PGPB-mediated IST against abiotic stress.
Abstract
Free-living plant growth-promoting rhizobacteria (PGPR) have favourable effect on plant growth, tolerance against stresses and are considered as a promising alternative to inorganic fertilizer for promoting plant growth, yield and quality. PGPR colonize at the plant root, increase germination rates, promote root growth, yield, leaf area, chlorophyll content, nitrogen content, protein content, tolerance to drought, shoot and root weight, and delayed leaf senescence. Several important bacterial characteristics, such as biological nitrogen fixation, solubilization of inorganic phosphate and mineralization of organic phosphate, nutrient uptake, 1-aminocydopropane-1-carboxylic acid (ACC) deaminase activity and production of siderophores and phytohormones, can be assessed as plant growth promotion traits. By efficient use, PGPR is expected to contribute to agronomic efficiency, chiefly by decreasing costs and environmental pollution, by eliminating harmful chemicals. This review discusses various bacteria acting as PGPR, their genetic diversity, screening strategies, working principles, applications for wheat and future aspects in terms of efficiency, mechanisms and the desirable properties. The elucidation of the diverse mechanisms will enable microorganisms developing agriculture further.
Keywords
- PGPR
- wheat
- abiotic stress
- enzymes
- nitrogen fixation
1. Introduction
Wheat (
Plant growth-promoting bacteria (PGPR), typically colonizing at the rhizosphere, is known to increase the yield and help alleviating the effects of biotic or abiotic stresses [2]. The practice of PGPRs is promising in reducing the use of chemical fertilisers, at the same time maintaining yields at commercially viable levels and/or maintaining grain protein content [3]. As such, PGPR contributes to the improvement of both local and global environments, reducing dependence on non-renewable resources while still being economically competitive (both price and quality aspect) [4–6].
Several beneficial free-living rhizobacteria have been termed as PGPR, including, but not limited to,
The biological nitrogen fixation (BNF) and phosphate solubilization
Secretion of hormones, for example, 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
Zinc and iron solubilization and organic matter mineralization
Secretion of certain volatiles and lowering of plant ethylene level
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
Interference with pathogen toxin production.
A non-exhaustive list of Plant Growth Promoting Rhizobacteria (PGPR)s used to alleviate various stresses is given in Table 1, and the various other uses of these bacteria are listed in Table 2. Two important mechanisms employed by PGPR are the production of different phytohormones, including auxins, cytokinins and gibberellins, and the synthesis of several enzymes, such as phosphatase and catalase, modulating plant growth and development as well as strengthening their immune system [16, 17]. In a review, Palacios et al. compiled many molecules facilitating interactions of PGPB with plants [18]. The list includes plant hormones, hydrolytic enzymes, antibiotics, flavonoids, other signal molecules, toxic molecules, siderophores, exopolysaccharide, volatiles, polyamines, lectins and vitamins. The PGPR efficiency, in turn, depends upon a number of factors like soil mineral content, type of crop and its genotype, specific PGPR strain and its combination with the plant, competition with indigenous strains, environmental conditions and the growth parameters evaluated, as illustrated in greenhouse and field trials [3] and other studies [19–22].
Stress type | Bacterial inoculate | Properties of the crop | Reference |
---|---|---|---|
Drought/water | Wheat, growth rate of coleoptiles | [132] | |
Drought | Wheat ( |
[133] | |
Drought | Wheat ( |
[134] | |
Drought | Wheat ( Grain yield, photosynthetic rate, water use efficiency, chlorophyll content |
[135] | |
Drought | Wheat ( |
[137] | |
Heavy metal-stressed | Wheat ( Indole-3-acetic acid Antioxidant defence system SOD shoots and roots Shoot POD and CAT |
[198] | |
Heavy metal | Higher heavy metal resistance Siderophore,, indole acetic acid, HCN, P solubilization |
[151] | |
Osmotic stress | Wheat ( |
[199] | |
Osmotic stress | Wheat ( |
[200] | |
Cold | IAA, P solubilization, rhamnolipids, siderophores | [201] | |
Cold | Root and shoot dry weight, leaf total chlorophyll content, stomatal conductance, leaf relative water content | [171] | |
Temperature | Wheat ( |
[202] | |
Heat stress | Wheat ( |
[98] | |
Temperature | Wheat ( |
[203] | |
Salinity | Wheat ( |
[62] | |
Salinity | Wheat ( |
[125] | |
Salinity | Wheat (Triticum aestivum) grain yield, 1000 grain weight, grain yield | [143] | |
Salinity | Wheat ( |
[142] | |
Salinity | Durum wheat ( |
[128] | |
Salinity | Wheat | [204] | |
Wheat ( |
[46] | ||
Salinity | P solubilization, indole acetic acid (IAA), siderophore, ammonia,proline accumulation, salt tolerance, choline oxidase activity | [140] | |
Wheat ( |
[85] | ||
Salinity | Wheat ( |
[97] | |
Wheat ( |
[95] | ||
Salinity | Wheat ( Germination rate percentage and index and improved nutrient status |
[205] | |
Salinity | Root length, root elongation, dry weight | [1] | |
Salinity | Number of tillers, grain weight, growth and yield | [138] |
PGPR | Source | Plant growth regulation | Results of addition of bacteria to plants | References |
---|---|---|---|---|
Wheat rhizospheric | N2 fixation | Grain yield, dry matter, N content | [32] | |
Mutant | Indole-3-acetic acid (IAA) | Number and length of lateral roots, distribution of root hairs. | [206] | |
Rhizospheric | N2 fixation | Root dry weight, N content root and hoot | [207] | |
Wheat | N2 fixation | Dry weight, nitrogen content | [192] | |
Wheat Rhizospheric | P solubilization, N2 fixation, IAA | Seed emergence radicle and plumule length | [114] | |
Wheat Rhizospheric | N2 fixation | Growth | [73] | |
Wheat | Cytokinin, N2 fixation | Plant growth | [208] | |
Digitaria decumbens | Lectins, N2 fixation | Activities of a-glucosidase, b-glucosidase and b-galactosidase in wheat-seedling | [209] | |
Non-sterilised and surface-sterilised wheat roots | N2 fixation | Root-hair deformation colonization | [99] | |
Wheat rhizospheric | N2 fixation | Plant growth, N accumulation and content, biomass, grain yield and protein concentration | [164] | |
Maize | N2 fixation | Dry weight of roots and shoots, total N per plant colonized the interior of wheat roots | [26] | |
Auxin | Plant growth | [210] | ||
Wheat roots, | Biomass number of ears nitrogen accumulation, N content | [172] | ||
Geographically and climatically diverse locations | Gibberellic acid (GA), IAA | Increase in number root hairs, thickening of roots, root and shoot biomass | [11] | |
Rhizosphere of wheat | P solubilization, siderophore Indole acetic acid ACC deaminase, diacetyl-phloroglucinol |
Protein content, yield and grain quality | [162] | |
Rhizosphere of wheat | P solubilization, N2 fixation | Root and shoot weight, total biomass | [111] | |
Various sources | N2 fixation | Grain and straw yield, N content in grain and straw | [211] | |
Rice | N2 fixation P solubilization |
Root and shoot weight, plant height, spike length, grain yield, seed P content, leaf protein and sugar content | [185] | |
Rhizosphere of wheat grown in saline soil | Hydrogen cyanide (HCN), IAA, ACC deaminase, protease, cellulases competitive colonisers, tolerated salt | Shoot and root length, shoot, root and dry matter of wheat | [125] | |
Rhizospheres of wheat. | P solubilization, siderophore IAA |
Wheat growth, increase in the rate of germination, in the root length and dry weight | [106] | |
N2 fixation | uptake of several macro and micronutrients | [5] | ||
N2 fixation, siderophores, P solubilization | Root growth Root length |
[45] | ||
Grass | IAA, siderophores P solubilization |
Shoot and root Weight colonisation |
[212] | |
Wheat | P solubilization, ACC deaminase, siderophores, IAA | Increased soil enzyme activities, total productivity, and nutrient uptake, nutrient assimilation | [102] | |
Wheat roots | P solubilization, IAA, siderophores, ACC deaminase, diacetyl-phloroglucinol | Grain yield Protein and mineral nutrient concentration (P, K, Cu, Fe, Zn, Mn) alkaline and acid phosphatase, urease, dehydrogenase. |
[163] | |
sorghum | Phytohormones(IAA, GA), HCN, ammonia, Siderophore, P-solubilization | Increased root, shoot length, dry biomass, chlorophyll content | [98] | |
Rhizosphere of wheat | P-solubilization, N2 fixation, ACC deaminase siderophore, ammonia, HCN | Seedling length, germination, plant height, panicle weight, root weight | [40] | |
ACC deaminase, IAA-like products, P solubilization | Height, tillers, number of grains/spike, garain and straw yield, N, P and K uptake | [54] | ||
Radish | P solubilization IAA, HCN, siderophores | Growth and nutrient uptake parameters | [64] | |
Wheat rhizosphere | Ammonia siderophore, HCN, IAA, P solubilization Zn solubilization | N uptake in wheat grain. protein content grain Fe, Zn, Mn, and Cu content | [161] | |
Barley | Siderophore ACC deaminase. Protease phytate | Grain number, weight and yield | [23] | |
Wheat | N2 fixation, P solubilization | Plant height, number spikes, grain yield, protein content | [213] | |
Wheat | N2 fixation | Agronomic performance and yield of wheat | [35] | |
Rubus and wheat | P solubilization | Shoot length, root and shoot dry weight, P uptake | [214] | |
Naturally saline habitats | ACC deaminase, IAA, HCN, siderophores, P solubilization, | Seed germination, root length, root elongation, dry weight root biomass | [1] | |
N2 fixation P solubilization, |
Nutrient status of soil and plants, plant biomass, N and P uptake | [177] | ||
N2 fixation P solubilization |
Grain and straw N content, root and shoot weight. grain and total biomass yield, protein content, grain weight per spike | [3] | ||
Rhizospheres of wheat and tomato | IAA, lipase, protease, siderophore, P solubilization salt tolerant | Germination, root length, root weight, panicle weight | [52] | |
Zeatin type cytokinins | Shoot concentrations of zeatin, total chlorophyll and nitrogen contents of wheat leaves | [90] | ||
Wheat roots | P solubilization, phytase, chitinase, IAA, siderophore | Growth, biomass, Fe, Mn and P content antifungal activity | [43] | |
Rhizosphere of wheat | IAA, ACC deaminase | Both coleoptiles and root elongation, root length, wheat seedling growth, growth and biomass of Wheat coleoptiles | [215] | |
Wheat rhizosphere | Zn solubilizing | Enhance grain yield and Zn content of wheat | [160] | |
Wheat rhizosphere | P solubilization | Plant biomass P, K, Mg, Zn and Mn contents at harvest |
[216] |
Despite the promising features from agronomic efficiency and crop yield perspective, the key bottleneck for the commercial use of PGPRs is their varying performance under field conditions: the results obtained in a field are not always similar to those of laboratory [23], which calls for immediate further research on the agricultural use of these PGPRs.
2. Mechanisms of plant growth promotion
2.1. Biological nitrogen fixation
PGPR improve plant growth by multiple mechanisms. A well-established mechanism is the biological nitrogen fixation (BNF), as described in extensive literature available on diazotrophic association in wheat and subsequent addition of nitrogen to the ecosystem [24], contributing to the total N2 requirement of wheat [25–27]. Nitrogen fixation is considered to be a direct plant growth-promoting trait and the nitrogen-fixing rhizobacteria provide an alternative source to inorganic nitrogen fertilizers.
2.2. Phosphate solubilization and mineralization
Soil stores several structures and forms of phosphate, both organic and inorganic. Phosphorus plays a key role in photosynthesis, respiration, root development, signal transduction, energy transfer, macromolecular biosynthesis and the resistance ability of plants to diseases and adverse conditions. However, majority of soil phosphorus is insoluble that is not available to plants. The secondary significant contributing factor to promoted growth is the availability of phosphorous in the rhizospheric region, as a result of phosphate solubilization by the PGPR [41].
PGPRs serve as phosphate (and zinc) solubilizer (PSB). This is due to the decreased pH of the medium, indicating the possible involvement of organic acids such as gluconic acid. Plant growth promotion can be achieved through solubilization of inorganic phosphates by these organic acids. de Werra et al. showed that this happens with not only gluconate but also malate [42, 43]. These results were consistent with earlier report on the P and Zn solubilizing properties of
Phosphorus-solubilizing
Combined application of PSB with conventional fertilizer (50% PSB, 25 kg/ha P2O5) improves plant growth. Similarly, a combination of PGPRs are more effective when compared with isolated applications as reported by Hassan et al. for wheat crops and by Baig et al. for wheat yield and P uptake [53, 55].
2.2.1. Mineralization
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 [56]. 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 [57, 58]. Previous research has shown that
Singh et al. reported that phytase-producing bacteria from Himalayan soils showed ability to solubilize inorganic phosphate, producing phytase, siderophores, ammonia and IAA and increased availability of P, IAA and ammonia leading to increased plant growth [57]. The role of PGPR in production of phosphataes, β-gluconase, dehydroginase, antibiotic, solubilization of phosphates and other nutrients, stabilization of soil aggregates, improved soil structure and organic matter contents has been recognized.
2.3. Production of plant hormones and other beneficial plant metabolite
There are five groups of plant hormones of well-known PGRs, namely auxins, gibberellins, cytokinins, ethylene and abscisic acid [60]. Direct plant growth promotion includes symbiotic and non-symbiotic PGPR, which functions through production of these plant hormones [11, 61–63]. Much attention has been given on the role of phytohormone auxin. Production of indole-3-ethanol or indole-3-acetic acid (IAA), the compounds belonging to auxins, which is known to stimulate in cell elongation, division and differentiation responses in plants, has been reported for several bacterial genera [12, 17, 64]. PGPR promote root growth by increasing root surface area, which, in turn, promotes nutrient uptake, thereby indirectly stimulating plant growth positively [52, 65]. Khalid et al. reported a correlation between
Inoculation with
When applied in optimum concentrations, bacterial indole-3-acetic acid (IAA), synthesized by gram-positive and -negative, photosynthetic, methylotrophic and cyanobacteria, is reported to stimulate root hair formation, at the same time increasing the length and the number of primary and lateral roots [66, 72, 79]. IAA synthesis by these bacteria is reported to be affected by tryptophan, vitamins, salt and oxygen levels, as well as pH, temperature, carbon and nitrogen source. For example, IAA from
As a PGPR application to wheat seedlings, Sachdev et al. reported that IAA producing
Cytokinins can be produced by representative strains of
2.3.1. Accumulation of osmolytes
Proline is a known osmoprotectant, promoting the protection of the plant from drought, salt and other stresses [94]. Alternative to proline accumulation, another defence strategy is to increase total soluble sugar level in plants under salinity stress. PGPRs have been demonstrated to enhance wheat stress tolerance via osmolyte accumulation as reported in Refs. [95–97]. Ali et al. used
Yegorenkova et al. suggested that lectin-carbohydrate interactions are involved in the initial stages of bacterial-plant root attachment [99]. Additionally, PGPR producing extracellular polymeric substance are reported to enhance greatly the soil volume macropores and the rhizosphere aggregation of soil, which results in increased water and fertiliser availability to plants [46].
2.4. Siderophore and exopolysaccharide production by PGPR
With its unique physico-chemical properties, iron (Fe) has a key role in plant growth, taking part in several metabolic pathways including TCA cycle, nitrogen fixation, respiration and ETC, oxidative phosphorylation and photosynthesis, biosynthetic regulation (chlorophyll, toxin, vitamins, antibiotic, cytochrome and pigment) and as cofactor for numerous enzymes [100]. Following this, iron deficiency (typically caused by low iron bioavailability) is frequently seen at elevated pH, alkali soils in dry regions, as well as in case of excessive fertilizer and pesticides application.
Siderophores are small iron carriers, chemically high-affinity iron chelating compounds secreted by PGPRs and are among the strongest soluble Fe3+ binding agents known. Comprehensive information on the role of siderophores in increasing iron oxide solubility and promoting dissolution in soils requires the consideration of the rates of various processes such as siderophore exudation, the uptake, and the degradation rates [101]. In BNF, siderophores are expected to play significant role, since in its very essence, nitrogenase requires Fe [102], also supported by a high correlation between N and Fe uptake.
Siderophore productions promote the crop growth, or protect the plant against pathogens. Produced by microorganisms, these are found in soil solutions and influence Fe nutrition of plants [103]. The role of siderophores has been reported as signalling molecules and as such, their use points to avenues for novel agricultural applications [54].
The wheat seed inoculation was tested for their effect on wheat in terms of healthier germination and productivity. The organisms used were siderophoregenic pyoverdin-producing
Some PGPR strains may also protect plants from salt and drought stress by producing exopolysaccharides (EPS), binding, in turn, Na+ or by biofilm formation [107]. Resultingly, reduced Na+ results in lower Na+ uptake and high K+/Na+ ratio, promoting survival in salt-stressed conditions [107, 108]. Another example is the wheat seedling inoculation by EPS producing strain of
2.5. PGPR and plant nutrient uptake
Seed inoculation with the bacterium has been found to improve the growth and nutrient uptake of wheat seedlings via promotion of the plant growth and increased root surface area or the general root architecture [110]. With enlarged root hairs, nutrient uptake is promoted [21, 71, 77, 111].
The PGPR effects also increase N and P uptake in field trials [112], presumably, by stimulating greater plant root growth. Both
Inoculation of efficient plant-growth-promoting actinobacterial
2.6. Alleviation of abiotic stress in wheat by PGPR
Abiotic stress is the major cause of decreasing crop productivity worldwide. The application of the combination of PGPR and mycorrhizal fungi alleviates the stress conditions, as reported by Nadeem et al., via the regulation of hormones, nutrition uptake and growth [124]. Similar outcomes have been reported by Cakmakci et al. for wheat and spinach plants [77]. Enzymatic activities in the leaves of these plants such as glucose-6-phosphate dehydrogenase, 6-phosphogluconate dehydrogenase, glutathione reductase and glutathione S-transferase have been observed.
Additionally, numerous studies suggested that both IAA and ACC deaminase-producing bacteria protect plants most effectively, against a wide range of different stresses [125]. Notable reports among those are
2.6.1. Drought
Drought stress, exhibited as limited water supply, usually causes a severe loss in plant yield, where the combination of severity and duration are critical factors for plant survival [130]. The application of PGPR can counteract damaging effects of moisture stress, and therefore boost crop yields. Creus et al. reported that growing
Moreover, Pereyra et al. reported that
Inoculation of wheat with
2.6.2. Salinity
Salinity decreases the yield of many crops because salt inhibits plant photosynthesis, protein synthesis and lipid metabolism. Nutrient contents decrease in the roots and shoots with increasing NaCl concentration in the growth medium. PGPR counteract osmotic stress and help plant growth. Investigations on interaction of PGPR with other microbes and their effect on the physiological response of crop plants under different soil salinity regimes are still in incipient stage.
Rhizobacteria that are residing within the rhizosphere of plants growing in saline habitats may have already been adapted to salt stress that may be a valuable resource to develop crop inoculants. Raheem and Ali isolated rhizobacteria that were producing beneficial plant growth-promoting metabolites such as IAA and ACC-deaminase activity [138]. The isolation of indigenous microorganisms from the stress-affected soils and screening on the basis of their stress tolerance and PGP traits may be useful in the rapid selection of efficient strains that could be used as bio-inoculants for stressed crops [139, 140]. For several durum cultivars, PGPR efficacy in mitigating salt stress in tetraploid wheat is salt level and bacterial strain-specific [128, 141, 142]. There are some instances of ameliorating salt-stricken cereal crops by PGPR’s. Salinity stress in the wheat was alleviated by inoculations with four strains of PGPR,
2.6.3. Mitigation of cold stress in wheat by PGPR
The over-wintering ability of PGPR is fundamental when considering uses in colder climates. De Freitas and Germida reported that
The effect of inoculation with 12 psychrotolerant
Higher chlorophyll content in leaves of cold acclimated winter wheat over control plants was also reported [105]. Proline is a dominant amino acid that accumulates in many organisms upon exposure to environmental stress and plays multiple roles in plant adaptation to stress. Also increased proline content in wheat plant at low temperature with the bacterial inoculation is an indication to chilling tolerance [105].
Turan et al. conducted greenhouse experiments in wheat and barley under cold stress conditions to determine the growth, freezing injury, antioxidant enzyme activity effect of four different rhizobacteria and boron [149]. The authors showed that boron+PGPR treatments have positive effect on root and shoot growth, H2O2, and SOD, POD and CAT antioxidant enzyme activities of wheat and barley plants under cold and control conditions. This suggests that the PGPB application can ameliorate the deleterious effects of cold stress by increasing chlorophyll content, photosynthetic activity and relative water content, altering mineral uptake, and decreasing membrane damage, increasing cold tolerance in wheat and barley.
2.6.4. Metal stress tolerance in wheat
Plant growth-promoting bacteria are able to also grow in heavy metal-contaminated environment and protect plants against heavy metals toxicity in contaminated soils [150, 151]. Hasnain and Sabri reported that upon
Under Cr stress conditions, Shahzadi et al. reported root length, shoot length, root dry weight and shoot dry weight, respectively, as compared to uninoculated control plants upon inoculation of wheat seeds with
2.7. Improve yield and quality of wheat
Beneficial rhizobacteria associated with cereals has increased recently and several studies clearly demonstrated the positive and beneficial effects of PGPR on growth and yield of wheat at different environment under variable ecological conditions (Turan et al., 2010).
Zn solubilizing rhizobacteria significantly influenced the growth, yield and Zn concentration of wheat grain over uninoculated control and Zn fertilizer [160, 161]. Similarly, increased nutrient concentrations in wheat due to inoculation were reported in Refs. [5, 118, 162–165]. It is pointed out by Mäder et al. that microbial inoculants have been shown to be a valid option for sustainable high quality wheat production in low-input areas, promising to improve the nutritional status and health of the rural population [163]. In a survey of 20 years of experiments, Okon and Labandera-Gonzalez reported that 60–70% of the experiments showed yield increases due to inoculation, with statistically significant increases in yield from 5 to 30% [31].
3. Co-inoculation of multiple PGPRs
Inoculation with mixed different strains could be an alternative to inoculation with individual strains, likely reflecting the different mechanisms used by each strain in the consortium [173]. Combined inoculation with N2-fixing and phosphate solubilizing bacteria were more effective than a single microorganism for providing a more balanced nutrition for plants [19, 174]. There are numerous examples in wheat whereby synergistic effects of multiple PGPRs are observed [97, 175, 176]. Among those, notable is the combined inoculation of mixtures and biofilmed bio-inoculants (
Seed bacterization with both strains,
Several authors conducted experiments on wheat either under pot and field conditions to examine the effect of co-inoculations of PGPR on the growth and yield of wheat. Kumar et al. found that
Nowadays, there is a greater awareness to use biological components such as PGPR and mycorrhizal fungi as a component of integrated nutrient management strategies to obtain higher input use efficiency, to maintain the desired productivity through optimization of the benefits from all possible sources, to cope with increasing fertilizer costs and their long-term adverse effects on agricultural ecosystems such as increased nutritional imbalances, declining productivity, adverse conditions prevailing in this ecosystem, and or a combination of these factors, as reported in Refs. [113, 177]. Note that some PGPR inoculants may adversely affect mutualistic associations between plants and indigenous soil microorganisms and suggest a possible reason as to why spring wheat growth was not consistently enhanced by these
Wheat rhizobacterial community structure is highly dynamic and influenced by different factors such as wheat cultivar line ages, plant’s age, growth stage, distance from the soil to the root, root exudation pattern, multiple soil properties and agronomic practises [162, 188, 189]. Roesti et al. employed a consortia formed by a PGPR
All in all, greater attention should be paid to new combinations of different types and properties organisms such as N2-fixing and P-solubilizing bacteria for improvement of biofertilizers efficiency [19].
4. PGPR reduce chemical fertilization
Due to high cost of chemical fertilizers and negative environmental effects, the use of PGPR as biofertilizer is advantageous for development of sustainable agriculture, increasing agronomic efficiency, once the use of chemical fertilizers can be reduced or eliminated if the inoculants are efficient [6]. The use of bio-fertilizers with a good management can decrease the leaching loss of nitrate and phosphate from the agricultural land and improve the ground water quality [190]. Also, the use of PGPR with low-fertilizer rate is also an environment friendly step and would be a viable supplementary strategy for further increasing crop yields [71, 78, 191].
Trials conducted under greenhouse conditions showed that most of PGPR in the absence of any fertilizer application achieved increases in root and shoot weight [3], corresponding to nitrogen treatment at the rate of 40 and 80 kg N ha−1 in wheat. Furthermore, co-inoculation of N2-fixing and P-solubilizing bacteria always gave equal or higher grain yield than conventional application of nitrogen.
Rosas et al. studied the promotion effect of
It could be concluded that application of PGPR with low-fertilizer rates could be a viable supplementary strategy for maximum benefits and should be employed with appropriate doses of fertilizers to get maximum benefit in terms of fertilizer savings and better growth in any yield of crops. Experiments as field trials with dry land areas, the co-inoculations of PGPR strains for wheat, maize and barley with chemical fertilizers gave improved response [3, 183, 192–197].
References
- 1.
Ramadoss D, Lakkineni VK, Bose P, Ali S, Annapurna K. Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats. SpringerPlus. 2013;2(1):1. - 2.
Chauhan A, Shirkot C, Kaushal R, Rao D. Plant Growth-Promoting Rhizobacteria of Medicinal Plants in NW Himalayas: Current Status and Future Prospects. Plant-Growth- Promoting Rhizobacteria (PGPR) and Medicinal Plants:Chapter 19. Soil Biology, Springer International Publishing Swetzerland ; 2015. pp. 381–412. - 3.
Cakmakci R, Turan M, Gulluce M, Sahin F. Rhizobacteria for reduced fertilizer inputs in wheat ( Triticum aestivum spp. vulgare) and barley (Hordeum vulgare) on Aridisols in Turkey. International Journal of Plant Production. 2014;8(2).163-182. - 4.
Adesemoye A, Torbert H, Kloepper J. Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microbial Ecology. 2009;58(4):921–9. - 5.
Hungria M, Campo RJ, Souza EM, Pedrosa FO. Inoculation with selected strains of Azospirillum brasilense andA. lipoferum improves yields of maize and wheat in Brazil. Plant and Soil. 2010;331(1–2):413–25. - 6.
Souza Rd, Ambrosini A, Passaglia LM. Plant growth-promoting bacteria as inoculants in agricultural soils. Genetics and Molecular Biology. 20158(4):401-419. - 7.
Kloepper J, Schroth M, Miller T. Effects of rhizosphere colonization by plant growth-promoting rhizobacteria on potato plant development and yield. Phytopathology. 1980;70(11):1078–82. - 8.
Vessey JK. Plant growth promoting rhizobacteria as biofertilizers. Plant and Soil. 2003;255(2):571–86. - 9.
Sharma MP, Srivastava K, Sharma SK. Biochemical characterization and metabolic diversity of soybean rhizobia isolated from Malwa region of Central India. Plant Soil and Environment. 2010;56(8):375–83. - 10.
Chanway C, Nelson L, Holl F. Cultivar-specific growth promotion of spring wheat ( Triticum aestivum L.) by coexistent Bacillus species. Canadian Journal of Microbiology. 1988;34(7):925–9. - 11.
Narula N, Deubel A, Gans W, Behl R, Merbach W. Paranodules and colonization of wheat roots by phytohormone producing bacteria in soil. Plant Soil and Environment. 2006;52(3):119. - 12.
Hayat R, Ali S, Amara U, Khalid R, Ahmed I. Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology. 2010;60(4):579–98. - 13.
Bhattacharyya P, Jha D. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World Journal of Microbiology and Biotechnology. 2012;28(4):1327–50. - 14.
Pérez-Montaño F, Alías-Villegas C, Bellogín R, Del Cerro P, Espuny M, Jiménez-Guerrero I, et al. Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiological Research. 2014;169(5):325–36. - 15.
Maksimov I, Veselova S, Nuzhnaya T, Sarvarova E, Khairullin R. Plant growth-promoting bacteria in regulation of plant resistance to stress factors. Russian Journal of Plant Physiology. 2015;62(6):715–26. - 16.
Glick BR. Plant growth-promoting bacteria: mechanisms and applications. Hindawi Publishing Corporation Scientifica.2012, 1-15, Article ID 963401. - 17.
Frankenberger J, Arshad M. Microbial synthesis of auxins. Phytohormones in soils. Marcel Dekker, New York. 1995. pp. 35–71. - 18.
Palacios OA, Bashan Y, de-Bashan LE. Proven and potential involvement of vitamins in interactions of plants with plant growth-promoting bacteria—an overview. Biology and Fertility of Soils. 2014;50(3):415–32. - 19.
Şahin F, Çakmakçi R, Kantar F. Sugar beet and barley yields in relation to inoculation with N2-fixing and phosphate solubilizing bacteria. Plant and Soil. 2004;265(1–2):123–9. - 20.
Cakmakçi R, Dönmez F, Aydın A, Şahin F. Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biology and Biochemistry. 2006;38(6):1482–7. - 21.
Cakmakci R, Dönmez MF, Erdoğan Ü. The effect of plant growth promoting rhizobacteria on barley seedling growth, nutrient uptake, some soil properties, and bacterial counts. Turkish Journal of Agriculture and Forestry. 2007;31(3):189–99. - 22.
Çakmakçı R, Dönmez MF, Ertürk Y, Erat M, Haznedar A, Sekban R. Diversity and metabolic potential of culturable bacteria from the rhizosphere of Turkish tea grown in acidic soils. Plant and Soil. 2010;332(1–2):299–318. - 23.
Smyth E, McCarthy J, Nevin R, Khan M, Dow J, O’Gara F, et al. In vitro analyses are not reliable predictors of the plant growth promotion capability of bacteria; a Pseudomonas fluorescens strain that promotes the growth and yield of wheat. Journal of Applied Microbiology. 2011;111(3):683–92. - 24.
Döbereiner J, editor Biological N2 fixation by endophytic diazotrophs in non-leguminous crops in the tropics. Abstr 7th Int Symp BNF with Non-legumes; 1996. - 25.
Islam N, Rao C, Kennedy I. Facilitating a N2-fixing symbiosis between diazotrophs and wheat. Biofertilisers in action. Rural Industries Research and Development Corporation, Canberra. 2002. pp. 84–93. - 26.
Iniguez AL, Dong Y, Triplett EW. Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Molecular Plant-Microbe Interactions. 2004;17(10):1078–85. - 27.
Venieraki A, Dimou M, Pergalis P, Kefalogianni I, Chatzipavlidis I, Katinakis P. The genetic diversity of culturable nitrogen-fixing bacteria in the rhizosphere of wheat. Microbial Ecology. 2011;61(2):277–85. - 28.
Hegazi N, Fayez M, Amin G, Hamza M, Abbas M, Youssef H, et al. Diazotrophs associated with non-legumes grown in sandy soils. Nitrogen fixation with non-legumes: Springer; 1998. pp. 209–22. - 29.
Ganguly T, Jana A, Moitra D. An evaluation of agronomic potential of Azospirillum brasilense and Bacillus megaterium in fibre-legume-cereal system in an Aeric Haplaquept. Indian Journal of Agricultural Research. 1999;33(1):35–9. - 30.
Balandreau J. The spermosphere model to select for plant growth promoting rhizobacteria. Biofertilisers in Action Rural Industries Research and Development Corporation, Canberra. 2002. pp. 55–63. - 31.
Okon Y, Labandera-Gonzalez CA. Agronomic applications of Azospirillum: an evaluation of 20 years worldwide field inoculation. Soil Biology and Biochemistry. 1994;26(12):1591–601. - 32.
Boddey RM, Baldani VL, Baldani JI, Döbereiner J. Effect of inoculation ofAzospirillum spp. on nitrogen accumulation by field-grown wheat. Plant and Soil. 1986;95(1):109–21. - 33.
Santa O, Santa H, Fernández R, Michela G, Ronzelli P, Soccol C. I Infl uence of Azospirillum sp. inoculation in wheat, barley and oats Rev Setor Ciênc Agrárias Ambientais. 2008;4(2):197–207. - 34.
Piccinin GG, Dan LGdM, de LE Braccini A. Agronomic Efficiency of Azospirillum brasilense in physiological parameters and yield components in wheat crop. Journal of Agronomy. 2011;10(4):132–5. - 35.
Piccinin GG, Braccini AL, Dan LG, Scapim CA, Ricci TT, Bazo GL. Efficiency of seed inoculation with Azospirillum brasilense on agronomic characteristics and yield of wheat. Industrial Crops and Products. 2013;43:393–7. - 36.
Merbach W, Ruppel S, Schulze J. Dinitrogen fixation of microbe-plant associations as affected by nitrate and ammonium supply. Isotopes in Environmental and Health Studies. 1998;34(1–2):67–73. - 37.
Ruppel S, Hecht-Buchholz C, Remus R, Ortmann U, Schmelzer R. Settlement of the diazotrophic, phytoeffective bacterial strain Pantoea agglomerans on and within winter wheat: an investigation using ELISA and transmission electron microscopy. Plant and Soil. 1992;145(2):261–73. - 38.
Remus R, Ruppel S, Jacob H-J, Hecht-Buchholz C, Merbach W. Colonization behaviour of two enterobacterial strains on cereals. Biology and Fertility of Soils. 2000;30(5–6):550–7. - 39.
Silini-Cherif H, Silini A, Ghoul M, Yadav S. Isolation and characterization of plant growth promoting traits of a rhizobacteria: Pantoea agglomerans lma2. Pakistan Journal of Biological Sciences. 2012;15(6):267. - 40.
Rana A, Saharan B, Joshi M, Prasanna R, Kumar K, Nain L. Identification of multi-trait PGPR isolates and evaluating their potential as inoculants for wheat. Annals of Microbiology. 2011;61(4):893–900. - 41.
Jones DL, Darrah PR. Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant and Soil. 1994;166(2):247–57. - 42.
de Werra P, Péchy-Tarr M, Keel C, Maurhofer M. Role of gluconic acid production in the regulation of biocontrol traits of Pseudomonas fluorescens CHA0. Applied and Environmental Microbiology. 2009;75(12):4162–74. - 43.
Jog R, Pandya M, Nareshkumar G, Rajkumar S. Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology. 2014;160(4):778–88. - 44.
Indiragandhi P, Anandham R, Madhaiyan M, Sa T. Characterization of plant growth–promoting traits of bacteria isolated from larval guts of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae). Current Microbiology. 2008;56(4):327–33. - 45.
Sachdev D, Nema P, Dhakephalkar P, Zinjarde S, Chopade B. Assessment of 16S rRNA gene-based phylogenetic diversity and promising plant growth-promoting traits of Acinetobacter community from the rhizosphere of wheat. Microbiological Research. 2010;165(8):627–38. - 46.
Upadhyay S, Singh J, Singh D. Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere. 2011;21(2):214–22. - 47.
Chen Y, Rekha P, Arun A, Shen F, Lai W-A, Young C. Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Applied Soil Ecology. 2006;34(1):33–41. - 48.
Afzal A, Ashraf M, Asad SA, Farooq M. Effect of phosphate solubilizing microorganisms on phosphorus uptake, yield and yield traits of wheat ( Triticum aestivum L.) in rainfed area. International Journal of Agriculture and Biology. 2005;7:207–9. - 49.
Shaharoona B, Jamro G, Zahir Z, Arshad M, Memon K. Effectiveness of various Pseudomonas spp. and Burkholderia caryophylli containing ACC-Deaminase for improving growth and yield of wheat ( Triticum aestivum I.). Journal of Microbiology and Biotechnology. 2007;17(8):1300. - 50.
Basheer A, Zaheer A, Qaisrani MM, Rasul G, Yasmin S, Mirza MS. Development of DNA markers for detection of inoculated bacteria in the rhizosphere of wheat ( Triticum aestivum L.). Pakistan Journal of Agriculture Science. 2016;53(1):135–42. - 51.
Turan M, Gulluce M, von Wirén N, Sahin F. Yield promotion and phosphorus solubilization by plant growth-promoting rhizobacteria in extensive wheat production in Turkey. Journal of Plant Nutrition and Soil Science. 2012;175(6):818–26. - 52.
Baghaee Ravari S, Heidarzadeh N. Isolation and characterization of rhizosphere auxin producing Bacilli and evaluation of their potency on wheat growth improvement. Archives of Agronomy and Soil Science. 2014;60(7):895–905. - 53.
Baig KS, Arshad M, Shaharoona B, Khalid A, Ahmed I. Comparative effectiveness of Bacillus spp. possessing either dual or single growth-promoting traits for improving phosphorus uptake, growth and yield of wheat ( Triticum aestivum L.). Annals of Microbiology. 2012;62(3):1109–19. - 54.
Zabihi H, Savaghebi G, Khavazi K, Ganjali A, Miransari M. Pseudomonas bacteria and phosphorous fertilization, affecting wheat ( Triticum aestivum L.) yield and P uptake under greenhouse and field conditions. Acta Physiologiae Plantarum. 2011;33(1):145–52. - 55.
Hassan TU, Bano A. Role of carrier-based biofertilizer in reclamation of saline soil and wheat growth. Archives of Agronomy and Soil Science. 2015;61(12):1719–31. - 56.
Pandey A, Trivedi P, Kumar B, Palni LMS. Characterization of a phosphate solubilizing and antagonistic strain of Pseudomonas putida (B0) isolated from a sub-alpine location in the Indian Central Himalaya. Current Microbiology. 2006;53(2):102–7. - 57.
Singh P, Kumar V, Agrawal S. Evaluation of phytase producing bacteria for their plant growth promoting activities. International Journal of Microbiology. 2014. - 58.
Richardson A, Hadobas P, Hayes J, O'hara C, Simpson R. Utilization of phosphorus by pasture plants supplied with myo-inositol hexaphosphate is enhanced by the presence of soil micro-organisms. Plant and Soil. 2001;229(1):47–56. - 59.
Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G. Endophytic bacteria in sunflower ( Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Applied Microbiology and Biotechnology. 2007;76(5):1145–52. - 60.
Zahir ZA, Arshad M, Frankenberger WT. Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Advances in Agronomy. 2003;81:97–168. - 61.
Dobbelaere S, Vanderleyden J, Okon Y. Plant growth-promoting effects of diazotrophs in the rhizosphere. Critical Reviews in Plant Sciences. 2003;22(2):107–49. - 62.
Creus CM, Sueldo RJ, Barassi CA. Water relations and yield in Azospirillum-inoculated wheat exposed to drought in the field. Canadian Journal of Botany. 2004;82(2):273–81. - 63.
Etesami H, Alikhani HA, Jadidi M, Aliakbari A. Effect of superior IAA producing rhizobia on N, P, K uptake by wheat grown under greenhouse condition. World Applied Sciences Journal. 2009;6:1629–33. - 64.
Selvakumar G, Joshi P, Suyal P, Mishra PK, Joshi GK, Bisht JK, 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. 2011;27(5):1129–35. - 65.
Egorshina A, Khairullin R, Sakhabutdinova A, Luk’yantsev M. Involvement of phytohormones in the development of interaction between wheat seedlings and endophytic Bacillus subtilis strain 11BM. Russian Journal of Plant Physiology. 2012;59(1):134–40. - 66.
Khalid A, Arshad M, Zahir Z. Screening plant growth‐promoting rhizobacteria for improving growth and yield of wheat. Journal of Applied Microbiology. 2004;96(3):473–80. - 67.
Harari A, Kigel J, Okon Y. Involvement of IAA in the interaction between Azospirillum brasilense and Panicum miliaceum roots. Nitrogen fixation with non-legumes: Springer; 1989. pp. 227–34. - 68.
Martin P, Glatzle A, Kolb W, Omay H, Schmidt W. N2‐fixing bacteria in the rhizosphere: Quantification and hormonal effects on root development. Zeitschrift für Pflanzenernährung und Bodenkunde. 1989;152(2):237–45. - 69.
Dobbelaere S, Croonenborghs A, Thys A, Broek AV, Vanderleyden J. Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant and Soil. 1999;212(2):153–62. - 70.
Akbari GA, Arab SM, Alikhani H, Allakdadi I, Arzanesh M. Isolation and selection of indigenous Azospirillum spp. and the IAA of superior strains effects on wheat roots. World Journal of Agricultural Sciences. 2007;3(4):523–9. - 71.
Spaepen S, Dobbelaere S, Croonenborghs A, Vanderleyden J. Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant and Soil. 2008;312(1-2):15–23. - 72.
Baudoin E, Lerner A, Mirza MS, El Zemrany H, Prigent-Combaret C, Jurkevich E, et al. Effects of Azospirillum brasilense with genetically modified auxin biosynthesis gene ipdC upon the diversity of the indigenous microbiota of the wheat rhizosphere. Research in Microbiology. 2010;161(3):219–26. - 73.
Mrkovacki N, Milic V. Use of Azotobacter chroococcum as potentially useful in agricultural application. Annals of Microbiology. 2001;51(2):145–58. - 74.
Egamberdieva D. Plant growth promoting properties of rhizobacteria isolated from wheat and pea grown in loamy sand soil. Turkish Journal of Biology. 2008;32(1):9–15. - 75.
Leinhos V, Vacek O. Biosynthesis of auxins by phosphate-solubilizing rhizobacteria from wheat ( Triticum aestivum and rye (Secale cereale). Microbiological Research. 1994;149(1):31–5. - 76.
Hafeez FY, Yasmin S, Ariani D, Zafar Y, Malik KA. Plant growth-promoting bacteria as biofertilizer. Agronomy for Sustainable Development. 2006;26(2):143–50. - 77.
Çakmakçı R, Erat M, Erdoğan Ü, Dönmez MF. The influence of plant growth–promoting rhizobacteria on growth and enzyme activities in wheat and spinach plants. Journal of Plant Nutrition and Soil Science. 2007;170(2):288–95. - 78.
Abbasi M, Sharif S, Kazmi M, Sultan T, Aslam M. Isolation of plant growth promoting rhizobacteria from wheat rhizosphere and their effect on improving growth, yield and nutrient uptake of plants. Plant Biosystems. 2011;145(1):159–68. - 79.
Duca D, Lorv J, Patten CL, Rose D, Glick BR. Indole-3-acetic acid in plant–microbe interactions. Antonie Van Leeuwenhoek. 2014;106(1):85–125. - 80.
Kucey R. Alteration of size of wheat root systems and nitrogen fixation by associative nitrogen-fixing bacteria measured under field conditions. Canadian Journal of Microbiology. 1988;34(6):735–9. - 81.
Dodd I, Zinovkina N, Safronova V, Belimov A. Rhizobacterial mediation of plant hormone status. Annals of Applied Biology. 2010;157(3):361–79. - 82.
Belimov AA, Dodd IC, Safronova VI, Dumova VA, Shaposhnikov AI, Ladatko AG, et al. Abscisic acid metabolizing rhizobacteria decrease ABA concentrations in planta and alter plant growth. Plant Physiology and Biochemistry. 2014;74:84–91. - 83.
Sachdev DP, Chaudhari HG, Kasture VM, Dhavale DD, Chopade BA. Isolation and characterization of indole acetic acid (IAA) producing Klebsiella pneumoniae strains from rhizosphere of wheat (Triticum aestivum ) and their effect on plant growth. Indian Journal of Experimental Biology. 2009;47(12):993. - 84.
Bothe H, Körsgen H, Lehmacher T, Hundeshagen B. Differential effects of Azospirillum, auxin and combined nitrogen on the growth of the roots of wheat. Symbiosis. 1992;13(1-3):167–79. - 85.
Sadeghi A, Karimi E, Dahaji PA, Javid MG, Dalvand Y, Askari H. Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World Journal of Microbiology and Biotechnology. 2012;28(4):1503–9. - 86.
Ahemad M, Kibret M. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. Journal of King Saud University-Science. 2014;26(1):1–20. - 87.
Selvakumar G, Kundu S, Gupta AD, Shouche YS, Gupta HS. Isolation and characterization of nonrhizobial plant growth promoting bacteria from nodules of Kudzu (Pueraria thunbergiana) and their effect on wheat seedling growth. Current microbiology. 2008;56(2):134–9. - 88.
Fatima Z, Saleemi M, Zia M, Sultan T, Aslam M, Rehman R, et al. Antifungal activity of plant growth-promoting rhizobacteria isolates against Rhizoctonia solani in wheat. African Journal of Biotechnology. 2009;8(2). - 89.
Ali B, Sabri AN, Hasnain S. Rhizobacterial potential to alter auxin content and growth of Vigna radiata (L.). World Journal of Microbiology and Biotechnology. 2010;26(8):1379–84. - 90.
Kudoyarova GR, Melentiev AI, Martynenko EV, Timergalina LN, Arkhipova TN, Shendel GV, et al. Cytokinin producing bacteria stimulate amino acid deposition by wheat roots. Plant Physiology and Biochemistry. 2014;83:285–91. - 91.
Arkhipova T, Prinsen E, Veselov S, Martinenko E, Melentiev A, Kudoyarova G. Cytokinin producing bacteria enhance plant growth in drying soil. Plant and Soil. 2007;292(1–2):305–15. - 92.
Arkhipova T, Veselov S, Melentiev A, Martynenko E, Kudoyarova G. Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant and Soil. 2005;272(1–2):201–9. - 93.
Kuz'mina LY, Melent'ev A. The effect of seed bacterization by Bacillus Cohn bacteria on their colonization of the spring wheat rhizosphere. Microbiology. 2003;72(2):230–5. - 94.
Peng YL, Gao ZW, Gao Y, Liu GF, Sheng LX, Wang DL. Eco‐physiological characteristics of Alfalfa seedlings in response to various mixed salt‐alkaline stresses. Journal of Integrative Plant Biology. 2008;50(1):29–39. - 95.
Zarea M, Hajinia S, Karimi N, Goltapeh EM, Rejali F, Varma A. Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biology and Biochemistry. 2012;45:139–46. - 96.
Bashan Y. Interactions of Azospirillum spp. in soils: a review. Biology and Fertility of Soils. 1999;29(3):246–56. - 97.
Upadhyay SK, Singh JS, Saxena AK, Singh DP. Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biology. 2012;14(4):605–11. - 98.
Ali SZ, Sandhya V, Grover M, Linga VR, Bandi V. 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. 2011;6(4):239–46. - 99.
Yegorenkova I, Konnova S, Sachuk V, Ignatov V. Azospirillum brasilense colonisation of wheat roots and the role of lectin–carbohydrate interactions in bacterial adsorption and root-hair deformation. Plant and Soil. 2001;231(2):275–82. - 100.
Sarode P, Rane M, Kadam M, Chincholkar S. Role of Microbial Siderophores in Improving Crop Productivity in Wheat. Bacteria in Agrobiology: Crop Productivity: Springer; 2013. pp. 287–308. - 101.
Scavino AF, Pedraza RO. The role of siderophores in plant growth-promoting bacteria. Bacteria in Agrobiology: Crop Productivity: Springer; 2013. pp. 265–85. - 102.
Sharma SK, Johri BN, Ramesh A, Joshi OP, Prasad SS. Selection of plant growth-promoting Pseudomonas spp. that enhanced productivity of soybean-wheat cropping system in central India. Journal of Microbiology and Biotechnology. 2011;21:1127–42. - 103.
Rroço E, Kosegarten H, Harizaj F, Imani J, Mengel K. The importance of soil microbial activity for the supply of iron to sorghum and rape. European Journal of Agronomy. 2003;19(4):487–93. - 104.
Jankiewicz U. Synthesis of siderophores by soil bacteria of the genus Pseudomonas under various culture conditions. Acta Scientiarum Polonorum Agricultura. 2006;5(2). - 105.
Mishra PK, Bisht SC, Ruwari P, Selvakumar G, Joshi GK, Bisht JK, et al. Alleviation of cold stress in inoculated wheat (Triticum aestivum L.) seedlings with psychrotolerant Pseudomonads from NW Himalayas. Archives of Microbiology. 2011;193(7):497–513. - 106.
Sarode Prashant D, Rane Makarand R, Chaudhari Bhushan L, Chincholkar Sudhir B. Siderophoregenic Acinetobacter calcoaceticus isolated from wheat rhizosphere with strong PGPR activity. Malaysian Journal of Microbiology. 2009;5(1):6–12. - 107.
Khodair T, Galal GF, El-Tayeb T. Effect of inoculating wheat seedlings with exopolysaccharide-producing bacteria in saline soil. Journal of Applied Sciences Research. 2008;4:2065–70. - 108.
Sandhya V, Grover M, Reddy G, Venkateswarlu B. Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biology and Fertility of Soils. 2009;46(1):17–26. - 109.
Amellal N, Bartoli F, Villemin G, Talouizte A, Heulin T. Effects of inoculation of EPS-producing Pantoea agglomerans on wheat rhizosphere aggregation. Plant and Soil. 1999;211(1):93–101. - 110.
Lucy M, Reed E, Glick BR. Applications of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek. 2004;86(1):1–25. - 111.
Canbolat MY, Bilen S, Çakmakçı R, Şahin F, Aydın A. Effect of plant growth-promoting bacteria and soil compaction on barley seedling growth, nutrient uptake, soil properties and rhizosphere microflora. Biology and Fertility of Soils. 2006;42(4):350–7. - 112.
Panwar J, Singh O. Response of Azospirillum and Bacillus on growth and yield of wheat under field conditions. Indian Journal of Plant Physiology. 2000;5(1):108–10. - 113.
Narula N, Remus R, Deubel A, Granse A, Dudeja S, Behl R, et al. Comparison of the effectiveness of wheat roots colonization by Azotobacter chroococcum and Pantoea agglomerans using serological techniques. Plant Soil and Environment. 2007;53(4):167. - 114.
Kumar V, Narula N. Solubilization of inorganic phosphates and growth emergence of wheat as affected by Azotobacter chroococcum mutants. Biology and Fertility of Soils. 1999;28(3):301–5. - 115.
Kumar V, Behl RK, Narula N. Establishment of phosphate-solubilizing strains of Azotobacter chroococcum in the rhizosphere and their effect on wheat cultivars under green house conditions. Microbiological Research. 2001;156(1):87–93. - 116.
Narula N, Kumar V, Behl RK, Deubel A, Gransee A, Merbach W. Effect of P‐solubilizing Azotobacter chroococcum on N, P, K uptake in P‐responsive wheat genotypes grown under greenhouse conditions. Journal of Plant Nutrition and Soil Science. 2000;163(4):393–8. - 117.
Singh R, Behl R, Jain P, Narula N, Singh K. Performance and gene effects for root characters and micronutrient uptake in wheat inoculated with arbuscular mycorrhizal fungi and Azotobacter chroococcum. Acta Agronomica Hungarica. 2007;55(3):325–30. - 118.
Khan MS, Zaidi A. Synergistic effects of the inoculation with plant growth-promoting rhizobacteria and an arbuscular mycorrhizal fungus on the performance of wheat. Turkish Journal of Agriculture and Forestry. 2007;31(6):355–62. - 119.
Zaidi A, Khan S. Interactive effect of rhizotrophic microorganisms on growth, yield, and nutrient uptake of wheat. Journal of Plant Nutrition. 2005;28(12):2079–92. - 120.
Abbasi M, Yousra M. Synergistic effects of biofertilizer with organic and chemical N sources in improving soil nutrient status and increasing growth and yield of wheat grown under greenhouse conditions. Plant Biosystems-An International Journal Dealing with all Aspects of Plant Biology. 2012;146(sup1):181–9. - 121.
Oliveira Ad, Urquiaga S, Döbereiner J, Baldani J, Omar M, Hamouda A, et al. Evaluating the efficiency of inoculating some diazotrophs on yield and protein content of 3 wheat cultivars under graded levels of nitrogen fertilization. Plant and Soil. 2002;242(2):205–15. - 122.
Yasin M, El-Mehdawi AF, Anwar A, Pilon-Smits EA, Faisal M. Microbial-enhanced selenium and iron biofortification of wheat (Triticum aestivum L.)-applications in phytoremediation and biofortification. International Journal of Phytoremediation. 2015;17(4):341–7. - 123.
Cakmak I, Pfeiffer WH, McClafferty B. Review: biofortification of durum wheat with zinc and iron. Cereal Chemistry. 2010;87(1):10–20. - 124.
Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnology Advances. 2014;32(2):429–48. - 125.
Egamberdieva D, Kucharova Z. Selection for root colonising bacteria stimulating wheat growth in saline soils. Biology and Fertility of Soils. 2009;45(6):563–71. - 126.
Bacilio M, Rodriguez H, Moreno M, Hernandez J-P, Bashan Y. Mitigation of salt stress in wheat seedlings by a gfp-tagged Azospirillum lipoferum. Biology and Fertility of Soils. 2004;40(3):188–93. - 127.
Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP, et al. Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stresses. Journal of Plant Growth Regulation. 2016;35(1):276–300. - 128.
Nabti E, Sahnoune M, Ghoul M, Fischer D, Hofmann A, Rothballer M, et al. Restoration of growth of durum wheat (Triticum durum var. waha) under saline conditions due to inoculation with the rhizosphere bacterium Azospirillum brasilense NH and extracts of the marine alga Ulva lactuca. Journal of Plant Growth Regulation. 2010;29(1):6–22. - 129.
El-Daim IAA, Bejai S, Meijer J. Improved heat stress tolerance of wheat seedlings by bacterial seed treatment. Plant and Soil. 2014;379(1–2):337–50. - 130.
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S. Plant drought stress: effects, mechanisms and management. Sustainable agriculture: Springer; 2009. pp. 153–88. - 131.
Pereyra M, Garcia P, Colabelli M, Barassi C, Creus C. A better water status in wheat seedlings induced by Azospirillum under osmotic stress is related to morphological changes in xylem vessels of the coleoptile. Applied Soil Ecology. 2012;53:94–7. - 132.
Alvarez M, Sueldo R, Barassi C. Effect of Azospirillum on coleoptile growth in wheat seedlings under water stress. Cereal Research Communications. 1996, 24 (1):101–107. - 133.
Díaz-Zorita M, Fernández-Canigia MV. Field performance of a liquid formulation of Azospirillum brasilense on dryland wheat productivity. European Journal of Soil Biology. 2009;45(1):3–11. - 134.
Arzanesh MH, Alikhani H, Khavazi K, Rahimian H, Miransari M. Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World Journal of Microbiology and Biotechnology. 2011;27(2):197–205. - 135.
Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A. Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regulation. 2014;73(2):121–31. - 136.
Khalafallah AA, Abo-Ghalia HH. 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. 2008;4(5):559–69. - 137.
Chakraborty U, Chakraborty B, Chakraborty A, Dey P. Water stress amelioration and plant growth promotion in wheat plants by osmotic stress tolerant bacteria. World Journal of Microbiology and Biotechnology. 2013;29(5):789–803. - 138.
Raheem A, Ali B. Halotolerant rhizobacteria: beneficial plant metabolites and growth enhancement of Triticum aestivum L. in salt-amended soils. Archives of Agronomy and Soil Science. 2015;61(12):1691–705. - 139.
Shrivastava P, Kumar R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Sciences. 2015;22(2):123–31. - 140.
Tiwari S, Singh P, Tiwari R, Meena KK, Yandigeri M, Singh DP, 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. 2011;47(8):907–16. - 141.
Tabatabaei S, Ehsanzadeh P. Comparative response of a hulled and a free-threshing tetraploid wheat to plant growth promoting bacteria and saline irrigation water. Acta Physiologiae Plantarum. 2016;38(1):1–17. - 142.
Zahir ZA, Ghani U, Naveed M, Nadeem SM, Asghar HN. Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for improving growth and yield of wheat ( Triticum aestivum L.) under salt-stressed conditions. Archives of Microbiology. 2009;191(5):415–24. - 143.
Abbaspoor A, Zabihi HR, Movafegh S, Asl MA. 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. 2009;3(4):824–8. - 144.
Nia SH, Zarea MJ, Rejali F, Varma A. Yield and yield components of wheat as affected by salinity and inoculation with Azospirillum strains from saline or non-saline soil. Journal of the Saudi Society of Agricultural Sciences. 2012;11(2):113–21. - 145.
Freitas JRd, Germida JJ. Plant growth promoting rhizobacteria for winter wheat. Canadian Journal of Microbiology. 1990;36(4):265–72. - 146.
Sun X, Griffith M, Pasternak J, Glick BR. Low temperature growth, freezing survival, and production of antifreeze protein by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Canadian Journal of Microbiology. 1995;41(9):776–84. - 147.
Xu H, Griffith M, Patten CL, Glick BR. Isolation and characterization of an antifreeze protein with ice nucleation activity from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Canadian Journal of Microbiology. 1998;44(1):64–73. - 148.
Mishra PK, Mishra S, Selvakumar G, Bisht SC, Bisht JK, Kundu S, et al. Characterisation of a psychrotolerant plant growth promoting Pseudomonas sp. strain PGERs17 (MTCC 9000) isolated from North Western Indian Himalayas. Annals of Microbiology. 2008;58(4):561–8. - 149.
Turan M, Güllüce M, Çakmak R, Şahin F. Effect of plant growth-promoting rhizobacteria strain on freezing injury and antioxidant enzyme activity of wheat and barley. Journal of Plant Nutrition. 2013;36(5):731–48. - 150.
Tica D, Udovic M, Lestan D. Immobilization of potentially toxic metals using different soil amendments. Chemosphere. 2011;85(4):577–83. - 151.
Kumar V, Singh S, Singh J, Upadhyay N. Potential of plant growth promoting traits by bacteria isolated from heavy metal contaminated soils. Bulletin of Environmental Contamination and Toxicology. 2015;94(6):807–14. - 152.
Hasnain S, Sabri AN. Growth stimulation of Triticum aestivum seedlings under Cr-stresses by non-rhizospheric pseudomonad strains. Environmental Pollution. 1997;97(3):265–73. - 153.
Shahzadi I, Khalid A, Mahmood S, Arshad M, Mahmood T, Aziz I. Effect of bacteria containing ACC deaminase on growth of wheat seedlings grown with chromium contaminated water. Pakistan Journal of Botany. 2013;45:487–94. - 154.
Jamali MK, Kazi TG, Arain MB, Afridi HI, Jalbani N, Kandhro GA, et al. Heavy metal accumulation in different varieties of wheat ( Triticum aestivum L.) grown in soil amended with domestic sewage sludge. Journal of Hazardous Materials. 2009;164(2):1386–91. - 155.
Hassan W, Bashir S, Ali F, Ijaz M, Hussain M, David J. Role of ACC-deaminase and/or nitrogen fixing rhizobacteria in growth promotion of wheat ( Triticum aestivum L.) under cadmium pollution. Environmental Earth Sciences. 2016;75(3):1–14. - 156.
Singh Y, Ramteke P, Shukla PK. Isolation and characterization of heavy metal resistant Pseudomonas spp. and their plant growth promoting activities. Advances in Applied Sciences Research 2013;4:269–72. - 157.
Barakat M. New trends in removing heavy metals from industrial wastewater. Arabian Journal of Chemistry. 2011;4(4):361–77. - 158.
Dell’Amico E, Cavalca L, Andreoni V. Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biology and Biochemistry. 2008;40(1):74–84. - 159.
Govindasamy V, Senthilkumar M, Annapurna K. Effect of mustard rhizobacteria on wheat growth promotion under cadmium stress: characterization of acdS gene coding ACC deaminase. Annals of Microbiology. 2015;65(3):1679–87. - 160.
Abaid-Ullah M, Hassan MN, Jamil M, Brader G, Shah MKN, Sessitsch A, et al. Plant growth promoting rhizobacteria: an alternate way to improve yield and quality of wheat ( Triticum aestivum ). International Journal of Agriculture and Biology. 2015;17:51–60. - 161.
Rana A, Joshi M, Prasanna R, Shivay YS, Nain L. Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. European Journal of Soil Biology. 2012;50:118–26. - 162.
Roesti D, Gaur R, Johri B, Imfeld G, Sharma S, Kawaljeet K, et al. Plant growth stage, fertiliser management and bio-inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields. Soil Biology and Biochemistry. 2006;38(5):1111–20. - 163.
Mäder P, Kaiser F, Adholeya A, Singh R, Uppal HS, Sharma AK, et al. Inoculation of root microorganisms for sustainable wheat–rice and wheat–black gram rotations in India. Soil Biology and Biochemistry. 2011;43(3):609–19. - 164.
Saubidet MI, Fatta N, Barneix AJ. The effect of inoculation with Azospirillum brasilense on growth and nitrogen utilization by wheat plants. Plant and Soil. 2002;245(2):215–22. - 165.
Cáceres ER, Anta GG, Lopez J, Ciocco CD, Basurco JP, Parada J. Response of field‐grown wheat to inoculation with Azospirillum brasilense andBacillus polymyxa in the semiarid region of Argentina. Arid Land Research and Management. 1996;10(1):13–20. - 166.
Rosas SB, Avanzini G, Carlier E, Pasluosta C, Pastor N, Rovera M. Root colonization and growth promotion of wheat and maize by Pseudomonas aurantiaca SR1. Soil Biology and Biochemistry. 2009;41(9):1802–6. - 167.
Shaharoona B, Naveed M, Arshad M, Zahir ZA. Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat ( Triticum aestivum L.). Applied Microbiology and Biotechnology. 2008;79(1):147–55. - 168.
Majeed A, Abbasi MK, Hameed S, Imran A, Rahim N. Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Frontiers in Microbiology. 2015;6:198. - 169.
Mehboob I, Zahir ZA, Arshad M, Tanveer A, Azam F. Growth promoting activities of different Rhizobium spp. in wheat. Pakistan Journal of Botany. 2011;43(3):1643–50. - 170.
Ozturk A, Caglar O, Sahin F. Yield response of wheat and barley to inoculation of plant growth promoting rhizobacteria at various levels of nitrogen fertilization. Journal of Plant Nutrition and Soil Science. 2003;166(2):262–6. - 171.
Turan M, Gulluce M, Şahin F. 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. 2012;43(12):1658–73. - 172.
Barneix A, Saubidet M, Fatta N, Kade M. Effect of rhizobacteria on growth and grain protein in wheat. Agronomy for Sustainable Development. 2005;25(4):505–11. - 173.
Trabelsi D, Mhamdi R. Microbial inoculants and their impact on soil microbial communities: a review. BioMed Research International. 2013. - 174.
Belimov A, Kojemiakov A, Chuvarliyeva Cn. Interaction between barley and mixed cultures of nitrogen fixing and phosphate-solubilizing bacteria. Plant and Soil. 1995;173(1):29–37. - 175.
Combes-Meynet E, Pothier JF, Moënne-Loccoz Y, Prigent-Combaret C. The Pseudomonas secondary metabolite 2, 4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Molecular Plant-Microbe Interactions. 2011;24(2):271–84. - 176.
Galal Y, El-Ghandour I, El-Akel E. Stimulation of wheat growth and N fixation through Azospirillum and Rhizobium inoculation: a field trial with 15N techniques. Plant Nutrition: Springer; 2001. pp. 666–7. - 177.
Swarnalakshmi K, Prasanna R, Kumar A, Pattnaik S, Chakravarty K, Shivay YS, et al. Evaluating the influence of novel cyanobacterial biofilmed biofertilizers on soil fertility and plant nutrition in wheat. European Journal of Soil Biology. 2013;55:107–16. - 178.
Nain L, Rana A, Joshi M, Jadhav SD, Kumar D, Shivay Y, et al. Evaluation of synergistic effects of bacterial and cyanobacterial strains as biofertilizers for wheat. Plant and Soil. 2010;331(1–2):217–30. - 179.
Manjunath M, Prasanna R, Sharma P, Nain L, Singh R. Developing PGPR consortia using novel genera Providencia and Alcaligenes along with cyanobacteria for wheat. Archives of Agronomy and Soil Science. 2011;57(8):873–87. - 180.
Minaxi J, Chandra S, Nain L. Synergistic effect of phosphate solubilizing rhizobacteria and arbuscular mycorrhiza on growth and yield of wheat plants Journal of Soil Science and Plant Nutrition, 2013, 13 (2), 511-525. - 181.
Kumar A, Maurya B, Raghuwanshi R. Isolation and characterization of PGPR and their effect on growth, yield and nutrient content in wheat (Triticum aestivum L.). Biocatalysis and Agricultural Biotechnology. 2014;3(4):121–8. - 182.
Baris O, Sahin F, Turan M, Orhan F, Gulluce M. Use of plant-growth-promoting rhizobacteria (PGPR) seed inoculation as alternative fertilizer inputs in wheat and barley production. Communications in Soil Science and Plant Analysis. 2014;45(18):2457–67. - 183.
Afzal A, Saleem S, Iqbal Z, Jan G, Malik MFA, Asad SA. Interaction of Rhizobium and Pseudomonas with Wheat ( Triticum Aestivum L.) in Potted Soil with or Without P2O5. Journal of Plant Nutrition. 2014;37(13):2144–56. - 184.
Bulut S. Evaluation of efficiency parameters of phosphorous-solubilizing and N-fixing bacteria inoculations in wheat ( Triticum aestivum L.). Turkish Journal of Agriculture and Forestry. 2013;37(6):734–43. - 185.
Afzal A, Bano A. Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat ( Triticum aestivum ). International Journal of Agriculture and Biology. 2008;10:85–8. - 186.
Germida J, Walley F. Plant growth-promoting rhizobacteria alter rooting patterns and arbuscular mycorrhizal fungi colonization of field-grown spring wheat. Biology and Fertility of Soils. 1996;23(2):113–20. - 187.
Bahrani A, Pourreza J, Joo MH. Response of Winter Wheat to Co-Inoculation with Azotobacter and Arbescular Mycorrhizal Fungi (AMF) under different sources of nitrogen fertilizer. American-Eurasian Journal of Agricultural & Environmental Sciences. 2010;9(4):376–84. - 188.
Germida J, Siciliano S. Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biology and Fertility of Soils. 2001;33(5):410–5. - 189.
Marschner P, Crowley D, Yang CH. Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant and Soil. 2004;261(1–2):199–208. - 190.
Kant C, Aydin A, Turan M, Huang YM. Mitigation of N and P leaching from irrigated wheat area as influence plant growth promoting rhizobacteria (PGPR). Romanian Biotechnological Letters. 2010;15(6):5754–63. - 191.
Fischer SE, Fischer SI, Magris S, Mori GB. Isolation and characterization of bacteria from the rhizosphere of wheat. World Journal of Microbiology and Biotechnology. 2007;23(7):895–903. - 192.
Sabry SR, Saleh SA, Batchelor CA, Jones J, Jotham J, Webster G, et al. Endophytic establishment of Azorhizobium caulinodans in wheat. Proceedings of the Royal Society of London B: Biological Sciences. 1997;264(1380):341–6. - 193.
Singh N, Chaudhary F, Patel D. Effectiveness of Azotobacter bio-inoculant for wheat grown under dryland condition. Journal of Environmental Biology. 2013;34(5):927. - 194.
Narula N, Kumar V, Singh B, Bhatia R, Lakshminarayana K. Impact of biofertilizers on grain yield in spring wheat under varying fertility conditions and wheat-cotton rotation. Archives of Agronomy and Soil Science. 2005;51(1):79–89. - 195.
Ali SM, Hamza MA, Amin G, Fayez M, El-Tahan M, Monib M, et al. Production of biofertilizers using baker's yeast effluent and their application to wheat and barley grown in north Sinai deserts: (Produktion von Biodüngern unter Verwendung von Backhefeabwasser und ihre Anwendung zu Weizen-und Gerstenanbau im Norden der Sinai-Wüste). Archives of Agronomy and Soil Science. 2005;51(6):589–604. - 196.
Mertens T, Hess D. Yield increases in spring wheat ( Triticum aestivum L.) inoculated withAzospirillum lipoferum under greenhouse and field conditions of a temperate region. Plant and Soil. 1984;82(1):87–99. - 197.
Bashan Y, Holguin G, De-Bashan LE. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Canadian Journal of Microbiology. 2004;50(8):521–77. - 198.
Wang H, Xu R, You L, Zhong G. Characterization of Cu-tolerant bacteria and definition of their role in promotion of growth, Cu accumulation and reduction of Cu toxicity in Triticum aestivum L. Ecotoxicology and Environmental Safety. 2013;94:1–7. - 199.
Pereyra M, Zalazar C, Barassi C. Root phospholipids in Azospirillum-inoculated wheat seedlings exposed to water stress. Plant Physiology and Biochemistry. 2006;44(11):873–9. - 200.
Creus CM, Sueldo RJ, Barassi CA. Water relations in Azospirillum-inoculated wheat seedlings under osmotic stress. Canadian Journal of Botany. 1998;76(2):238–44. - 201.
Mishra PK, Mishra S, Bisht SC, Selvakumar G, Kundu S, Bisht J, et al. Isolation, molecular characterization and growth-promotion activities of a cold tolerant bacterium Pseudomonas sp. NARs9 (MTCC9002) from the Indian Himalayas. Biological Research. 2009;42(3):305–13. - 202.
Abd-Alla MH, El-Sayed E-SA, Rasmey A-HM. Indole-3-acetic acid (IAA) production by Streptomyces atrovirens isolated from rhizospheric soil in Egypt. Journal of Biology and Earth Sciences. 2013;3(2):B182–B93. - 203.
Egamberdiyeva D, Höflich G. Influence of growth-promoting bacteria on the growth of wheat in different soils and temperatures. Soil Biology and Biochemistry. 2003;35(7):973–8. - 204.
Nadeem SM, Zahir ZA, Naveed M, Asghar HN, Arshad M. Rhizobacteria capable of producing ACC-deaminase may mitigate salt stress in wheat. Soil Science Society of America Journal. 2010;74(2):533–42. - 205.
Nadeem SM, Zahir ZA, Naveed M, Nawaz S. Mitigation of salinity-induced negative impact on the growth and yield of wheat by plant growth-promoting rhizobacteria in naturally saline conditions. Annals of Microbiology. 2013;63(1):225–32. - 206.
Barbieri P, Galli E. Effect on wheat root development of inoculation with an Azospirillum brasilense mutant with altered indole-3-acetic acid production. Research in Microbiology. 1993;144(1):69–75. - 207.
Obreht Z, Kerby NW, Gantar M, Rowell P. Effects of root-associated N2-fixing cyanobacteria on the growth and nitrogen content of wheat ( Triticum vulgare L.) seedlings. Biology and Fertility of Soils. 1993;15(1):68–72. - 208.
Timmusk S, Nicander B, Granhall U, Tillberg E. Cytokinin production by Paenibacillus polymyxa. Soil Biology and Biochemistry. 1999;31(13):1847–52. - 209.
Alen’kina S, Payusova O, Nikitina V. Effect of Azospirillum lectins on the activities of wheat-root hydrolytic enzymes. Plant and Soil. 2006;283(1–2):147–51. - 210.
Egamberdiyeva D. Plant‐growth‐promoting rhizobacteria isolated from a Calcisol in a semi‐arid region of Uzbekistan: biochemical characterization and effectiveness. Journal of Plant Nutrition and Soil Science. 2005;168(1):94–9. - 211.
Kızılkaya R. Yield response and nitrogen concentrations of spring wheat ( Triticum aestivum ) inoculated with Azotobacter chroococcum strains. Ecological Engineering. 2008;33(2):150–6. - 212.
Hassen AI, Labuschagne N. Root colonization and growth enhancement in wheat and tomato by rhizobacteria isolated from the rhizoplane of grasses. World Journal of Microbiology and Biotechnology. 2010;26(10):1837–46. - 213.
El-Razek UA, El-Sheshtawy A. Response of some wheat varieties to bio and mineral nitrogen fertilizers. Asian Journal of Crop Science. 2013;5(2):200. - 214.
Schoebitz M, Ceballos C, Ciamp L. Effect of immobilized phosphate solubilizing bacteria on wheat growth and phosphate uptake. Journal of Soil Science and Plant Nutrition. 2013;13(1):1–10. - 215.
Magnucka EG, Pietr SJ. Various effects of fluorescent bacteria of the genus Pseudomonas containing ACC deaminase on wheat seedling growth. Microbiological Research. 2015;181:112–9. - 216.
Ogut M, Er F. Mineral composition of field grown winter wheat inoculated with phosphorus solubilizing bacteria at different plant growth stages. Journal of Plant Nutrition. 2016;39(4):479–90.