Biochemical and Proteomics Analysis of the Plant Growth-Promoting Rhizobacteria in Stress Conditions

  • Kalpna D. Rakholiya
  • Mital J. Kaneria
  • Satya P. Singh
  • V. D. Vora
  • G. S. Sutaria
Chapter
First Online:

Abstract

Among the emerging environmental threats of the twentieth century, the effect of biotic and abiotic stress on agricultural soils has been considered as one of the most alarming threats in both developed and developing countries. Among them, salt stress is a major problem, and cost associated with the salt salinity is potentially enormous affecting agriculture, food quality, safety, biodiversity, and environments. Several bacteria present in rhizosphere have great potential in improving crop production. Among these bacteria, plant growth-promoting rhizobacteria (PGPR) are the most important. PGPR are able to provide the plant with essential elements, ammonia, growth hormone, and hydrolytic enzymes helping against plant pathogens in salinity and improving soil fertility. The present review aims to establish the conception of the rhizospheric bacteria and to elucidate the mechanisms of rhizobacteria-mediated plant growth promotion. Recent tools available to analyze gene expression and metabolites under the larger umbrella of the genomics and proteomics will also be discussed.

Keywords

Plant growth-promoting rhizobacteria (PGPR) 1-Aminocyclopropane-1-carboxylic acid (ACC) Stress Rhizosphere Plant-microbe interaction 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We thank the Science and Engineering Research Board (SERB) for providing financial support under National Postdoctoral Fellowship (NPDF) scheme(File No. PDF/2015/000430/ LS, 06 June, 2016), Department of Science and Technology, New Delhi, India.

Conflicts of Interest

There is no conflict of interest.

References

  1. Adams J, Wright M, Wagner H, Valiente J, Britta D, Anderson A (2017) Cu from dissolution of CuO nanoparticles signals changes in root morphology. Plant Physiol Biochem 110:108–117CrossRefPubMedGoogle Scholar
  2. Agbodjato NA, Noumavo PA, Baba-Moussa F, Salami HA, Sina H, Sezan A, Bankolé H, Adjanohoun A, Baba-Moussa L (2015) Characterization of potential plant growth promoting rhizobacteria isolated from Maize (Zea mays L.) in Central and Northern Benin (West Africa). Appl Environ Soil Sci. doi: 10.1155/2015/901656
  3. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20CrossRefGoogle Scholar
  4. Ahmed E, Holmstrom SJM (2014) Siderophores in environmental research: roles and applications. J Microbial Biotechnol 7:196–208CrossRefGoogle Scholar
  5. Akhgar AR, Arzanlou M, Bakker PAHM, Hamidpour M (2014) Characterization of 1-Aminocyclopropane-1-Carboxylate (ACC) deaminase-containing Pseudomonas spp. in the rhizosphere of salt-stressed canola. Pedosphere 24:461–468CrossRefGoogle Scholar
  6. Anatala TJ, Gajera HP, Mandavia MK, Dave RA, Kothari VV, Golakiya BA (2015) Leaf proteome alterations in tolerant pearl millet (Pennisetum glaucum L.) genotype under water stress. Int J Agric Environ Biotechnol 8:539–549CrossRefGoogle Scholar
  7. Azarmi F, Mozaffari V, Hamidpour M, Abbaszadeh-Dahaji P (2016) Interactive effect of fluorescent Pseudomonads rhizobacteria and Zn on the growth, chemical composition, and water relations of Pistachio (Pistacia vera L.) seedlings under NaCl stress. Commun Soil Sci Plant Anal 47:955–972CrossRefGoogle Scholar
  8. Baig KS, Arshad M, Khalid A, Hussain S, Abbas MN, Imran M (2014) Improving growth and yield of maize through bioinoculants carrying auxin production and phosphate solubilizing activity. Soil Environ 33:159–168Google Scholar
  9. Banaei-Asl F, Bandehagh A, Uliaei ED, Farajzadeh D, Sakata K, Mustafa G, Komatsu S (2015) Proteomic analysis of canola root inoculated with bacteria under salt stress. J Proteomics 124:88–111Google Scholar
  10. Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051CrossRefPubMedPubMedCentralGoogle Scholar
  11. Boiero L, Perrig D, Masciarelli O, Penna C, Cassán F, Luna V (2006) Phytohormone production by three strains of Bradyrhizobium japonicum, and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880Google Scholar
  12. Bose A, Kher MM, Nataraj M, Keharia H (2016) Phytostimulatory effect of indole-3-acetic acid by Enterobacter cloacae SN19 isolated from Teramnus labialis (L. f.) Spreng rhizosphere. Biocatal Agric Biotechnol 6:128–137Google Scholar
  13. Chakraborty U, Roy S, Chakraborty AP, Dey P, Chakraborty B (2011) Plant growth promotion and amelioration of salinity stress in crop plants by a salt-tolerant bacterium. Recent Res Sci Technol 3:61–70Google Scholar
  14. Dinesh R, Anandaraj M, Kumar A, Bini YK, Subila KP, Aravind R (2015) Isolation, characterization, and evaluation of multi-trait plant growth promoting rhizobacteria for their growth promoting and disease suppressing effects on ginger. Microbiol Res 173:34–43CrossRefPubMedGoogle Scholar
  15. Dodd IC, Perez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63:3415–3428CrossRefPubMedGoogle Scholar
  16. Egamberdieva D, Egamberdieva Z (2009) Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45:563–571CrossRefGoogle Scholar
  17. Egamberdieva D, Kamilova F, Validov S, Gafurova L, Kucharova Z, Lugtenberg B (2008) High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environ Microbiol 10:1–9PubMedGoogle Scholar
  18. Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189CrossRefGoogle Scholar
  19. English MM, Coulson TJD, Horsman SR, Patten CL (2010) Overexpression of hns in the plant growth-promoting bacterium Enterobacter cloacae UW5 increases root colonization. J Appl Microbiol 108:2180–2190PubMedGoogle Scholar
  20. Fan B, Li Y, Li L, Peng X, Bu C, Wu X, Borriss R (2017) Malonylome analysis of rhizobacterium Bacillus amyloliquefaciens FZB42 reveals involvement of lysine malonylation in polyketide synthesis and plant-bacteria interactions. J Proteomics 154:1–12Google Scholar
  21. Gamalero E, Marzachi C, Galetto L, Veratti F, Massa N, Bona E, Novello G, Glick BR, Ali S, Cantamessa S, D’Agostino G, Berta G (2016) An 1-Aminocyclopropane-1-carboxylate (ACC) deaminase-expressing endophyte increases plant resistance to flavescencedoree phytoplasma infection. Plant Biosyst. doi: 10.1080/11263504.2016.1174172
  22. Ghosh U, Subhashini P, Dilipan E, Raja S, Thangaradjou T, Kannan L (2012) Bacteria from seagrass rhizosphere soil. J Ocean Univ China 11:86–92CrossRefGoogle Scholar
  23. Glick R, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242CrossRefGoogle Scholar
  24. Godino A, Principe A, Fischer S (2016) A ptsP deficiency in PGPR Pseudomonas fluorescens SF39a affects bacteriocin production and bacterial fitness in the wheat rhizosphere. Res Microbiol 167:178–189CrossRefPubMedGoogle Scholar
  25. Gontia-Mishra I, Sasidharan S, Tiwari S (2014) Recent developments in use of 1-aminocyclopropane-1-carboxylate (ACC) deaminase for conferring tolerance to biotic and abiotic stress. Biotechnol Lett doi:  10.1007/s10529-014-1458-9
  26. Gontia-Mishra I, Sapre S, Sharma A, Tiwari S (2016) Alleviation of mercury toxicity in wheat by the interaction of mercury-tolerant plant growthpromoting rhizobacteria. J Plant Growth Regul. doi:  10.1007/s00344-016-9598-x
  27. Goswami D, Dhandhukia P, Patel P, Thakker JN (2014) Screening of PGPR from saline desert of Kutch: growth promotion in Arachis hypogea by Bacillus licheniformis A2. Microbiol Res 169:66–75CrossRefPubMedGoogle Scholar
  28. Gouffi K, Blanco C (2000) Is the accumulation of osmoprotectant the unique mechanism involved in bacterial osmoprotection? Int J Food Microbiol 55:171–174CrossRefPubMedGoogle Scholar
  29. Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240CrossRefGoogle Scholar
  30. Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7:096–102Google Scholar
  31. Gururani MA, Upadhyaya CP, Baskar V, Venkatesh J, Nookaraju A, Park AW (2012) Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ros-scavenging enzymes and improved photosynthetic performance. J Plant Growth Regul. doi: 10.1007/s00344-012-9292-6
  32. Habib SH, Kausar H, Saud HM, Ismail MR, Othman R (2015) Molecular characterization of stress tolerant plant growth promoting rhizobacteria (PGPR) for growth enhancement of rice. Int J Agric Biol. doi: 10.17957/IJAB/15.0094
  33. Han Y, Wang R, Yang Z, Zhan Y, Ma Y, Ping S, Zhang L, Lin M, Yan Y (2015) 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas stutzeri A1501 facilitates the growth of rice in the presence of salt or heavy metals. J Microbiol Biotechnol 25:1119–1128CrossRefPubMedGoogle Scholar
  34. Hassan W, Bashir S, Ali F, Ijaz M, Hussain M, David J (2016) Role of ACC-deaminase and/or nitrogen fixing rhizobacteria in growth promotion of wheat (Triticum aestivum L.) under cadmium pollution. Environ Earth Sci 75:267CrossRefGoogle Scholar
  35. Hiltner L (1904) Uber neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter besonderer Berucksichtigung der Gründüngung und Brache. Arb Landwirtsch Ges 98:59–78Google Scholar
  36. Ibekwe AM, Poss JA, Grattan SR, Grieve CM, Suarez D (2010) Bacterial diversity in cucumber (Cucumis sativus) rhizosphere in response to salinity, soil pH, and boron. Soil Biol Biochem 42:567–575CrossRefGoogle Scholar
  37. Jing Y, He Z, Yang X (2007) Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J Zhejiang Univ Sci B 8:192–207CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kandasamy S, Loganathan K, Muthuraj R, Duraisamy S, Seetharaman S, Thiruvengadam R, Ponnusamy B, Ramasamy S (2009) Understanding the molecular basis of plant growth promotional effect of Pseudomonas fluorescens on rice through protein profiling. Proteome Sci 7:47Google Scholar
  39. Kavamura VN, Santos SN, da Silva JL, Parma MM, Avila LA, Visconti A, Zucchi TD, Taketani RG, Andreote FD, de Melo IS (2013) Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol Res 168:183–191CrossRefPubMedGoogle Scholar
  40. Kloepper JW, Beauchamp CJ (1992) A review of issues related to measuring colonization of plant roots by bacteria. Can J Microbiol 38:1219–1232CrossRefGoogle Scholar
  41. Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free living bacterial inocula for enhancing crop productivity. Trends Biotechnol 7:39–44CrossRefGoogle Scholar
  42. Kumar P, Dubey RC, Maheshwari DK (2012) Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiol Res 167:493–499CrossRefPubMedGoogle Scholar
  43. Kumar P, Dubey RC, Maheshwari DK, Park Y, Bajpai VK (2016) Isolation of plant growth-promoting Pseudomonas sp. PPR 8 from the rhizosphere of Phaseolus vulgaris L. Arch Biol Sci 68:363–374CrossRefGoogle Scholar
  44. Kuppusamy S, Thavamani P, Venkateswarlu K, Lee YB, Naidu R, Megharaj M (2017) Remediation approaches for polycyclic aromatic hydrocarbons (PAHs) contaminated soils: technological constraints, emerging trends and future directions. Chemosphere 168:944–968CrossRefPubMedGoogle Scholar
  45. Kwon YS, Lee DY, Rakwal R, Baek SB, Lee JH, Kwak YS, Seo JS, Chung WS, Bae DW, Kim SG (2016) Proteomic analyses of the interaction between the plant-growth promoting rhizobacterium Paenibacillus polymyxa E681 and Arabidopsis thaliana. Proteomics 16:122–135Google Scholar
  46. Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant and Soil 321:83–115CrossRefGoogle Scholar
  47. Li Z, Chang S, Lin L, Li Y, An Q (2011) A colorimetric assay of 1-aminocyclopropane-1-carboxylate(ACC) based on ninhydrin reaction for rapid screening of bacteria containing ACC deaminase. Lett Appl Microbiol 53:178–185CrossRefPubMedGoogle Scholar
  48. Liu Z, Li YC, Zhang S, Fu Y, Fan X, Patel JS, Zhang M (2015) Characterization of phosphate-solubilizing bacteria isolated from calcareous soils. Appl Soil Ecol 96:217–224Google Scholar
  49. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572CrossRefPubMedGoogle Scholar
  50. Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663CrossRefPubMedGoogle Scholar
  51. Nadeem SM, Ahmad M, Naveed M, Imran M, Zahir ZA, Crowley DE (2016) Relationship between in vitro characterization and comparative efficacy of plant growth promoting rhizobacteria for improving cucumber salt tolerance. Arch Microbiol. doi: 10.1007/s00203-016-1197-5
  52. Nadeem SM, Shaharoona B, Arshad M, Crowley DE (2012) Population density and functional diversity of plant growth promoting rhizobacteria associated with avocado trees in saline soils. Appl Soil Ecol 62:147–154CrossRefGoogle Scholar
  53. Nakbanpote W, Panitlurtumpai N, Sangdee A, Sakulpone N, Sirisom P, Pimthong A (2014) Salt-tolerant and plant growth-promoting bacteria isolated from Zn/Cd contaminated soil: identification and effect on rice under saline conditions. J Plant Interact 9:379–387CrossRefGoogle Scholar
  54. Nascimento FX, Rossi MJ, Soares CRFS, McConkey BJ, Glick BR (2014) New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS One 9:99168CrossRefGoogle Scholar
  55. Natarajan A, Kumar K, Madhuri K, Usharani GK (2016) Isolation and characterization of salt tolerant plant growth promoting rhizobacteria from plants grown in Tsunami affected regions of Andaman and Nicobar Islands. Geomicrobiol J. doi: 10.1080/01490451.2015.1128994
  56. Noor R, Feroz F (2015) Requirements for microbiological quality management of the agricultural products. Nutr Food Sci 45:808–816CrossRefGoogle Scholar
  57. Oburger E, Schmidt H (2016) New methods to unravel rhizosphere processes. Trends Plant Sci 21:243–255CrossRefPubMedGoogle Scholar
  58. Pandey S, Rakholiya KD, Raval H, Singh SP (2012) Catalysis and stability of an alkaline protease from a haloalkaliphilic bacterium under non-aqueous conditions as a function of pH, salt and temperature. J Biosci Bioeng 114:251–256CrossRefPubMedGoogle Scholar
  59. Passari AK, Mishra VK, Gupta VK, Yadav MK, Saikia R, Singh BP (2016) In vitro and in vivo plant growth promoting activities and DNA fingerprinting of antagonistic endophytic actinomycetes associates with medicinal plants. PLOS One. doi:  10.1371/journal.pone.0139468
  60. Paul D (2013) Osmotic stress adaptations in rhizobacteria. J Basic Microbiol 53:101–110CrossRefPubMedGoogle Scholar
  61. Paul D, Nair S (2008) Stress adaptations in a plant growth promoting rhizobacterium [PGPR] with increasing salinity in the coastal agricultural soils. J Basic Microbiol 48:378–384CrossRefPubMedGoogle Scholar
  62. Perez-Montano F, Alías-Villegas C, Bellogín RA, del Cerro P, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336CrossRefPubMedGoogle Scholar
  63. Piccoli P, Bottini R (1994) Effects of C/N ratio, N-content, pH, and incubation time on growth and gibberellin production by Azospirillum lipoferum. Symbiosis 17:229–236Google Scholar
  64. Piromyou P, Noisangiam R, Uchiyama H, Tittabutr P, Boonkerd N, Teaumroong N (2013) Indigenous microbial community structure in rhizosphere of Chinese kale as affected by plant Growth-promoting rhizobacteria inoculation. Pedosphere 23:577–592CrossRefGoogle Scholar
  65. Pothier JF, Prigent-Combaret C, Haurat J, Menne-Loccoz Y, Wisniewski-Dye F (2008) Duplication of plasmidborne nitrite reductase gene nirK in the wheat-associated plant growth-promoting rhizobacterium Azospirillum brasilense Sp245. Mol Plant Microbe Interact 21:831–842Google Scholar
  66. Qin Y, Druzhinina IS, Pan X, Yuan Z (2016) Microbially mediated plant salt tolerance and microbiome-based solutions for saline agriculture. Biotechnol Adv 15:1245–1259CrossRefGoogle Scholar
  67. Qurashi AW, Sabri AN (2012) Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J Microbiol 43:1183–1191Google Scholar
  68. Ramadoss D, Lakkineni VK, Bose P, Ali S, Annapurna K (2013) Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats. SpringerPlus 2(1):6CrossRefPubMedPubMedCentralGoogle Scholar
  69. Rashedul IM, Madhaiyan M, DekaBoruah HP, Yim W, Lee G, Saravanan VS et al (2009) Characterization of plant growth-promoting traits of free-living diazotrophic bacteria and their inoculation effects on growth and nitrogen uptake of crop plants. Microbiol Biotechnol 19:1213–1222Google Scholar
  70. Reinhold-Hurek B, Bunger W, Burbano CS, Sabale M, Hurek T (2015) Roots shaping their microbiome: global hotspots for microbial activity. Annu Rev Phytopathol 53:403–424CrossRefPubMedGoogle Scholar
  71. Saha M, Maurya BR, Meena VS, Bahadur I, Kumar A (2016) Identification and characterization of potassium solubilizing bacteria (KSB) from Indo-Gangetic Plains of India. Biocatal Agric Biotechnol. doi: 10.1016/j.bcab.2016.06.007
  72. Saleem M, Moe LA (2014) Multitrophic microbial interactions foreco- and agro-biotechnological processes: theory and practice. Trends Biotechnol 32:529–537CrossRefPubMedGoogle Scholar
  73. Sandhya V, Ali SKZ, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol Fertil Soils 46:17–26CrossRefGoogle Scholar
  74. Scagliola M, Pii Y, Mimmo T, Cesco S, Ricciuti P, Crecchio C (2016) Characterization of plant growth promoting traits of bacterial isolates from the rhizosphere of barley (Hordeum vulgare L.) and tomato (Solanum lycopersicon L.) grown under Fe sufficiency and deficiency. Plant Physiol Biochem 107:187–196CrossRefPubMedGoogle Scholar
  75. Sharma R, Sharma P, Chauhan A, Walia A, Shirkot CK (2016) Plant growth promoting activities of rhizobacteria isolated from Podophyllum hexandrum growing in North-West regions of the Himalaya. Proc Natl Acad Sci India B Biol Sci. doi: 10.1007/s40011-016-0722-2
  76. Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131CrossRefPubMedGoogle Scholar
  77. Siddikee MA, Chauhan PS, Anandham R, Han G, Sa T (2010) Isolation, characterization, and use for plant growth promotion under salt stress, of ACC Deaminase-producing halotolerant bacteria derived from coastal soil. J Microbiol Biotechnol 20:1577–1584CrossRefPubMedGoogle Scholar
  78. Singh P, Singh P, Singh MP (2015a) Assessment of antifungal activity of PGPR (plant growth-promoting rhizobacterial) isolates against Rhizoctonia solani in wheat (Triticum aestivum L.) Int J Adv Res 3:803–812Google Scholar
  79. Singh RP, Jha P, Jha PN (2015b) The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J Plant Physiol 184:57–67CrossRefPubMedGoogle Scholar
  80. Singh Y, Lal N (2015) In vitro screening of salt tolerant bacillus from rhizosphere of tomato (Lycopersicon esculentum) showing plant growth promoting traits. Ind J Biol 2:55–60Google Scholar
  81. Soussi A, Ferjani R, Marasco R, Guesmi A, Cherif H, Rolli E, Mapelli F, Ouzari HI, Daffonchio D, Cherif A (2015) Plant-associated microbiomes in arid lands: diversity, ecology and biotechnological potential. Plant and Soil doi:  10.1007/s11104-015-2650-y
  82. Szymańska S, Piernik A, Baum C, Złoch M, Hrynkiewicz K (2014) Metabolic profiles of microorganisms associated with the halophyte Salicornia europaea in soils with different levels of salinity. Ecosci 21:114–122CrossRefGoogle Scholar
  83. Szymańska S, Piernik A, Hrynkiewicz K (2013) Metabolic potential of microorganisms associated with the halophyte Aster tripolium L. in saline soils. Ecol Quest 18:9–19CrossRefGoogle Scholar
  84. Tiwari S, Pandey S, Chauhan PS, Pandey R (2017) Biocontrol agents in co-inoculation manages root knot nematode [Meloidogyne incognita (Kofoid & White) Chitwood] and enhances essential oil content in Ocimum basilicum L. Ind Crop Prod 97:292–301Google Scholar
  85. Tiwari S, Singh P, Tiwari R, Meena KK, Yandigeri M, Singh DP, Arora DK (2011) Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (Triticum aestivum) and chemical diversity in rhizosphere enhance plant growth. Biol Fertil Soils 47:907–916CrossRefGoogle Scholar
  86. Upadhyay A, Kochar M, Upadhyay A, Tripathy S, Rajam MV, Srivastava S (2017) Small RNAs regulate the biocontrol property of fluorescent Pseudomonas strain Psd. Microbiol Res 196:80–88Google Scholar
  87. Upadhyay SK, Singh DP (2015) Effect of salt-tolerant plant growth-promoting rhizobacteria on wheat plants and soil health in a saline environment. Plant Biol 17:288–293CrossRefPubMedGoogle Scholar
  88. Upadhyay SK, Singh JS, Singh DP (2011) Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere 21:214–222Google Scholar
  89. Vacheron J, Desbrosses G, Bouffaud M, Touraine B, Moenne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dye F, Prigent-Combaret C (2013) Plant growth-promoting Rhizobacteria and root system functioning. Front Plant Sci 4:1–19CrossRefGoogle Scholar
  90. Vejan P, Abdullah R, Khadiran T, Ismail S, Boyce AN (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21:573CrossRefGoogle Scholar
  91. Vurukonda SKP, Vardharajula S, Shrivastava M, Skz A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24CrossRefPubMedGoogle Scholar
  92. Walia A, Mehta P, Chauhan A, Shirkot CK (2014) Effect of Bacillus subtilis strain CKT1 as inoculum on growth of tomato seedlings under net house conditions. Proc Natl Acad Sci India B Biol Sci 84:145–155CrossRefGoogle Scholar
  93. Yao L, Wu Z, Zheng Y, Kaleem I, Li C (2010) Growth promotion and protection against salt stress by Pseudomonas putida Rs-198 on cotton. Eur J Soil Biol 46:49–54CrossRefGoogle Scholar
  94. Ali Z, Ullah N, Naseem S, Inam-Ul-Haq M, Jacobsen H (2015) Soil bacteria conferred a positive relationship and improved salt stress tolerance in transgenic pea (Pisum sativum L.) harboring Na+/H+ antiporter. Turk J Bot 39:962. doi: 10.3906/bot-1505-50 CrossRefGoogle Scholar
  95. Zerrouk IZ, Benchabane M, Khelifi L, Yokawa K, Ludwig-Müller J, Baluska F (2016) A Pseudomonas strain isolated from date-palm rhizospheres improves root growth and promotes root formation in maize exposed to salt and aluminum stress. J Plant Physiol 191:111–119Google Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Kalpna D. Rakholiya
    • 1
  • Mital J. Kaneria
    • 2
  • Satya P. Singh
    • 2
  • V. D. Vora
    • 3
  • G. S. Sutaria
    • 3
  1. 1.Institute of Biotechnology, Department of BiosciencesSaurashtra UniversityRajkotIndia
  2. 2.Department of Biosciences (UGC-CAS)Saurashtra UniversityRajkotIndia
  3. 3.Main Dry Farming Research StationJunagadh Agricultural UniversityRajkotIndia

Personalised recommendations