Annals of Microbiology

, Volume 66, Issue 1, pp 35–42 | Cite as

Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands

  • Manoj KaushalEmail author
  • Suhas P. Wani
Review Article


Drylands are known for being a drought stressed environment, which is an alarming constraint to crop productivity. To rescue plant growth in such stressful conditions, plant-growth-promoting rhizobacteria (PGPR) are a bulwark against drought stress and imperilled sustainability of agriculture in drylands. PGPR mitigates the impact of drought stress on plants through a process called rhizobacterial-induced drought endurance and resilience (RIDER), which includes physiological and biochemical changes. Various RIDER mechanisms include modification in phytohormonal levels, antioxidant defense, bacterial exopolysaccharides (EPS), and those associated with metabolic adjustments encompass accumulation of several compatible organic solutes like sugars, amino acids and polyamines. Production of heat-shock proteins (HSPs), dehydrins and volatile organic compounds (VOCs) also plays significant role in the acquisition of drought tolerance. Selection, screening and application of drought-stress-tolerant PGPRs to crops can help to overcome productivity limits in drylands.


Drought stress PGPR LapA EPS VOCs RIDER 



Financial help provided by ICRISAT is highly acknowledged.


  1. Ahn TS, Ka JO, Lee GH, Song HG (2007) Microcosm study for revegetation of barren land with wild plants by some plant growth-promoting rhizobacteria. J Microbiol Biotechnol 17:52–57PubMedGoogle Scholar
  2. Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharides-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66:3393–3398PubMedCentralCrossRefPubMedGoogle Scholar
  3. Alcazar R, Bitrian M, Bartels D, Koncz C, Altabella T, Tiburcio AF (2010) Polyamines, molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249CrossRefPubMedGoogle Scholar
  4. Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2011) Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum. Plant Signal Behav 6:243–250PubMedCentralCrossRefPubMedGoogle Scholar
  5. Ali Sk Z, Sandhya V, Grover M, Kishore N, Rao LV, Venkateswarlu B (2009) Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fert Soil 46:45–55Google Scholar
  6. Allison S, Chang B, Randolph T, Carpenter J (1999) Hydrogen bonding between sugar and protein is responsible for inhibition of dehydration-induced protein unfolding. Arch Biochem Biophy 365:289–298CrossRefGoogle Scholar
  7. Amellal N, Burtin G, Bartoli F, Heulin T (1998) Colonization of wheat roots by an exopolysaccharides-producing Pantoea agglomerans strain and its effect on rhizosphere soil aggregation. Appl Environ Microbiol 64:3740–3747PubMedCentralPubMedGoogle Scholar
  8. Ansary MH, Rahmani HA, Ardakani MR, Paknejad F, Habibi D, Mafakheri S (2012) Effect of Pseudomonas fluorescens on proline and phytohormonal status of maize (Zea mays L.) under water deficit stress. Annal Biol Res 3:1054–1062Google Scholar
  9. Apel K, Hirt H (2004) Reactive oxygen species, metabolism, oxidative stress, and signal transduction. Annal Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  10. Awad NM, Turky AS, Abdelhamid MT, Attia M (2012) Ameliorate of environmental salt stress on the growth of Zea mays L. plants by exopolysaccharides producing bacteria. J Appl Sci Res 8:2033–2044Google Scholar
  11. Bano A, Fatima M (2009) Salt tolerance in Zea mays (L.) following inoculation with Rhizobium and Pseudomonas. Biol Fert Soils 45:405–413CrossRefGoogle Scholar
  12. Barka EA, Nowak J, Clement C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Env Microbiol 72:7246–7252CrossRefGoogle Scholar
  13. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  14. Bensalim S, Nowak J, Asiedu S (1998) A plant growth promoting rhizobacterium and temperature effects on performance of 18 clones of potato. A Potato J 75:145–152CrossRefGoogle Scholar
  15. Berjak P (2006) Unifying perspectives of some mechanisms basic to desiccation tolerance across life forms. Seed Sci Res 16:1–15CrossRefGoogle Scholar
  16. Bhaskar PV, Bhosle NB (2005) Microbial extracellular polymeric substances in marine biogeochemical processes. Curr Sci 88:45–53Google Scholar
  17. Boiero L, Perrig D, Masciarelli O, Penna C, Cassan F, Luna V (2006) Phytohormone production by three strains of Bradyrhizobium japonicum, and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880CrossRefPubMedGoogle Scholar
  18. Borlee B, Goldman A, Murakami K, Samudrala R, Wozniak D, Parsek M (2010) Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75:827–842PubMedCentralCrossRefPubMedGoogle Scholar
  19. Borovskii GB, Stupnikova IV, Antipina AI, Vladimirova SV, Voinikov VK (2002) Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment. BMC Plant Biol 2:5PubMedCentralCrossRefPubMedGoogle Scholar
  20. Bresson J, Varoquaux F, Bontpart T, Touraine B, Vile D (2013) The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytol 200:558–569CrossRefPubMedGoogle Scholar
  21. Cassan F, Maiale S, Masciarelli O, Vidal A, Luna V, Ruiz O (2009) Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. Eur J Soil Biol 45:12–19CrossRefGoogle Scholar
  22. Chang WS, Van de Mortel M, Nielsen L, de Guzman GN, Li X, Halverson LJ (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol 189:8290–8299PubMedCentralCrossRefPubMedGoogle Scholar
  23. Chanway CP, Holl FB (1994) Growth of outplanted lodepole pine seedlings one year after inoculation with plant growth promoting rhizobacteria. Forest Sci 40:238–246Google Scholar
  24. Chen TH, Murata N (2008) Glycinebetaine, an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505CrossRefPubMedGoogle Scholar
  25. Chen K, Kurgan L, Rahbari M (2007) Prediction of protein crystallization using collocation of amino acid pairs. Biochem Biophys Res Commun 355:764–769CrossRefPubMedGoogle Scholar
  26. Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH, Cho BH, Yang KY, Ryu CM, Kim YC (2008) 2R, 3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant Microbe Interact 21:1067–1075CrossRefPubMedGoogle Scholar
  27. Cohen AC, Bottini R, Piccoli PN (2008) Azosprillium brasilense Sp 245 produces ABA in chemically defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul 54:97–103CrossRefGoogle Scholar
  28. Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botanique 87:455–462CrossRefGoogle Scholar
  29. Debaeke P, Abdellah A (2004) Adaptation of crop management to water limited environments. Europ Agron J 21:433–446CrossRefGoogle Scholar
  30. Dekankova K, Luxova M, GaS parikova O, Kolarovi CL (2004) Response of maize plants to water stress. Biologia 13:151–155Google Scholar
  31. Egamberdieva D, Kucharova Z (2009) Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biol Fert Soil 45:561–573CrossRefGoogle Scholar
  32. Ekaza E, Teyssier J, Ouahrani-Bettache S, Liautard J, Kohler S (2001) Characterization of Brucella suis clpB and clpAB mutants and participation of the genes in stress responses. J Bacteriol 183:2677–2684Google Scholar
  33. Enebak SA, Wei G, Kloepper JW (1997) Effects of plant growth-promoting rhizobacteria on loblolly and slash pine seedlings. Forest Sci 44:139–144Google Scholar
  34. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress, effects, mechanisms and management. Agron Sustain Develop 29:185–212CrossRefGoogle Scholar
  35. Figueiredo MVB, Burity HA, Martìnez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182–188CrossRefGoogle Scholar
  36. Glick BR (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242CrossRefGoogle Scholar
  37. Gruszka Vendruscolo EC, Schuster I, Pileggi M, Scapim CA, Correa Molinari HB, Marur CJ, Esteves Vieira LG (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367–1376CrossRefGoogle Scholar
  38. Halverson LJ (2009) Role of alginate in bacterial biofilms. In: Rehm BHA (ed) Alginates, biology and applications. Springer, Dordrecht, pp 136–141Google Scholar
  39. Han HS, Lee KD (2005) Physiological responses of soybean-inoculation of Bradyrhizobium japonicum with PGPR in saline soil conditions. Res J Agric Biol Sci 1:216–221Google Scholar
  40. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation in plants. Plant, Cell Environ 21:535–553CrossRefGoogle Scholar
  41. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438CrossRefPubMedGoogle Scholar
  42. Hontzeas N, Saleh SS, Glick BR (2004) Changes in gene expression in canola roots induced by ACC-deaminase-containing plant growth promoting bacteria. Mol Plant Microbe Interact 17:865–871CrossRefPubMedGoogle Scholar
  43. Hui LJ, Kim SD (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in Pepper. Plant Pathol J 29(2):201–208CrossRefGoogle Scholar
  44. Iqbal N, Ashraf Y, Muhammad A (2011) Modulation of endogenous levels of some key organic metabolites by exogenous application of glycine betaine in drought stressed plants of sunflower (Helianthus annuus L.). Plant Growth Regul 63:7–12CrossRefGoogle Scholar
  45. Jha Y, Subramanian RB, Patel S (2011) Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol Plant 33:797–802CrossRefGoogle Scholar
  46. Kechid M, Desbrosses G, Rokhsi W, Varoquaux F, Djekoun A, Touraine B (2013) The NRT2.5 and NRT2.6 genes are involved in growth promotion of Arabidopsis by the plant growth-promoting rhizobacterium (PGPR) strain Phyllobacterium brassicacearum STM196. New Phytol 198:514–524CrossRefPubMedGoogle Scholar
  47. Kets EP, de Bont JA, Heipieper HJ (1996) Physiological response of Pseudomonas putida s12 subjected to reduced water activity. FEMS Microbiol Lett 139:133–137CrossRefGoogle Scholar
  48. Khalid A, Arshad M, Zahir ZA (2006) Phytohormones, microbial production and applications. In: Uphoff N, Ball AS, Fernandes E, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P, Sanginga N, Thies J (eds) Biological approaches to sustainable soil systems. Taylor and Francis/CRC Press, Boca Raton, pp 207–220CrossRefGoogle Scholar
  49. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608PubMedCentralCrossRefPubMedGoogle Scholar
  50. Lahesaare A, Moor H, Kivisaar M, Teras R (2014) Pseudomonas putida Fis binds to the lapF promoter in vitro and represses the expression of LapF. PLoS ONE 9(12):e115901. doi: 10.1371/journal.pone.0115901 PubMedCentralCrossRefPubMedGoogle Scholar
  51. Liu F, Xing S, Ma H, Du Z, Ma B (2013) Cytokinin producing, plant growth promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol 97(20):9155–9164CrossRefPubMedGoogle Scholar
  52. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Ann Rev Microbiol 63:541–556CrossRefGoogle Scholar
  53. Mantelin S, Touraine B (2004) Plant growth-promoting rhizobacteria and nitrate availability: impacts on root development and nitrate uptake. J Expt Bot 55:27–34CrossRefGoogle Scholar
  54. Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, Abou-Hadid AF, El-Behairy UA, Sorlini C, Cherif A, Zocchi G, Daffonchio D (2012) A drought resistance promoting microbiome is selected by root system under desert farming. PLoS ONE 7:e48479. doi: 10.1371/ journal.pone.0048479 PubMedCentralCrossRefPubMedGoogle Scholar
  55. Martinez-Gil M, Isabel Ramos-Gonzalez M, Espinosa-Urgel M (2014) Roles of cyclic Di-GMP and the Gac system in transcriptional control of the genes coding for Pseudomonas putida adhesions LapA and LapF. J Bacteriol 196:1484–1495PubMedCentralCrossRefPubMedGoogle Scholar
  56. Marulanda A, Porcel R, Barea JM, Azcon R (2007) Drought tolerance and antioxidant activities in lavender plants colonized by native drought tolerant or drought sensitive Glomus species. Microb Ecol 54(3):543–552CrossRefPubMedGoogle Scholar
  57. Marulanda A, Barea JM, Azcon R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environment. mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124CrossRefGoogle Scholar
  58. Mayak S, Tirosh T, Glick BR (2004) Plant growth promoting bacteria that confer resistance to water stress in tomato and pepper. Plant Sci 166:525–530CrossRefGoogle Scholar
  59. Millennium Ecosystem Assessment (2005) Ecosystems and human well-being, desertication synthesis. World Resources Institute, Washington DCGoogle Scholar
  60. Miller G, Susuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ 33:453–467CrossRefGoogle Scholar
  61. Munchbach M, Nocker A, Narberhaus F (1999) Multiple small heat shock proteins in rhizobia. J Bacteriol 181:83–90PubMedCentralPubMedGoogle Scholar
  62. Naseem H, Bano A (2014) Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize. J Plant Inter 9(1):689–701Google Scholar
  63. Nayer M, Reza H (2008) Drought-induced accumulation of soluble sugars and proline in two maize varieties. World Appl Sci J 3:448–453Google Scholar
  64. Patakas A, Noitsakis B (2001) Leaf age effects on solute accumulation in water-stressed grapevines. Plant Physiol 158:63–69CrossRefGoogle Scholar
  65. Paul D, Nair S (2008) Stress adaptations in a plant growth promoting rhizobac-terium (PGPR) with increasing salinity in the coastal agricultural soils. J Basic Microbiol 48:378–384CrossRefPubMedGoogle Scholar
  66. Pereyra MA, Garcia P, Colabelli MN, Barassi CA, Creus CM (2012) A better water status in wheat seedlings induced by Azospirillum under osmotic stress is related to morphological changes in xylem vessels of the coleoptile. Appl Soil Ecol 53:94–97CrossRefGoogle Scholar
  67. Pitzschke AM, Forzani C, Hirt H (2006) Reactive oxygen species signalling in plants. Antiox Redox Signal 8:1757–1764CrossRefGoogle Scholar
  68. Pompelli MF, Barata-Luis R, Vitorino H, Gonclaves E, Rolim E, Santos M, Almeida-Cortez J, Endrez L (2010) Photosynthesis, photoprotection and antioxidant activity of purging nut under drought deficit and recovery. Biomass Bioenergy 34:1207–1215CrossRefGoogle Scholar
  69. Qudsaia B, Noshinil Y, Asghari B, Nadia Z, Abida A, Fayazul H (2013) Effect of Azospirillum inoculation on maize (Zea mays L.) under drought stress. Pak J Bot 45:13–20Google Scholar
  70. Rincon A, Valladares F, Gimeno TE, Pueyo JJ (2008) Water stress responses of two Mediterranean tree species influenced by native soil microorganisms and inoculation with a plant growth promoting rhizobacterium. Tree Physiol 28:1693–1701CrossRefPubMedGoogle Scholar
  71. Roberson EB, Firestone MK (1992) Relationship between desiccation and exopolysaccharide production in a soil Pseudomonas spp. Appl Environ Microbiol 58:1284–1291PubMedCentralPubMedGoogle Scholar
  72. Rocha FR, Papini-Terzi FS, Nishiyama MY, ZN Venico R, Vicentini R, DC Duarte R, de Rosa VE Jr, Vinagre F, Barsalobres C, Medeiros AH, Rodrigues FA, Ulian EC, Zingaretti SM, Galbiatti JA, Almeida RS, Figueira AVO, Hemerly AS, Silva-Filho MC, Menossi M, Souza GM (2007) Signal transduction-related responses to phytohormones and environmental challenges in sugarcane. BMC Genomics 8:71. doi: 10.1186/1471-2164-8-71 PubMedCentralCrossRefPubMedGoogle Scholar
  73. Rodriguez-Salazar J, Suarez R, Caballero-Mellado J, Itturiaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296:52–59CrossRefPubMedGoogle Scholar
  74. Ruiz-Sanchez M, Armada E, Munoz Y, Garcia de Salamone IE, Aroca R, Ruiz-Lozano JM, Azcon R (2011) Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. J Plant Physiol 168:1031–1037CrossRefPubMedGoogle Scholar
  75. Ryu CM (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026PubMedCentralCrossRefPubMedGoogle Scholar
  76. Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress, clues from transgenic plants. Plant, Cell Environ 25:163–171CrossRefGoogle Scholar
  77. Sandhya V, Ali SZ, Grover M, Reddy G, Venkateswaralu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes antioxidant status and plant growth of maize under drought stress. Plant Growth Regu 62:21–30CrossRefGoogle Scholar
  78. Sang-Mo K, Radhakrishnan R, Khan AL, Min-Ji K, Jae-Man P, Bo-Ra K, Dong-Hyun S, In-Jung L (2014) Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol Biochem 84:115–124CrossRefGoogle Scholar
  79. Sarkar NK, Kim YK, Grover A (2009) Rice sHsp genes, genomic organization and expression profiling under stress and development. BMC Genomics 10:393PubMedCentralCrossRefPubMedGoogle Scholar
  80. Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Lett Appl Microbiol 42:155–159Google Scholar
  81. Stajner D, Kevresan S, Gasic O, Mimica-Dukic N, Zongli H (1997) Nitrogen and Azotobacter chroococcum enhance oxidative stress tolerance in sugar beet. Biol Plantarum 39(3):441–445CrossRefGoogle Scholar
  82. Suarez R, Wong A, Ramirez M, Barraza A, OrozcoMdel C, Cevallos MA, Lara M, Hernandez 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):958–966CrossRefPubMedGoogle Scholar
  83. Timmusk S, Wagner EGH (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-Microbe Inter 12:951–959CrossRefGoogle Scholar
  84. Valentovic P, Luxova M, Kolarovic L, Gasparikova O (2006) Effect of osmotic stress on compatible solutes content, membrane stability and water relations in two maize cultivars. Plant Soil Environ 52(4):186–191Google Scholar
  85. Vanderlinde EM, Harrison JJ, Muszynski A, Carlson RW, Turner RJ, Yost CK (2010) Identification of a novel ABC-transporter required for desiccation tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Ecol 71:327–340Google Scholar
  86. 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 Inter 6:1–14Google Scholar
  87. Vile D, Pervent M, Belluau M, Vasseur F, Bresson J, Muller B, Granier C, Simonneau T (2012) Arabidopsis growth under prolonged high temperature and water deficit, independent or interactive effects. Plant, Cell Environ 35:702–718CrossRefGoogle Scholar
  88. Wang Y, Ohara Y, Nakayashiki H, Tosa Y, Mayama S (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol Plant Microbe Inter 18:385–396CrossRefGoogle Scholar
  89. Wang CJ, Yang W, Wang C, Gu C, Niu D-D, Liu HX, Wang YP, Guo JH (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS ONE 7(12):e52565. doi: 10.1371/journal.pone.0052565 PubMedCentralCrossRefPubMedGoogle Scholar
  90. Yadav SK, Jyothi Lakshmi N, Maheswari M, Vanaja M, Venkateswarlu B (2005) Influence of water deficit at vegetative, anthesis and grain filling stages on water relation and grain yield in Sorghum. Indian J Plant Physiol 10:20–22Google Scholar
  91. Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting elementin an Arabidopsis gene is involved in responsiveness todrought, low-temperature, or high-salt stress. Plant Cell 6:251–264PubMedCentralCrossRefPubMedGoogle Scholar
  92. Yang S, Vanderbeld B, Wan J, Huang Y (2010) Narrowing down the targets, towards successful genetic engineering of drought-tolerant crops. Mol Plant 3:469–490CrossRefPubMedGoogle Scholar
  93. Yoshiba Y, Kiyosue T, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol 38:1095–1102CrossRefPubMedGoogle Scholar
  94. Zahir ZA, Munir A, Asghar HN, Arshad M, Shaharoona B (2008) Effectiveness of rhizobacteria containing ACC-deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotech 18:958–963Google Scholar
  95. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Pare PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851CrossRefPubMedGoogle Scholar
  96. Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Zak JC, Dowd SE, Pare PW (2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant Microbe Interact 23:1097–1104. doi: 10.1094/ MPMI-23-8-1097 CrossRefPubMedGoogle Scholar
  97. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg and the University of Milan 2015

Authors and Affiliations

  1. 1.Resilient Dryland SystemsInternational Crops Research Institute for the Semi-Arid Tropics (ICRISAT)HyderabadIndia

Personalised recommendations