Clarifications of causal mechanisms gave new impulses to find ways for the use of biological means to protect plant roots against pathogens action in disease through the agency of one or more living organisms other than the host [111,112]. During the last two decades, several examples of rhizobacteria capable of providing substantial disease control in the field have been reported. Many bacterial genera have shown their potential for biocontrol both under in vitro and in vivo conditions such as Agrobacterium [113]. Arthrobacter [114]. Azotobacter [115]. Bacillus, Enterobacter [17]. Pseudomonas [116]. Burkholderia [117]. Rhizobium and Bradyrhizobium [118,119]. Serratia [120], and Stenotrophomonas [121], were found to be potent for suppression of soil-borne fungal pathogens.

The production of antibiotics is considered to be one of the most powerful and studied biocontrol mechanisms of plant growth promoting bacteria against phytopathogens has become increasingly better understood over the past two decades [122-124]. A variety of antibiotics have been identified, including compounds such as amphisin, 2,4-diacetylphloroglucinol (DAPG), oomycin A, phenazine, pyoluteorin, pyrrolnitrin, tensin, tropolone, and cyclic lipopeptides produced by Pseudomonads and oligomycin A, kanosamine, zwittermicin A, and xanthobaccin produced by Bacillus, Streptomyces, and Stenotrophomonas sp. to prevent the proliferation of plant pathogens. Bacillus amyloliquefaciens is known for lipopeptide and polyketide production for biological control activity and plant growth promotion activity against soil borne pathogens [125]. Apart from the production of antibiotic, some bacteria are also capable of producing volatile compound known as hydrogen cyanide (HCN) for biocontrol of black root rot of tobacco, caused by Thielaviopsis basicola [126,127], also reported the production of DAPG and HCN by Pseudomonas contributing to the biological control of bacterial canker of tomato. Growth enhancement through enzymatic activity is another mechanism used by plant growth promoting bacteria. Plant growth promoting bacterial strains can produce certain enzymes such as chitinases, dehydrogenase, β-glucanase, lipases, phosphatases, proteases etc. exhibit hyperparasitic activity, attacking pathogens by excreting cell wall hydrolases [128]. Through the activity of these enzymes, plant growth promoting bacteria play a very significant role in plant growth promotion particularly to protect them from biotic and abiotic stresses by suppression of pathogenic fungi including Botrytis cinerea, Sclerotium rolfsii, Fusarium oxysporum, Phytophthora sp., Rhizoctonia solani, and Pythium ultimum [129].

657



Relationships between microbes and their hosts

Microbes that establish inside plant roots, forming more intimate associations are endophytes. These include a wide range of soil microbes forming less formal associations than the rhizobia-legume symbiosis; endophytes may stimulate plant growth, directly or indirectly and include the rhizobia. Endophytic microbes are those microbes that can be isolated from surface disinfected plant tissue or extracted from within the plant, and that do not visibly harm the plant [2,14,130,131]. In general, a greater proportion of endophytes are PGP microbes than is the case for microbes inhabiting the rhizoplane or rhizosphere. Nodulating (rhizobia) and other N2-fixing rhizobacteria are also endophytes, living in specially developed root organs; given their ability to promote plant growth through N2 fixation. These bacteria primarily rhizobia and the woody plant associated Frankia, although the cyanobacterial N2-fixing symbionts of the cycads could also be included as PGP microbes. Soil microbes in the genera Rhizobium, Bradyrhizobium, Sinorhizobium, Azorhizobium, Mesorhizobium and Allorhizobium, belonging to the family Rhizobiaceae, invade plant root systems and form root nodules. Collectively they are often referred to as rhizobia. These PGP microbes are mostly Gram-negative and rod-shaped, with a lower proportion being Gram-positive rods, cocci and pleomorphic forms. The primary mechanism by which rhizobia increase plant growth is N2 fixation [132].

It is generally assumed that PGP microbial stimulation of plant growth requires the binding of the bacterium to the plant root. The successful use of either rhizobial or PGP microbial inoculants in agriculture depends upon the delivery of viable bacteria to the root zone which is most frequently accomplished by inoculating seeds with a preparation of dormant bacterial cells, by means of coated seed or bulk inoculants. PGPB have a beneficial effect on plant growth via an enhancement of the nutrient status of their host, there obviously needs to be an intimate relationship between the PGP microbes and the host plant. However, the degree of intimacy between the PGPB and the host plant can vary depending on where and how the PGP microbes colonize the host plant. Relationships between PGP microbes and their hosts can be categorized into two levels of complexity rhizospheric and endophytic [23,133]. In rhizospheric relationships, PGP microbes may colonize the rhizosphere, the surface of the root, or even superficial intercellular spaces although this latter situation may often involve dead cell layers. Not any soil bacterium can colonize these areas.

Role of epiphytic as well as endophytic microbes from different host has been well characterized and described for plant growth promotion, adaptation for sustainable agriculture. The epiphytic microbes may survive or proliferates on phyllospheric surface depending on extent of influences of material in phyllospheric diffusates or exudates. The phyllospheric diffusates contains the principal nutrients factors (amino acids, glucose, fructose and sucrose), and such specialized habitats may provide niche for nitrogen fixation and secretions of substances capable of promoting the growth of plants. The phyllospheric microbes may performs an effective function in controlling the air borne pathogens inciting plant disease. Endophytic microbes enter in host plants mainly through wounds, naturally occurring as a result of plant growth or through root hairs and at epidermal conjunctions. Endophytes may be transmitted either vertically (directly from parent to offspring) or horizontally (among individuals). A given endophytic microbiome can be modified by factors such as the physicochemical structure of the soil, plant growth phase and plant physiological state, as well as by diverse environmental factors [134,135]. Endophytic microbes live in plant tissues without causing substantive harm to the host. Endophytic microbes exist within the living tissues of most plant species in form of symbiotic to slightly pathogenic.

Conclusion and Future Prospect

In conclusion, the present review revealed about the ecological significance, microbial diversity of microbes associated with wheat growing in diverse agro-climatic conditions and role of microbes in plant growth and ameliorations of diverse abiotic stress. Wheat is generally cultivated under different environmental conditions and after sowing, generally the crop suffers due to abiotic stresses such as high/low temperatures, salinity, low/high pH, and water deficient conditions. During this period, if the plant is protected with a better vigour, it can tide over the stress and grow normally. The modern agriculture is mostly dependent on chemical fertilizers which can be replaced by eco-friendly PGP microbial consortium or biofertilizers. Application of high doses of chemical fertilizers may temporarily help to increase crop production. However, this may turn into bitter and highly regrettable consequences where soil fertility will be depleted or become acidic and devoid of macro and micro nutrients for crops to grow and microorganisms to proliferate. Thus, it is

658



absolutely necessary to awake timely and be able to use eco-friendly inputs such as beneficial plant growth promoting microflora to save our ‘currency’, the soil and its constituents.

Acknowledgement

The authors are grateful to the Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi and Department of Biotechnology (DBT), Ministry of Science and Technology for providing the facilities and financial support.

Competing InterestsThe authors declare no conflict of interest.

Bibliography

1. Gupta HS., et al. “Wheat improvement in northern hills of india”. Agricultural Research 1.2 (2012): 100-116.

2. Yadav., et al. “Plant microbiomes and its beneficial multifunctional plant growth promoting attributes”. International Journal of Environmental Sciences and Natural Resources 3.1 (2017): 1-8.

3. Verma., et al. “Molecular diversity and multifarious plant growth promoting attributes of bacilli associated with wheat (triticum aestivum l.) rhizosphere from six diverse agro-ecological zones of india”. International Journal of Current Microbiology and Applied Sciences 56.1 (2016): 44-58.

4. Verma., et al. “Appraisal of diversity and functional attributes of thermotolerant wheat associated bacteria from the peninsular zone of india”. Saudi Journal of Biological Sciences (2016).

5. Yadav., et al. “Phosphorus solubilizing endophytic microbes: Potential application for sustainable agriculture”. Eu Voice 2 (2016): 21-22.

6. Yadav., et al. “Bioprospecting of plant growth promoting psychrotrophic bacilli from cold desert of north western indian Himalayas”. Indian Journal of Experimental Biology 54.2 (2016): 142-150.

7. Yadav and Ajar Nath. “Studies of methylotrophic community from the phyllosphere and rhizosphere of tropical crop plants”. M.Sc. Thaesis, Bundelkhand University (2009): 66.

8. Meena., et al. “Epiphytic pink-pigmented methylotrophic bacteria enhance germination and seedling growth of wheat (triticum aestivum) by producing phytohormone”. Anton Leeuw 101.4 (2012): 777-786.

9. Verma., et al. “Elucidating the diversity and plant growth promoting attributes of wheat (triticum aestivum) associated acidotolerant bacteria from southern hills zone of india”. Indian Journal of Life Sciences 10.2 (2013): 219-227.

10. Verma., et al. “Evaluating the diversity and phylogeny of plant growth promoting bacteria associated with wheat (triticum aestivum) growing in central zone of india”. International Journal of Current Microbiology and Applied Sciences 3.5 (2014): 432-447.

11. Verma Priyanka. “Genotypic and functional characterization of wheat associated microflora from different agro-ecological zones”. IARI, New Delhi/ NIT, Durgapur (2015): 182.

12. Verma., et al. “Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (triticum aestivum) from the northern hills zone of india”. Annals of Microbiology 65.4 (2015): 1885-1899.

13. Verma., et al. “Alleviation of cold stress in wheat seedlings by bacillus amyloliquefaciens iari-hhs2-30, an endophytic psychrotolerant k-solubilizing bacterium from nw indian Himalayas”. National Journal of Life Sciences 12.2 (2015a): 105-110.

https://link.springer.com/article/10.1007/s40003-012-0020-z

https://juniperpublishers.com/ijesnr/pdf/IJESNR.MS.ID.555601.pdf

https://juniperpublishers.com/ijesnr/pdf/IJESNR.MS.ID.555601.pdf

https://www.ncbi.nlm.nih.gov/pubmed/26567901



https://www.sciencedirect.com/science/article/pii/S1319562X16000449

https://www.sciencedirect.com/science/article/pii/S1319562X16000449

https://www.researchgate.net/publication/306212116_Phosphorus_Solubilizing_Endophytic_Microbes_Potential_Application_for_Sustainable_Agriculture

https://www.researchgate.net/publication/306212116_Phosphorus_Solubilizing_Endophytic_Microbes_Potential_Application_for_Sustainable_Agriculture



https://www.researchgate.net/publication/232768552_Studies_of_Methylotrophic_Community_from_the_Phyllosphere_and_Rhizosphere_of_Tropical_Crop_Plants

https://www.researchgate.net/publication/232768552_Studies_of_Methylotrophic_Community_from_the_Phyllosphere_and_Rhizosphere_of_Tropical_Crop_Plants



https://www.ijcmas.com/vol-3-5/Priyanka%20Verma,%20ET%20AL.pdf

https://www.ijcmas.com/vol-3-5/Priyanka%20Verma,%20ET%20AL.pdf

https://www.researchgate.net/publication/271743291_Genotypic_and_Functional_Characterization_of_Wheat_Associated_Microflora_from_Different_Agro-Ecological_Zones

https://www.researchgate.net/publication/271743291_Genotypic_and_Functional_Characterization_of_Wheat_Associated_Microflora_from_Different_Agro-Ecological_Zones

https://link.springer.com/article/10.1007/s13213-014-1027-4


https://www.researchgate.net/publication/286935556_Alleviation_of_cold_stress_in_wheat_seedlings_by_Bacillus_amyloliquefaciens_IARI-HHS2-30_an_endophytic_psychrotolerant_K-solubilizing_bacterium_from_NW_Indian_Himalayas

https://www.researchgate.net/publication/286935556_Alleviation_of_cold_stress_in_wheat_seedlings_by_Bacillus_amyloliquefaciens_IARI-HHS2-30_an_endophytic_psychrotolerant_K-solubilizing_bacterium_from_NW_Indian_Himalayas

659



14. Suman., et al. “Development of hydrogel-based bio-inoculant formulations and their impact on plant biometric parameters of wheat (triticum aestivum l.)”. International Journal of Current Microbiology and Applied Sciences 5.3 (2016): 890-901.

15. Damodaran., et al. “Isolation of salt tolerant endophytic and rhizospheric bacteria by natural selection and screening for promising plant growth-promoting rhizobacteria (pgpr) and growth vigour in tomato under sodic environment”. African Journal of Microbiology Research 7.44 (2013): 5082-5089.

16. Suman., et al. “Endophytic microbes in crops: Diversity and beneficial impact for sustainable agriculture In: Singh dp, abhilash pc, prabha r (eds), microbial inoculants in sustainable agricultural productivity, research perspectives”. Springer-verlag, india (2016): 117-143.

17. Wang., et al. “Isolation of a strong promoter fragment from endophytic enterobacter cloacae and verification of its promoter activity when its host strain colonizes banana plants”. Applied microbiology and biotechnology 93.4 (2012): 1585-1599.

18. Glick BR and Pasternak JJ. “Plant growth promoting bacteria. Molecular biotechnology principles and applications of recombinant DNA, 3rd edition”. ASM Press, Washington (2003): 436-454.

19. Kumar., et al. “Β-propeller phytases: Diversity, catalytic attributes, current developments and potential biotechnological applications”. The International Journal of Biological Macromolecules 98 (2017): 595-609.

20. Singh., et al. “First, high quality draft genome sequence of a plant growth promoting and cold active enzymes producing psychrotrophic arthrobacter agilis strain l77”. Standards in Genomic Sciences 11.1 (2016): 54.

21. Ashrafuzzaman., et al. “Efficiency of plant growth-promoting rhizobacteria (pgpr) for the enhancement of rice growth”. African Journal of Biotechnology 8.7 (2009).

22. Mia., et al. “Effect of plant growth promoting rhizobacterial (pgpr) inoculation on growth and nitrogen incorporation of tissue-cultured musa plantlets under nitrogen-free hydroponics condition”. Australian Journal of Crop Science 4.2 (2010): 85-90.

23. Srivastava., et al. “Diversity analysis of bacillus and other predominant genera in extreme environments and its utilization in agriculture” (2014).

24. Tiwari., et al. “Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (triticum aestivum) and chemical diversity in rhizosphere enhance plant growth”. Biology and Fertility of Soils 47.8 (2011): 907.

25. Abbaspoor., et al. “The efficiency of plant growth promoting rhizobacteria (pgpr) on yield and yield components of two varieties of wheat in salinity condition”. American-Eurasian Journal of Sustainable Agriculture 3.4 (2009): 824-828.

26. Ali., et al. “Effect of inoculation with a thermotolerant plant growth promoting pseudomonas putida strain akmp7 on growth of wheat (triticum spp.) under heat stress”. Journal of plant interactions 6.4 (2011): 239-246.

27. Alvarez MI., et al. “Effect of azospirillum on coleoptile growth in wheat seedlings under water stress”. Cereal Research Communications 24.1 (1996):101-107.

28. Arzanesh., et al. “Wheat (triticum aestivum l.) growth enhancement by azospirillum sp. Under drought stress”. World Journal of Microbiology and Biotechnology 27.2 (2011):197-205.

29. Ashraf., et al. “Inoculating wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress”. Biology and Fertility of Soils 40.3 (2004): 157-162.

30. Barra., et al. “Formulation of bacterial consortia from avocado (persea americana mill.) and their effect on growth, biomass and superoxide dismutase activity of wheat seedlings under salt stress”. Applied Soil Ecology 102 (2016): 80-91.

https://www.ijcmas.com/5-3-2016/Archna%20Suman,%20et%20al.pdf

https://www.ijcmas.com/5-3-2016/Archna%20Suman,%20et%20al.pdf

http://www.academicjournals.org/journal/AJMR/article-abstract/9EF0F3941484



https://www.researchgate.net/publication/282504957_Endophytic_Microbes_in_Crops_Diversity_and_Beneficial_Impact_for_Sustainable_Agriculture





https://www.sigmaaldrich.com/catalog/product/sigma/z701378?lang=en&region=IN

https://www.sigmaaldrich.com/catalog/product/sigma/z701378?lang=en&region=IN



https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5000428/


https://www.researchgate.net/publication/235929278_Efficiency_of_plant_growth-promoting_rhizobacteria_PGPR_for_the_enhancement_of_rice_growth

https://www.researchgate.net/publication/235929278_Efficiency_of_plant_growth-promoting_rhizobacteria_PGPR_for_the_enhancement_of_rice_growth

http://www.cropj.com/mia_4_2_2010_85_90.pdf

http://www.cropj.com/mia_4_2_2010_85_90.pdf

https://www.researchgate.net/publication/271838168_Diversity_analysis_of_Bacillus_and_other_predominant_genera_in_extreme_environments_and_its_utilization_in_Agriculture

https://www.researchgate.net/publication/271838168_Diversity_analysis_of_Bacillus_and_other_predominant_genera_in_extreme_environments_and_its_utilization_in_Agriculture

https://www.researchgate.net/publication/228870774_The_efficiency_of_Plant_Growth_Promoting_Rhizobacteria_PGPR_on_yield_and_yield_components_of_two_varieties_of_wheat_in_salinity_condition

https://www.researchgate.net/publication/228870774_The_efficiency_of_Plant_Growth_Promoting_Rhizobacteria_PGPR_on_yield_and_yield_components_of_two_varieties_of_wheat_in_salinity_condition

https://www.tandfonline.com/doi/full/10.1080/17429145.2010.545147

https://www.tandfonline.com/doi/full/10.1080/17429145.2010.545147

https://www.researchgate.net/publication/279539996_Effect_of_Azospirillum_on_coleoptile_growth_in_wheat_seedlings_under_water_stress

https://www.researchgate.net/publication/279539996_Effect_of_Azospirillum_on_coleoptile_growth_in_wheat_seedlings_under_water_stress



https://link.springer.com/article/10.1007/s00374-004-0766-y


https://www.sciencedirect.com/science/article/pii/S0929139316300488


660



31. Chakraborty., et al. “Water stress amelioration and plant growth promotion in wheat plants by osmotic stress tolerant bacteria”. World Journal of Microbiology and Biotechnology 29.5 (2013): 789.

32. Creus., et al. “Water relations and yield in azospirillum-inoculated wheat exposed to drought in the field”. Canadian Journal of Botany 82.2 (2004): 273-281.

33. Egamberdiyeva., et al. “Influence of growth-promoting bacteria on the growth of wheat in different soils and temperatures”. Soil Biology and Biochemistry 35.7 (2003): 973-978.

34. El-Azeem., et al. “Effect of seed inoculation with plant growth-promoting rhizobacteria on the growth and yield of wheat (triticum aestivum l.) cultivated in a sandy soil (2008).

35. Jha., et al. “Investigation on phosphate solubilization potential of agricultural soil bacteria as affected by different phosphorus sources, temperature, salt, and ph”. Communications in soil science and plant analysis 44.16 (2013): 2443-2458.

36. Kasim., et al. “Control of drought stress in wheat using plant-growth-promoting bacteria”. [journal article]. Journal of Plant Growth Regulation 32.1 (2013): 122-130.

37. Khalafallah., et al. “Effect of arbuscular mycorrhizal fungi on the metabolic products and activity of antioxidant system in wheat plants subjected to short-term water stress, followed by recovery at different growth stages”. Journal of applied sciences research 4.5 (2008): 559-569.

38. Mishra., et al. “Isolation, molecular characterization and growth-promotion activities of a cold tolerant bacterium pseudomonas sp. Nars9 (mtcc9002) from the indian himalayas. Biological research 42.3 (2009b): 305-313.

39. Mishra., et al. “Alleviation of cold stress in inoculated wheat (triticum aestivum l.) seedlings with psychrotolerant pseudomonads from nw Himalayas”. Archives of microbiology 193.7 (2011): 497-513.

40. Naveed., et al. “Drought stress amelioration in wheat through inoculation with burkholderia phytofirmans strain psjn”. Journal of Plant Growth Regulation 73.2 (2014): 121.

41. Rana., et al. “Diversity and biotechnological applications of endophytic microbes associated with maize (zea mays l.) growing in indian himalayan regions”. Paper presented at the In: Proceeding of National Conference on Advances in Food Science and Technology (2017).

42. Saxena., et al. “Role of archaea in sustenance of plants in extreme saline environments”. Paper presented at the In: Proceeding of 56th

Annual Conference of Association of Microbiologists of India and International Symposium on Emerging Discoveries in Microbiology (2015).

43. Selvakumar., et al. “Pseudomonas lurida m2rh3 (mtcc 9245), a psychrotolerant bacterium from the uttarakhand himalayas, solubilizes phosphate and promotes wheat seedling growth”. World Journal of Microbiology and Biotechnology 27.5 (2011): 1129-1135.

44. Sezen., et al. “Isolation and characterization of plant growth promoting rhizobacteria (pgpr) and their effects on improving growth of wheat”. Journal of Applied Biological Sciences 10.1 (2016): 41-46.

45. Singh., et al. “A halotolerant bacterium bacillus licheniformis hsw-16 augments induced systemic tolerance to salt stress in wheat plant (triticum aestivum)”. Frontiers in plant science 7 (2016).

46. Turan., et al. “Effects of plant-growth-promoting rhizobacteria on yield, growth, and some physiological characteristics of wheat and barley plants”. Communications in soil science and plant analysis 43.12 (2012): 1658-1673.

47. Yadav., et al. “Haloarchaea endowed with phosphorus solubilization attribute implicated in phosphorus cycle”. Scientific Reports (2015): 5.



http://www.nrcresearchpress.com/doi/abs/10.1139/b03-119

http://www.nrcresearchpress.com/doi/abs/10.1139/b03-119



https://www.researchgate.net/publication/257941476_Effect_of_Seed_Inoculation_with_Plant_Growth-Promoting_Rhizobacteria_on_the_Growth_and_Yield_of_Wheat_Triticum_aestivum_L_Cultivated_in_a_Sandy_Soil

https://www.researchgate.net/publication/257941476_Effect_of_Seed_Inoculation_with_Plant_Growth-Promoting_Rhizobacteria_on_the_Growth_and_Yield_of_Wheat_Triticum_aestivum_L_Cultivated_in_a_Sandy_Soil

https://www.tandfonline.com/doi/abs/10.1080/00103624.2013.803557




http://www.aensiweb.com/old/jasr/jasr/2008/559-569.pdf









https://www.researchgate.net/publication/315688130_Diversity_and_biotechnological_applications_of_endophytic_microbes_associated_with_maize_Zea_mays_L_growing_in_Indian_Himalayan_regions



https://www.researchgate.net/publication/286454452_Role_of_Archaea_in_sustenance_of_plants_in_extreme_saline_environments





https://www.researchgate.net/publication/309618718_Isolation_and_Characterization_of_Plant_Growth_Promoting_Rhizobacteria_PGPR_and_Their_Effects_on_Improving_Growth_of_Wheat

https://www.researchgate.net/publication/309618718_Isolation_and_Characterization_of_Plant_Growth_Promoting_Rhizobacteria_PGPR_and_Their_Effects_on_Improving_Growth_of_Wheat





661



48. Yaghoubian., et al. “Effect of glomus mosseae and piriformospora indica on growth and antioxidant defense responses of wheat plants under drought stress”. Journal of agricultural research 3.3 (2014): 239-245.

49. Krishna and Akhouri Pramod. “Characteristics of snow and glacier fed rivers in mountainous regions with special reference to himalayan basins Encyclopedia of snow, ice and glaciers”. Springer (2011): 128-133.

50. Chenu., et al. “Environment characterization as an aid to wheat improvement: Interpreting genotype– environment interactions by modelling water-deficit patterns in north-eastern Australia”. Journal of experimental botany 62.6 (2011): 1743-1755.

51. Yadav., et al. “Culturable diversity and functional annotation of psychrotrophic bacteria from cold desert of leh ladakh (india)”. World Journal of Microbiology Biotechnology 31.1 (2015): 95-108.

52. Sahay., et al. “Hot springs of indian himalayas: Potential sources of microbial diversity and thermostable hydrolytic enzymes”. 3 Biotechnology 7.2 (2017): 1-11.

53. Yadav., et al. “Diversity and phylogenetic profiling of niche-specific bacilli from extreme environments of india”. Annals of Microbiology 65.2 (2015): 611-629.

54. Federhen and Scott. “Type material in the ncbi taxonomy database”. Nucleic Acids Research (2014): 1127.

55. Moore and Ben. “Life in our universe Elephants in space”. Springer (2014): 99-113.

56. Amann., et al. “Phylogenetic identification and in situ detection of individual microbial cells without cultivation”. Archive of “Microbiological Reviews” 59.1 (1995): 143-169.

57. Boivin-Jahns., et al. “Comparison of phenotypical and molecular methods for the identification of bacterial strains isolated from a deep subsurface environment”. Applied and Environmental Microbiology 61.9 (1995): 3400-3406.

58. MacLean., et al. “Application of’next-generation’sequencing technologies to microbial genetics”. Nature Reviews Microbiology 7.4 (2009): 287-296.

59. Kaur., et al. “Production and characterization of a neutral phytase of penicillium oxalicum eufr-3 isolated from himalayan region”. NUS Department of Biological Sciences 9.1 (2017): 68-76.

60. Kumar., et al. “Unravelling rhizospheric diversity and potential of phytase producing microbes”. SM Journal of Biology 2.1 (2016): 1009.

61. Saxena., et al. “Microbial diversity of extreme regions: An unseen heritage and wealth”. Indian Journal of Plant Genetic Resources 29.3 (2016): 246-248.

62. Verma., et al. “Microbes in termite management: Potential role and strategies Sustainable termite management:”. Springer (2017): 197-217.

63. Glick., et al. “A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria”. Journal of Theoretical Biology 190.1 (1998): 63-68.

64. Gupta., et al. “Mechanism of plant growth promotion by rhizobacteria”. Indian Journal of Experimental Biology 38.9 (2000): 856-862.

65. Shukla., et al. “Syntrophic microbial system for ex-situ degradation of paddy straw at low temperature under controlled and natural environment”. Journal of Applied Biology and Biotechnology 4.2 (2016): 30-37.

66. Kim., et al. “Distinctive phyllosphere bacterial communities in tropical trees”. Microbial ecology 63.3 (2012): 674-681.

https://link.springer.com/article/10.1007/s40003-014-0114-x

https://link.springer.com/article/10.1007/s40003-014-0114-x

https://www.researchgate.net/publication/263449047_Characteristics_of_Snow_and_Glacier_Fed_Rivers_in_Mountainous_Regions_with_Special_Reference_to_Himalayan_Basins

https://www.researchgate.net/publication/263449047_Characteristics_of_Snow_and_Glacier_Fed_Rivers_in_Mountainous_Regions_with_Special_Reference_to_Himalayan_Basins










https://www.springer.com/in/book/9783319056715







https://doaj.org/article/a98a6b697510455cbc1c8b813e736ca1

https://doaj.org/article/a98a6b697510455cbc1c8b813e736ca1

https://www.researchgate.net/publication/302908874_Unravelling_Rhizospheric_Diversity_and_Potential_of_Phytase_Producing_Microbes

https://www.researchgate.net/publication/302908874_Unravelling_Rhizospheric_Diversity_and_Potential_of_Phytase_Producing_Microbes

http://www.indianjournals.com/ijor.aspx?target=ijor:ijpgr&volume=29&issue=3&article=007

http://www.indianjournals.com/ijor.aspx?target=ijor:ijpgr&volume=29&issue=3&article=007

https://link.springer.com/chapter/10.1007/978-3-319-68726-1_9





http://www.scopemed.org/?mno=220181

http://www.scopemed.org/?mno=220181


662



67. Perazzolli., et al. “Resilience of the natural phyllosphere microbiota of the grapevine to chemical and biological pesticides”. Archive of “Applied and Environmental Microbiology” 12 (2014): 3585-3596.

68. Rastogi., et al. “New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches”. FEMS Microbiology Letters 348.1 (2013): 1-10.

69. Redford., et al. “The ecology of the phyllosphere: Geographic and phylogenetic variability in the distribution of bacteria on tree leaves”. Environmental Microbiology 12.11 (2010): 2885-2893.

70. Sharma., et al. “Isolation of phosphate solubilizing microorganism (psms) from soil”. Journal of Microbiology and Biotechnology Research 1.2 (2011): 90-95.

71. Yadav., et al. “Archaea endowed with plant growth promoting attributes”. EC Microbiology 8.6 (2017): 294-298.

72. Osman and Khan Towhid. “Plant nutrients and soil fertility management Soils”. Springer (2013): 129-159.

73. Richardson., et al. “Plant mechanisms to optimise access to soil phosphorus”. Crop and Pasture Science 60.2 (2009): 124-143.

74. Yadav., et al. “Current applications and future prospects of eco-friendly microbes”. EU Voice 3.1 (2017).

75. Ziadi., et al. “Assessment and modeling of soil available phosphorus in sustainable cropping systems”. Advances in Agronomy 122 (2013): 85-126.

76. Gaba., et al. “Draft genome sequence of halolamina pelagica cdk2 isolated from natural salterns from rann of kutch, gujarat, india”. Genome Announcements 5.6 (2017): 1-2.

77. Antoun., et al. “Potential of rhizobium and bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: Effect on radishes (raphanus sativus l.)”. Plant and Soil 204.1 (1998): 57-67.

78. Mehta., et al. “An efficient method for qualitative screening of phosphate-solubilizing bacteria”. Current Microbiology 43.1 (2001): 51-56.

79. Sparks DL and Huang PM. “Physical chemistry of soil potassium”. Potassium in agriculture 16 (1985): 238-249.

80. Memon YM., et al. “Utilization of non-exchangeable soil potassium in relation to soil type, plant species and stage of growth”. Soil Research 26.3 (1988): 489-496.

81. Sharpley and Andrew N. “Relationship between soil potassium forms and mineralogy”. Soil Science Society of America Journal 53.4 (1989): 1023-1028.

82. Xiafang., et al. “Study on the conditions of potassium release by strain nbt of silicate bacteria”. Scientia Agricultural Sinica (China) 35.6 (2002): 373-377.

83. Sindhu., et al. “Nutrient cycling: Potassium solubilization by microorganisms and improvement of crop growth Geomicrobiology and biogeochemistry”. Springer (2014): 175-198.

84. Alloway BJ. “Soil factors associated with zinc deficiency in crops and humans”. Environmental Geochemistry and Health 31.5 (2009): 537-548.

85. Kochian and Leon V. “Molecular physiology of mineral nutrient acquisition, transport, and utilization”. Biochemistry and Molecular Biology of Plants (2000): 1204-1249.

http://aem.asm.org/content/early/2014/03/24/AEM.00415-14

http://aem.asm.org/content/early/2014/03/24/AEM.00415-14



https://www.jmbronline.com/index.php/JMBR/article/viewFile/22/22

https://www.jmbronline.com/index.php/JMBR/article/viewFile/22/22

https://www.researchgate.net/publication/318227054_Archaea_Endowed_with_Plant_Growth_Promoting_Attributes

https://www.researchgate.net/publication/228339784_Plant_mechanisms_to_optimise_access_to_soil_phosphorus

http://joann-whalen.research.mcgill.ca/Articles%20to%20be%20linked/Advances%20in%20Agronomy%202013%20v122%20pp85-126%20Assessment%20and%20Modeling%20of%20Soil%20Available%20P.pdf

http://joann-whalen.research.mcgill.ca/Articles%20to%20be%20linked/Advances%20in%20Agronomy%202013%20v122%20pp85-126%20Assessment%20and%20Modeling%20of%20Soil%20Available%20P.pdf



https://link.springer.com/article/10.1023/A:1004326910584

https://link.springer.com/article/10.1023/A:1004326910584



http://www.publish.csiro.au/SR/SR9880489

http://www.publish.csiro.au/SR/SR9880489

https://pubag.nal.usda.gov/pubag/downloadPDF.xhtml?id=21090&content=PDF

https://pubag.nal.usda.gov/pubag/downloadPDF.xhtml?id=21090&content=PDF

https://eurekamag.com/research/003/951/003951450.php

https://eurekamag.com/research/003/951/003951450.php





663



86. Zia., et al. “Fertility issues and fertilizer management in rice wheat system”. Farm management Notes FAO Reg. Off. Asia and Pacific, Bangkok, Thailand 23 (1997).

87. Mandal., et al. “Transformation of zinc in soils under submerged condition and its relation with zinc nutrition of rice”. Plant and soil 106.1 (1988): 121-126.

88. Verma., et al. “Impact of plant growth promoting rhizobacteria on crop production”. International Journal of Agricultural Research 5.11 (2010): 954-983.

89. Maheshwari DK. Potential microorganisms for sustainable agriculture: A techno-commercial perspective: IK International Pvt Ltd (2008).

90. Prasanna., et al. “Microbial diversity and multidimensional interactions in the rice ecosystem”. Archives of Agronomy and Soil Science 58.7 (2012): 723-744.

91. Glick and Bernard R. “Introduction to plant growth-promoting bacteria Beneficial plant-bacterial interactions”. Springer (2015): 1-28.

92. Lugtenberg Ben and Kamilova, Faina. “Plant-growth-promoting rhizobacteria”. Annual Review of Microbiology 63 (2009): 541-556.

93. Mehnaz, Samina. “Azospirillum: A biofertilizer for every crop Plant microbes symbiosis: Applied facets Springer (2015): 297-314.

94. Aarab., et al. “Isolation and screening of bacteria from rhizospheric soils of rice fields in northwestern morocco for different plant growth promotion (pgp) activities: An in vitro study”. International Journal of Current Microbiology and Applied Sciences 4.1 (2015): 260-269.

95. Jiang., et al. “Iaa-producing bacteria and bacterial-feeding nematodes promote arabidopsis thaliana root growth in natural soil”. European Journal of Soil Biology 52 (2012): 20-26.

96. Timmusk., et al. “Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: Enhanced biomass production and reduced emissions of stress volatiles”. PloS one 9.5 (2014): e96086.

97. Ahmad., et al. “Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities”. Microbiological Research 163.2 (2008): 173-181.

98. Pothier., et al. “Promoter-trap identification of wheat seed extract-induced genes in the plant-growth-promoting rhizobacterium azospirillum brasilense sp245”. Microbiology 153.10 (2007): 3608-3622.

99. Selvakumar G., et al. “Legume root nodule associated bacteria Plant microbe symbiosis: Fundamentals and advances”. Springer (2013): 215-232.

100. Glick., et al. “Biochemical and genetic mechanisms used by plant growth promoting bacteria: World Scientific (1999).

101. Glick and Bernard R. “Modulation of plant ethylene levels by the bacterial enzyme acc deaminase”. FEMS Microbiology Letters 251.1 (2005): 1-7.

102. Chen., et al. “The rhizobacterium variovorax paradoxus 5c-2, containing acc deaminase, promotes growth and development of arabidopsis thaliana via an ethylene-dependent pathway”. Journal of experimental botany ert031 64.6 (2013): 1565-1573.

103. de-Bashan., et al. “The potential contribution of plant growth-promoting bacteria to reduce environmental degradation–a comprehensive evaluation”. Applied Soil Ecology 61 (2012): 171-189.

104. Egamberdieva., et al. “Use of plant growth-promoting rhizobacteria to alleviate salinity stress in plants Use of microbes for the alleviation of soil stresses”. Springer 1 (2014): 73-96.

https://link.springer.com/article/10.1007/BF02371203


https://scialert.net/abstract/?doi=ijar.2010.954.983

https://scialert.net/abstract/?doi=ijar.2010.954.983

https://www.ikbooks.com/books/book/life-sciences/agriculture/potential-microorganisms-sustainable-agriculture/9788190746205/

https://www.ikbooks.com/books/book/life-sciences/agriculture/potential-microorganisms-sustainable-agriculture/9788190746205/



https://www.researchgate.net/publication/278650990_Introduction_to_Plant_Growth-promoting_Bacteria

https://www.annualreviews.org/doi/10.1146/annurev.micro.62.081307.162918

https://www.researchgate.net/publication/315721583_Azospirillum-_A_biofertilizer_for_every_crop

https://www.ijcmas.com/vol-4-1/Saida%20Aarab,%20et%20al.pdf









https://books.google.co.in/books/about/Biochemical_And_Genetic_Mechanisms_Used.html?id=vPq3CgAAQBAJ&redir_esc=y







https://www.researchgate.net/publication/258439662_Use_of_Plant_Growth-Promoting_Rhizobacteria_to_Alleviate_Salinity_Stress_in_Plants

https://www.researchgate.net/publication/258439662_Use_of_Plant_Growth-Promoting_Rhizobacteria_to_Alleviate_Salinity_Stress_in_Plants

664



105. Hayat., et al. “Soil beneficial bacteria and their role in plant growth promotion: A review”. Annals of Microbiology 60.4 (2010): 579-598.

106. Verma., et al. “Microbes mediated biofortification of wheat (triticum aestivum l.) for micronutrients by fe-chelating and zn-solubilizing bacteria”. Paper presented at the In: Proceeding of National Conference on Advances in Food Science and Technology (2017).

107. Yang., et al. “Rhizosphere bacteria help plants tolerate abiotic stress”. Trends Plant Sci, 14.1 (2009): 1-4.

108. Neilands JB. “Iron absorption and transport in microorganisms”. Annual Review of Nutrition 1.1 (1981): 27-46.

109. Viruel., et al. “Plant growth promotion traits of phosphobacteria isolated from puna, argentina”. Archives of microbiology 193.7 (2011): 489-496.

110. Jackson KA and Hunt JD. “Transparent compounds that freeze like metals”. Acta Metallurgica 13.11 (1965): 1212-1215.

111. Chugh., et al. “Molecular characterization of diverse wheat germplasm for puroindolineproteins and their antimicrobial activity”. Turkish Journal of Biology 39.3 (2015): 359-369.

112. Lynch JM and Ebben MH. “The use of micro-organisms to control plant disease”. The Journal of Applied Microbiology 61.15 (1986): 115-126.

113. Hammami I., et al. “Optimization and biochemical characterization of a bacteriocin from a newly isolated bacillus subtilis strain 14b for biocontrol of agrobacterium spp. Strains”. Letters in applied microbiology, 48.2 (2009): 253-260.

114. Banerjee., et al. “Stress induced phosphate solubilization by’arthrobacter’sp. And’bacillus’ sp. Isolated from tomato rhizosphere 4.6 (2010).

115. Kannan., et al. “Synergistic effect of beneficial rhizosphere microflora in biocontrol and plant growth promotion”. Journal of Basic Microbiology 49.2 (2009): 158-164.

116. Goswami., et al. “Elucidating multifaceted urease producing marine pseudomonas aeruginosa bg as a cogent pgpr and bio-control agent”. Plant Growth Regulation 75.1 (2015): 253-263.

117. Santiago., et al. “Biological control of eucalyptus bacterial wilt with rhizobacteria”. Biological Control 80 (2015): 14-22.

118. Akhtar., et al. “Biocontrol of fusarium wilt by bacillus pumilus, pseudomonas alcaligenes, and rhizobium sp. On lentil”. Turkish Journal of Biology 34.3 (2010): 1-7.

119. Mishra., et al. “Isolation, molecular characterization and growth-promotion activities of a cold tolerant bacterium pseudomonas sp. Nars9 (mtcc9002) from the indian Himalayas”. Biological Research 42.3 (2009a): 305-313.

120. Liu X., et al. “Biocontrol potential of an endophytic serratia sp. G3 and its mode of action”. World Journal of Microbiology and Biotechnology 26.8 (2010): 1465-1471.

121. Jankiewicz., et al. “Identification and characterization of a chitinase of stenotrophomonas maltophilia, a bacterium that is antagonistic towards fungal phytopathogens”. Journal of Bioscience and Bioengineering 113.1 (2012): 30-35.

122. Gupta G., et al. “Plant growth promoting rhizobacteria (pgpr): Current and future prospects for development of sustainable agriculture”. Journal of Microbial and Biochemical Technology 7 (2015): 096-102.

123. Shilev and Stefan. “Soil rhizobacteria regulating the uptake of nutrients and undesirable elements by plants Plant microbe symbiosis: Fundamentals and advances”. Springer (2013): 147-167.



https://www.researchgate.net/publication/315688053_Microbes_mediated_biofortification_of_wheat_Triticum_aestivum_L_for_micronutrients_by_Fe-chelating_and_Zn-solubilizing_bacteria

https://www.researchgate.net/publication/315688053_Microbes_mediated_biofortification_of_wheat_Triticum_aestivum_L_for_micronutrients_by_Fe-chelating_and_Zn-solubilizing_bacteria





https://www.sciencedirect.com/science/article/pii/0001616065900611

http://dergipark.gov.tr/download/article-file/121982

http://dergipark.gov.tr/download/article-file/121982



https://search.informit.com.au/documentSummary;dn=414789554792811;res=IELHSS

https://search.informit.com.au/documentSummary;dn=414789554792811;res=IELHSS





https://www.researchgate.net/publication/233388258_Biocontrol_of_Fusarium_wilt_by_Bacillus_pumilus_Pseudomonas_alcaligenes_and_Rhizobium_sp_on_lentil

https://www.researchgate.net/publication/233388258_Biocontrol_of_Fusarium_wilt_by_Bacillus_pumilus_Pseudomonas_alcaligenes_and_Rhizobium_sp_on_lentil







https://www.omicsonline.org/open-access/plant-growth-promoting-rhizobacteria-pgpr-current-and-future-prospects-for-development-of-sustainable-agriculture-1948-5948-1000188.php?aid=51029

https://www.omicsonline.org/open-access/plant-growth-promoting-rhizobacteria-pgpr-current-and-future-prospects-for-development-of-sustainable-agriculture-1948-5948-1000188.php?aid=51029



665



124. Verma., et al. “Hydrolytic enzymes production by thermotolerant bacillus altitudinis iari-mb-9 and gulbenkiania mobilis iari-mb-18 isolated from manikaran hot springs”. International Journal of Advanced Research 3.9 (2015b): 1241-1250.

125. Ongena., et al. “Bacillus lipopeptides: Versatile weapons for plant disease biocontrol”. Trends in microbiology 16.3 (2008): 115-125.

126. Sacherer., et al. “Extracellular protease and phospholipase c are controlled by the global regulatory gene gaca in the biocontrol strain pseudomonas fluorescens cha0”. FEMS microbiology letters 116.2 (1994): 155-160.

127. Lanteigne., et al. “Production of dapg and hcn by pseudomonas sp. Lbum300 contributes to the biological control of bacterial canker of tomato”. Phytopathology 102.10 (2012): 967-973.

128. Suman., et al. “Bioprospecting for extracellular hydrolytic enzymes from culturable thermotolerant bacteria isolated from manikaran thermal springs”. Research journal of biotechnology 10.4 (2015): 4.

129. Arora and Naveen Kumar. “Plant microbe symbiosis: Fundamentals and advances: Springer Science and Business Media (2013).

130. Yadav., et al. “Extreme cold environments: A suitable niche for selection of novel psychrotrophic microbes for biotechnological applications”. Advances in Biotechnology and Microbiology 2.2 (2017): 1-4.

131. Yadav., et al. “Biodiversity and biotechnological applications of psychrotrophic microbes isolated from indian himalayan regions”. EC Microbiology ECO.01 (2017): 48-54.

132. Saxena., et al. “Biotechnological applications of microbes isolated from cold environments in agriculture and allied sectors”. Paper presented at the International Conference on “Low Temperature Science and Biotechnological Advances (2015).

133. Tarafdar JC and Claassen N1. “Organic phosphorus compounds as a phosphorus source for higher plants through the activity of phosphatases produced by plant roots and microorganisms”. Biology and Fertility of Soils 5.4 (1988): 308-312.

134. Lian., et al. “Response of endophytic bacterial communities in banana tissue culture plantlets to fusarium wilt pathogen infection”. The Journal of general and applied microbiology 54.2 (2008): 83-92.

135. Mitter., et al. “A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds”. Frontiers in microbiology 8 (2017): 11.

Volume 14 Issue 9 September 2018©All rights reserved by Priyanka Verma and Archna Suman.

https://www.researchgate.net/publication/282441863_Hydrolytic_enzymes_production_by_thermotolerant_Bacillus_altitudinis_IARI-MB-9_and_Gulbenkiania_mobilis_IARI-MB-18_isolated_from_Manikaran_hot_springs

https://www.researchgate.net/publication/282441863_Hydrolytic_enzymes_production_by_thermotolerant_Bacillus_altitudinis_IARI-MB-9_and_Gulbenkiania_mobilis_IARI-MB-18_isolated_from_Manikaran_hot_springs






https://www.researchgate.net/publication/275256353_Bioprospecting_for_extracellular_hydrolytic_enzymes_from_culturable_thermotolerant_bacteria_isolated_from_Manikaran_thermal_springs

https://www.researchgate.net/publication/275256353_Bioprospecting_for_extracellular_hydrolytic_enzymes_from_culturable_thermotolerant_bacteria_isolated_from_Manikaran_thermal_springs

https://www.springer.com/in/book/9788132212867

https://juniperpublishers.com/aibm/pdf/AIBM.MS.ID.555584.pdf

https://juniperpublishers.com/aibm/pdf/AIBM.MS.ID.555584.pdf

https://www.researchgate.net/publication/317616861_Biodiversity_and_Biotechnological_Applications_of_Psychrotrophic_Microbes_Isolated_from_Indian_Himalayan_Regions

https://www.researchgate.net/publication/317616861_Biodiversity_and_Biotechnological_Applications_of_Psychrotrophic_Microbes_Isolated_from_Indian_Himalayan_Regions

https://www.researchgate.net/publication/275637659_Biotechnological_applications_of_microbes_isolated_from_cold_environments_in_agriculture_and_allied_sectors

https://www.researchgate.net/publication/275637659_Biotechnological_applications_of_microbes_isolated_from_cold_environments_in_agriculture_and_allied_sectors







Documents

Cronicon · Priyanka Verma1,2* and Archna Suman2 Among cereal crops, wheat (Triticum aestivum L.) is the most important cereal crop which is contributes almost one-third to the total