Alleviating Drought Stress of Crops Through PGPR: Mechanism and Application

  • Firoz Ahmad Ansari
  • Iqbal Ahmad


Crop productivity is severely affected by drought, and its incidence is predicted to enhance under environmental fluctuations and climate change throughout the world. Scarcity of water induced loss in crop growth as well as yields due to major changes in metabolic pathways and gene regulation. Innovative approaches using biochemical and molecular mechanisms increased our understanding of drought alleviation and its management. Previous researches have been focused on the alleviation of drought using rhizobacteria for sustainable agriculture. In recent years, drought stresses in the agriculture system have gained attention due to their deleterious impact on the crop production, protection, and soil health environment. Rhizobacteria perform an important role in the surface colonization of soil colloids and roots of the plant and facilitate proliferation in desired niche, while also improving soil fertility. Despite this fact, numerous papers have reported on growth-stimulating rhizobacteria, but insufficient evidence is available on the rhizobacterial-mediated mitigation of drought stress in soil system. Implications of climate change, namely, drought, would cause disturbance in plant nutrition and soil quality, and plant protection can be better appreciated via an improved understanding of plant microbe as well as soil microbe interaction. Understanding the involvement of various key regulators such as biochemical adjustment, genetic modifications, and molecular strategies will assist effectively for drought stress amelioration in environment-friendly and sustainable agriculture. The present article addresses the biochemical and molecular modification during stress situation in the alleviation of stress under plant soil system. Special consideration is given to plant growth-promoting rhizobacteria with drought tolerance and alleviation capability by the modification of their regulatory mechanisms.


Antioxidant enzymes Drought stress PGPR Plant-microbe interaction, Plant health Rhizosphere colonization 


  1. Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66(8):3393–3398PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alavi P, Starcher M, Zachow C, Müller H, Berg G (2013) Root-microbe systems: the effect and mode of interaction of stress protecting agent (SPA) Stenotrophomonas rhizophila DSM14405T. Front Plant Sci 4:141PubMedPubMedCentralCrossRefGoogle Scholar
  3. Ali SZ, Sandhya V, Rao LV (2014) Isolation and characterization of drought-tolerant ACC deaminase and exopolysaccharide-producing fluorescent Pseudomonas sp. Ann Microbiol 64(2):493–502CrossRefGoogle Scholar
  4. Anjum SA, Xie XY, Wang LC, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6(9):2026–2032Google Scholar
  5. Ansary MH, Rahmani HA, Ardakani MR, Paknejad F, Habibi D, Mafakheri S (2012) Effect of Pseudomonas fluorescent on proline and phytohormonal status of maize (Zea mays L.) under water deficit stress. Ann Biol Res 3(2):1054–1062Google Scholar
  6. Armada E, Roldán A, Azcon R (2014) Differential activity of autochthonous bacteria in controlling drought stress in native Lavandula and Salvia plants species under drought conditions in natural arid soil. Microb Ecol 1 67(2):410–420PubMedCrossRefGoogle Scholar
  7. Arshad M, Shaharoona B, Mahmood T (2008) Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield, and ripening of pea (Pisum sativum L.). Pedosphere 18(5):611–620CrossRefGoogle Scholar
  8. Ayala-Astorga GI, Alcaraz-Meléndez L (2010) Salinity effects on protein content, lipid peroxidation, pigments, and proline in Paulownia imperialis (Siebold & Zuccarini) and Paulownia fortunei (Seemann & Hemsley) grown in vitro. Electron J Biotechnol 13(5):13–14CrossRefGoogle Scholar
  9. Balloi A, Rolli E, Marasco R, Mapelli F, Tamagnini I, Cappitelli F, Borin S, Daffonchio D (2010) The role of microorganisms in bioremediation and phytoremediation of polluted and stressed soils. Agrochimica 54(6):353–369Google Scholar
  10. Bano QU, Ilyas N, Bano A, Zafar NA, Akram AB, Hassan F (2013) Effect of Azospirillum inoculation on maize (Zea mays L.) under drought stress. Pak J Bot 45(S1):13–20Google Scholar
  11. Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol 181(2):413–423PubMedCrossRefGoogle Scholar
  12. Bensalim S, Nowak J, Asiedu SK (1998) A plant growth promoting rhizobacterium and temperature effects on performance of 18 clones of potato. Am J Potato Res 75(3):145–152CrossRefGoogle Scholar
  13. Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84(1):11–18PubMedCrossRefGoogle Scholar
  14. Caravaca F, Alguacil MM, Hernández JA, Roldán A (2005) Involvement of antioxidant enzyme and nitrate reductase activities during water stress and recovery of mycorrhizal Myrtus communis and Phillyrea angustifolia plants. Plant Sci 169(1):191–197CrossRefGoogle Scholar
  15. Cherif H, Marasco R, Rolli E, Ferjani R, Fusi M, Soussi A, Mapelli F, Blilou I, Borin S, Boudabous A, Cherif A (2015) Oasis desert farming selects environment-specific date palm root endophytic communities and cultivable bacteria that promote resistance to drought. Environ Microbiol Rep 7(4):668–678PubMedCrossRefGoogle Scholar
  16. Cho SM, Kang BR, Kim YC (2013) Transcriptome analysis of induced systemic drought tolerance elicited by Pseudomonas chlororaphis O6 in Arabidopsis thaliana. Plant Pathol J 29(2):209PubMedPubMedCentralCrossRefGoogle Scholar
  17. Choluj D, Karwowska R, Jasinska M, Haber G (2004) Growth and dry matter partitioning in sugar beet plants (Beta vulgaris L.) under moderate drought. Plant Soil Environ 50(6):265–272CrossRefGoogle Scholar
  18. Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97(4):795–803CrossRefGoogle Scholar
  19. Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Barka EA (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71(4):1685–1693PubMedPubMedCentralCrossRefGoogle Scholar
  20. Compant S, Kaplan H, Sessitsch A, Nowak J, Ait Barka E, Clément C (2008) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63(1):84–93PubMedCrossRefGoogle Scholar
  21. Creus CM, Graziano M, Casanovas EM, Pereyra MA, Simontacchi M, Puntarulo S, Barassi CA, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221(2):297–303PubMedCrossRefGoogle Scholar
  22. Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32(12):1682–1694PubMedCrossRefGoogle Scholar
  23. Ding GC, Piceno YM, Heuer H, Weinert N, Dohrmann AB, Carrillo A, Andersen GL, Castellanos T, Tebbe CC, Smalla K (2013) Changes of soil bacterial diversity as a consequence of agricultural land use in a semi-arid ecosystem. PLoS One 8(3):e59497PubMedPubMedCentralCrossRefGoogle Scholar
  24. Dodd IC, Belimov AA, Sobeih WY, Safronova VI, Grierson D, Davies WJ (2004) Will modifying plant ethylene status improve plant productivity in water-limited environments. In: Proceedings for the 4th international crop science congress, vol 26, Brisbane, AustraliaGoogle Scholar
  25. Egamberdieva D (2013) The role of phytohormone producing bacteria in alleviating salt stress in crop plants. Biotechnological techniques of stress tolerance in plants. Studium, Houston, pp 21–39Google Scholar
  26. Egamberdieva D, Davranov K, Wirth S, Hashem A, Abd Allah EF (2017) Impact of soil salinity on the plant-growth–promoting and biological control abilities of root associated bacteria. Saudi J Biol Sci 24(7):1601–1608PubMedPubMedCentralCrossRefGoogle Scholar
  27. Fahad S, Hussain S, Bano A, Saud S, Hassan S, Shan D, Khan FA, Khan F, Chen Y, Wu C, Tabassum MA (2015) Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: consequences for changing environment. Environ Sci Pollut Res 22(7):4907–4921CrossRefGoogle Scholar
  28. German MA, Burdman S, Okon Y, Kigel J (2000) Effects of Azospirillum brasilense on root morphology of common bean (Phaseolus vulgaris L.) under different water regimes. Biol Fertil Soils 32(3):259–264CrossRefGoogle Scholar
  29. Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312Google Scholar
  30. Gou W, Tian L, Ruan Z, Zheng PE, Chen FU, Zhang L, Cui Z, Zheng P, Li Z, Gao M, Shi W (2015) Accumulation of choline and glycinebetaine and drought stress tolerance induced in maize (Zea mays) by three plant growth promoting rhizobacteria (PGPR) strains. Pak J Bot 47(2):581–586Google Scholar
  31. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37(3):395–412CrossRefGoogle Scholar
  32. 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(5):1231–1240CrossRefGoogle Scholar
  33. Gusain YS, Singh US, Sharma AK (2015) Bacterial mediated amelioration of drought stress in drought tolerant and susceptible cultivars of rice (Oryza sativa L.). Afr J Biotechnol 14(9):764–773CrossRefGoogle Scholar
  34. Hallmann J, Quandt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43(10):895–914CrossRefGoogle Scholar
  35. Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16(10):463–471CrossRefGoogle Scholar
  36. Heidari M, Golpayegani A (2012) Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.). J Saudi Soc Agric Sci 11(1):57–61Google Scholar
  37. Hendry GA (1993) Oxygen, free radical processes and seed longevity. Seed Sci Res 3(3):141–153CrossRefGoogle Scholar
  38. Hepper CM (1975) Extracellular polysaccharides of soil bacteria. In: Walker N (ed) Soil microbiology. Elsevier, AmsterdamGoogle Scholar
  39. Hill CB, Taylor JD, Edwards J, Mather D, Bacic A, Langridge P, Roessner U (2013) Whole genome mapping of agronomic and metabolic traits to identify novel quantitative trait loci in bread wheat grown in a water-limited environment. Plant Physiol 162:1266–1281PubMedPubMedCentralCrossRefGoogle Scholar
  40. Hsiao TC (2000) Leaf and root growth in relation to water status. Hort Sci 35:1051–1058CrossRefGoogle Scholar
  41. Hussain MB, Zahir ZA, Asghar HN, Asgher M (2014) Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat? Int J Agric Biol 16(1)Google Scholar
  42. Jaleel CA, Manivannan PA, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram RA, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11(1):100–105Google Scholar
  43. Johnová P, Skalák J, Saiz-Fernández I, Brzobohatý B (2016) Plant responses to ambient temperature fluctuations and water-limiting conditions: a proteome-wide perspective. Biochimica et Biophysica Acta (BBA)-proteins and. Proteomics 1864(8):916–931CrossRefGoogle Scholar
  44. Kamara AY, Menkir A, Badu-Apraku B, Ibikunle O (2003) The influence of drought stress on growth, yield and yield components of selected maize genotypes. J Agric Sci 141(1):43–50CrossRefGoogle Scholar
  45. 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(1):47PubMedPubMedCentralCrossRefGoogle Scholar
  46. Kasim WA, Osman ME, Omar MN, El-Daim IA, Bejai S, Meijer J (2013) Control of drought stress in wheat using plant-growth-promoting bacteria. J Plant Growth Regul 32(1):122–130CrossRefGoogle Scholar
  47. Kaushal M, Wani SP (2016) Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann Microbiol 66(1):35–42CrossRefGoogle Scholar
  48. Kim YC, Glick BR, Bashan Y, Ryu CM (2012) Enhancement of plant drought tolerance by microbes. In: Plant responses to drought stress. Springer, Berlin/Heidelberg, pp 383–413CrossRefGoogle Scholar
  49. Köberl M, Müller H, Ramadan EM, Berg G (2011) Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PLoS One 6:e24452. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Köberl M, Schmidt R, Ramadan EM, Bauer R, Berg G (2013) The microbiome of medicinal plants: diversity and importance for plant growth, quality and health. Front Microbiol 20(4):400Google Scholar
  51. Konnova SA, Brykova OS, Sachkova OA, Egorenkova IV, Ignatov VV (2001) Protective role of the polysaccharide-containing capsular components of Azospirillum brasilense. Microbiology 70(4):436–440CrossRefGoogle Scholar
  52. Lafitte HR, Yongsheng G, Yan S, Li ZK (2006) Whole plant responses, key processes, and adaptation to drought stress: the case of rice. J Exp Bot 58(2):169–175PubMedCrossRefGoogle Scholar
  53. Lau JA, Lennon JT (2011) Evolutionary ecology of plant–microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192(1):215–224PubMedCrossRefGoogle Scholar
  54. Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci 109(35):14058–14062CrossRefGoogle Scholar
  55. Lifshitz R, Kloepper JW, Scher FM, Tipping EM, Laliberté M (1986) Nitrogen-fixing pseudomonads isolated from roots of plants grown in the Canadian high Arctic. Appl Environ Microbiol 51(2):251–255PubMedPubMedCentralGoogle Scholar
  56. Lim JH, Kim SD (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J 29(2):201PubMedPubMedCentralCrossRefGoogle Scholar
  57. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556PubMedCrossRefGoogle Scholar
  58. Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A, Ouzari I, Daffonchio D, Borin S (2013) Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. Biomed Res Int 2013:1CrossRefGoogle Scholar
  59. Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, Abou-Hadid AF, El-Behairy UA, Sorlini C, Cherif A, Zocchi G (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7(10):e48479PubMedPubMedCentralCrossRefGoogle Scholar
  60. Marasco R, Rolli E, Vigani G, Borin S, Sorlini C, Ouzari H, Zocchi G, Daffonchio D (2013) Are drought-resistance promoting bacteria cross-compatible with different plant models? Plant Signal Behav 8(10):e26741PubMedPubMedCentralCrossRefGoogle Scholar
  61. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315(5811):513–515PubMedCrossRefGoogle Scholar
  62. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42(6):565–572PubMedCrossRefGoogle Scholar
  63. Miller GA, Suzuki N, Ciftci-Yilmaz SU, Mittler RO (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33(4):453–467PubMedCrossRefGoogle Scholar
  64. Mishra SK, Khan MH, Misra S, Dixit VK, Khare P, Srivastava S, Chauhan PS (2017 Feb 1) Characterization of Pseudomonas spp. and Ochrobactrum sp. isolated from volcanic soil. Antonie Van Leeuwenhoek 110(2):253–270PubMedCrossRefGoogle Scholar
  65. Molina-Favero C, Creus CM, Simontacchi M, Puntarulo S, Lamattina L (2008) Aerobic nitric oxide production by Azospirillum brasilense Sp245 and its influence on root architecture in tomato. Mol Plant-Microbe Interact 21(7):1001–1009PubMedCrossRefGoogle Scholar
  66. Nair AS, Abraham TK, Jaya DS (2008) Studies on the changes in lipid peroxidation and antioxidants in drought stress induced cowpea (Vigna unguiculata L.) varieties. J Environ Biol 29:689–691PubMedGoogle Scholar
  67. Naseem H, Bano A (2014) Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize. J Plant Interact 9(1):689–701CrossRefGoogle Scholar
  68. Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441PubMedCrossRefGoogle Scholar
  69. Rahdari P, Hoseini SM (2012) Drought stress: a review. Int J Agronomy Plant Production 3(10):443–446Google Scholar
  70. Rahdari P, Tavakoli S, Hosseini SM (2012) Studying of salinity stress effect on germination, proline, sugar, protein, lipid and chlorophyll content in purslane (Portulaca oleracea L.) leaves. J Stress Physiol Biochem 8(1):182–193Google Scholar
  71. Rampino P, Pataleo S, Gerardi C, Mita G, Perrotta C (2006) Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. Plant Cell Environ 29(12):2143–2152PubMedCrossRefGoogle Scholar
  72. Redman RS, Kim YO, Woodward CJ, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6(7):e14823PubMedPubMedCentralCrossRefGoogle Scholar
  73. Roberson EB, Firestone MK (1992) Relationship between desiccation and exopolysaccharide production in a soil Pseudomonas sp. Appl Environ Microbiol 58(4):1284–1291PubMedPubMedCentralGoogle Scholar
  74. Rodríguez-Salazar J, Suárez R, Caballero-Mellado J, Iturriaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296(1):52–59PubMedCrossRefGoogle Scholar
  75. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Pierotti Cei F (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17(2):316–331PubMedPubMedCentralCrossRefGoogle Scholar
  76. Saikia J, Sarma RK, Dhandia R, Yadav A, Bharali R, Gupta VK, Saikia R (2018) Alleviation of drought stress in pulse crops with ACC deaminase producing rhizobacteria isolated from acidic soil of Northeast India. Sci Rep 8(1):3560PubMedPubMedCentralCrossRefGoogle Scholar
  77. Samarah NH (2005) Effects of drought stress on growth and yield of barley. Agron Sustain Dev 25(1):145–149CrossRefGoogle Scholar
  78. Sandhya VZ, 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(1):17–26CrossRefGoogle Scholar
  79. Sandhya VS, Ali SZ, Grover M, Reddy G, Venkateswarlu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62(1):21–30CrossRefGoogle Scholar
  80. Schlauch KA, Grimplet J, Cushman J, Cramer GR (2010) Transcriptomics analysis methods: microarray data processing, analysis and visualization using the Affymetrix Genechip® Vitis Vinifera genome Array. In: Methodologies and results in grapevine research. Springer, Dordrecht, pp 317–334CrossRefGoogle Scholar
  81. Schmidt R, Köberl M, Mostafa A, Ramadan EM, Monschein M, Jensen KB, Bauer R, Berg G (2014) Effects of bacterial inoculants on the indigenous microbiome and secondary metabolites of chamomile plants. Front Microbiol 5:64PubMedPubMedCentralGoogle Scholar
  82. Selvakumar G, Panneerselvam P, Ganeshamurthy AN (2012) Bacterial mediated alleviation of abiotic stress in crops. In: Bacteria in agrobiology: stress management. Springer, Berlin, Heidelberg, pp 205–224CrossRefGoogle Scholar
  83. Sgherri CL, Maffei M, Navari-Izzo F (2000) Antioxidative enzymes in wheat subjected to increasing water deficit and rewatering. Journal of Plant 157(3):273–279Google Scholar
  84. Shakir MA, Bano A, Arshad M (2012) Rhizosphere bacteria containing ACC-deaminase conferred drought tolerance in wheat grown under semi-arid climate. Soil & Environment 31(1):108–112Google Scholar
  85. Sharma P, Khanna V, Kumari P (2013) Efficacy of aminocyclopropane-1-carboxylic acid (ACC)-deaminase-producing rhizobacteria in ameliorating water stress in chickpea under axenic conditions. Afr J Microbiol Res 7(50):5749–5757CrossRefGoogle Scholar
  86. Shintu PV, Jayaram KM (2015) Phosphate solubilising bacteria (Bacillus polymyxa)-an effective approach to mitigate drought in tomato (Lycopersicon esculentum Mill). Tropic Plant Res 2:17–22Google Scholar
  87. Siddiqi EH, Ashraf M, Hussain M, Jamil A (2009) Assessment of intercultivar variation for salt tolerance in safflower (Carthamus tinctorius L.) using gas exchange characteristics as selection criteria. Pak J Bot 41(5):2251–2259Google Scholar
  88. Skirycz A, Inzé D (2010) More from less: plant growth under limited water. Curr Opin Biotechnol 21(2):197–203PubMedCrossRefGoogle Scholar
  89. Suárez R, Wong A, Ramírez M, Barraza A, Orozco MD, Cevallos MA, Lara M, Hernández G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant-Microbe Interact 21(7):958–966PubMedCrossRefGoogle Scholar
  90. Tao JJ, Chen HW, Ma B, Zhang WK, Chen SY, Zhang JS (2015 Nov 27) The role of ethylene in plants under salinity stress. Front Plant Sci 6:1059PubMedPubMedCentralCrossRefGoogle Scholar
  91. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7(11):847PubMedCrossRefGoogle Scholar
  92. Theocharis A, Bordiec S, Fernandez O, Paquis S, Dhondt-Cordelier S, Baillieul F, Clément C, Barka EA (2012) Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Mol Plant-Microbe Interact 25(2):241–249PubMedCrossRefGoogle Scholar
  93. Timmusk S, Nevo E (2011) Plant root associated biofilms. In: Maheshwari DK (ed) Bacteria in agrobiology (vol 3) plant nutrient management. Springer Verlag, Berlin. Google Scholar
  94. Timmusk S, Wagner EG (1999) The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol Plant Microb Interact 12:951CrossRefGoogle Scholar
  95. Timmusk S, El-Daim IA, Copolovici L, Tanilas T, Kännaste A, Behers L, Nevo E, Seisenbaeva G, Stenström E, Niinemets Ü (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS One 9(5):e96086PubMedPubMedCentralCrossRefGoogle Scholar
  96. Tisdall JM, Oades J (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33(2):141–163CrossRefGoogle Scholar
  97. Trewavas A (2006) A brief history of systems biology: “every object that biology studies is a system of systems.” Francois Jacob (1974). Plant Cell 18(10):2420–2430PubMedPubMedCentralCrossRefGoogle Scholar
  98. Ullah N, Yüce M, Gökçe ZN, Budak H (2017) Comparative metabolite profiling of drought stress in roots and leaves of seven Triticeae species. BMC Genomics 18(1):969PubMedPubMedCentralCrossRefGoogle Scholar
  99. Vardharajula S, Zulfikar Ali S, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6(1):1–4CrossRefGoogle Scholar
  100. Vargas L, Santa Brígida AB, Mota Filho JP, de Carvalho TG, Rojas CA, Vaneechoutte D, Van Bel M, Farrinelli L, Ferreira PC, Vandepoele K, Hemerly AS (2014) Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus: a transcriptomic view of hormone pathways. PLoS One 9(12):e114744PubMedPubMedCentralCrossRefGoogle Scholar
  101. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57PubMedPubMedCentralCrossRefGoogle Scholar
  102. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217(4566):1214–1222PubMedCrossRefGoogle Scholar
  103. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4PubMedCrossRefGoogle Scholar
  104. Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, Madden PA, Heath AC, Martin NG, Montgomery GW, Goddard ME (2010) Common SNPs explain a large proportion of the heritability for human height. Nat Genet 42(7):565PubMedPubMedCentralCrossRefGoogle Scholar
  105. Yuwono T, Handayani D, Soedarsono J (2005) The role of osmotolerant rhizobacteria in rice growth under different drought conditions. Aust J Agric Res 56(7):715–721CrossRefGoogle Scholar
  106. Zahir ZA, Munir A, Asghar HN, Shaharoona B, Arshad M (2008) Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18(5):958–963PubMedGoogle Scholar
  107. Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A (2017) Modulation of antioxidant defense system is associated with combined drought and heat stress tolerance in citrus. Front Plant Sci 7(8):953CrossRefGoogle Scholar
  108. Zeisel SH (2006) Choline: critical role during fetal development and dietary requirements in adults. Annu Rev Nutr 26:229–250PubMedPubMedCentralCrossRefGoogle Scholar
  109. Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Zak JC, Dowd SE, Paré PW (2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant-Microbe Interact 23(8):1097–1104PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Firoz Ahmad Ansari
    • 1
  • Iqbal Ahmad
    • 1
  1. 1.Biofilm Research Laboratory, Department of Agricultural Microbiology, Faculty of Agricultural SciencesAligarh Muslim UniversityAligarhIndia

Personalised recommendations