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Plant and Soil

, Volume 410, Issue 1–2, pp 335–356 | Cite as

Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria

  • Cinzia Forni
  • Daiana Duca
  • Bernard R. Glick
Regular Article

Abstract

Background

Soil salinity and drought are an enormous worldwide problem for agriculture, horticulture and silviculture. The initial responses of plants to drought and salinity are similar; both are attributed to water deficit which inhibits plant growth and development.

Scope

In this review, an overview of the major physiological and biochemical changes that occur in plants as a consequence of salt and drought stress is presented. In addition, the role of beneficial plant growth-promoting bacteria in ameliorating many of the deleterious consequences of salt and drought stress is discussed. Mechanisms used by plant growth-promoting bacteria to ameliorate the effects of these stresses include the production of cytokinin, indoleacetic acid, ACC deaminase, abscisic acid, trehalose, volatile organic compounds, and exopolysaccharides.

Conclusion

Given the fundamental understanding of many of the mechanisms operating in plant-bacterial interactions, it is expected that the practical use of beneficial bacteria in agriculture, horticulture and silviculture will grow dramatically in the coming years.

Graphical Abstract

Overview of salt- and drought-stress responses in plants. The perception of stress by plant cell elicits stress-signaling pathways that involve transcriptional remodeling, metabolic changes and altered hormonal activity. Bacterial activity may affect the latter. A positive stress response leads to plant tolerance of the stress while a negative response leads to growth inhibition

Keywords

Drought stress Plant growth-promoting bacteria PGPB Salt stress 

References

  1. Aamir M, Aslam A, Khan MY, Jamshaid MU, Ahmad M, Asghar HN, Zahir ZA (2013) Co-inoculation with Rhizobium and plant growth promoting rhizobacteria (PGPR) for inducing salinity tolerance in mung bean under field condition of semi-arid climate. Asian J Agri. Biol 1:17–22Google Scholar
  2. Abd El-Samad HM (2013) The physiological response of wheat plants to exogenous application of gibberellic acid (GA3) or indole-3-acetic acid (IAA) with endogenous ethylene under salt stress conditions. Int J Plant Physiol Biochem 5:58–64Google Scholar
  3. Abd El-Samad Hamdia M, Shaddad MAK, Doaa MM (2004) Mechanisms of salt tolerance and interactive effects of inoculation on maize cultivars under salt stress conditions. Plant Growth Regulat 44:165–174CrossRefGoogle Scholar
  4. Abeles FB, Morgan PW, Saltveit ME Jr (1992) Ethylene in plant biology. Academic Press, New YorkGoogle Scholar
  5. Afzal I, Basra S, Iqbal A (2005) The effect of seed soaking with plant growth regulators on seedling vigor of wheat under salinity stress. J Stress Physiol Biochem 1:6–14Google Scholar
  6. Ahmad M, Zahir ZA, Nazli F, Akram F, Arshad M, Khalid M (2013) Effectiveness of halo-tolerant, auxin producing Pseudomonas and Rhizobium strains to improve osmotic stress tolerance in mung bean (Vigna radiata L. Braz J Microbiol 44:1341–1348PubMedCrossRefGoogle Scholar
  7. Ahmad P, Rasool S, Gul A, Sheikh SA, Akram NA, Ashraf M, Kazi AM, Gucel S (2016) Jasmonates: multifunctional roles in stress tolerance. Front. Plant Sci. 7:813. doi: 10.3389/fpls.2016.00813 PubMedPubMedCentralGoogle Scholar
  8. Ahmed IM, Nadira UA, Bibi N, Cao F, He X, Zhang G, Wu F (2015) Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley. Environ Exper. Botany 111:1–12Google Scholar
  9. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249PubMedCrossRefGoogle Scholar
  10. Ali S, Charles TC, Glick BR (2014) Amelioration of damages caused by high salinity stress by plant growth-promoting bacterial endophytes. Plant Physiol Biochem 80:160–167PubMedCrossRefGoogle Scholar
  11. Araus JL, Slafer GA, Royo C, Serret MD (2008) Breeding for yield potential and stress adaptation in cereals. Cr rev. Plant Sci 27:6Google Scholar
  12. Arkhipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315CrossRefGoogle Scholar
  13. Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exper. Botany 63:3523–3543Google Scholar
  14. Aziz A, Martin-Tanguy J, Larher F (1998) Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiol Plant 104:195–202CrossRefGoogle Scholar
  15. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  16. Balderas-Hernández VE, Alvarado-Rodríguez M, Fraire-Velázquez S (2013) Conserved versatile master regulators in signaling pathways in response to stress in plants. AoB PLANTS 5:plt033. doi: 10.1093/aobpla/plt033 PubMedPubMedCentralCrossRefGoogle Scholar
  17. Ballizany WL, Hofmann RW, Jahufer MZZ, Barrett BA (2012) Genotype x environment analysis of flavonoid accumulation and morphology in white clover under contrasting field conditions. Field Crops Res 128:156–166CrossRefGoogle Scholar
  18. Bandurska H, Stroìnski A (2005) The effect of salicylic acid on barley response to water deficit. Acta Physiol Plant 27:379–386CrossRefGoogle Scholar
  19. Bangash N, Khalid A, Mahmood T, Siddique MT (2013) Screening rhizobacteria containing ACC-deaminase for growth promotion of wheat under water stress. Pak J Bot 45(SI):91–96Google Scholar
  20. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–28CrossRefGoogle Scholar
  21. Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safranova 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 signaling. New Phytol 181:413–423PubMedCrossRefGoogle Scholar
  22. Belimov AA, Dodd IC, Safronova VI, Shaposhnikov AI, Azarova TS, Makarova NM, Davies WJ, Tikhonovich IA (2015) Rhizobacteria that produce auxins and contain1-amino-cyclopropane-1-carboxylic acid deaminase decrease amino acid concentrations in the rhizosphere and improve growth and yield of well-watered and water-limited potato (Solanum tuberosum. Ann Appl Biol 167:11–25CrossRefGoogle Scholar
  23. Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107PubMedCrossRefGoogle Scholar
  24. Bianco C, Imperlini E, Calogero R, Senatore B, Amoresano A, CarpentieriA PP, Defez R (2006) Indole-3-acetic acid improves Escherichia coli’s defences to stress. Arch Microbiol 185:373–382PubMedCrossRefGoogle Scholar
  25. Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses,” in biochemistry and molecular biology of plants, eds B. B. Buchanan, W. Gruissem, and R. L. Jones (Rockville. Am Soc Plant Physiol:1158–1203Google Scholar
  26. Brígido C, Nascimento F, Duan J, Glick BR, Oliveira S (2013) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Mesorhizobium spp. reduces the negative effects of salt stress in chickpea. FEMS Microbiol Lett 349:46–53PubMedGoogle Scholar
  27. Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547. doi: 10.3389/fpls.2015.00547 PubMedPubMedCentralCrossRefGoogle Scholar
  28. Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9CrossRefGoogle Scholar
  29. Chang P, Gerhardt KE, Huang X-D, Yu X-M, Glick BR, Gerwing PD, Greenberg BM (2014) Plant growth-promoting bacteria that contain ACC deaminase facilitate the growth of barley and oats in salt-impacted soil: potential for phytoremediation of saline soils. Internat J Phytoremed 16:1133–1147CrossRefGoogle Scholar
  30. Chen L, Dodd IC, Davies WJ, Wilkinson S (2013) Ethylene limits abscisic acid- or drying-induced stomatal closure in aged wheat leaves. Plant Cell Environ 38:1850–1856CrossRefGoogle Scholar
  31. Cheng Z, Park E, Glick BR (2007) 1-aminocyclopropane-1-carboxylate (ACC) deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Can J Microbiol 53:912–918PubMedCrossRefGoogle Scholar
  32. Cho S-T, Chang H-H, Egamberdieva D, Kamilova F, Lugtenberg B, Kuo C-H (2015) Genome analysis of Pseudomonas fluorescens PCL1751: a rhizobacterium that controls root diseases and alleviates salt stress for its plant host. PLoS ONE. doi: 10.1371/journal.pone.0140231 Google Scholar
  33. Chrispeels MJ, Maurel C (1994) Aquaporins: the molecular basis of facilitated water movement through living plant cells. Plant Physiol 105:9–15PubMedPubMedCentralCrossRefGoogle Scholar
  34. Cohen AC, Bottini R, Piccoli PN (2008) Azospirillum brasilense Sp245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul 54:97–103CrossRefGoogle Scholar
  35. 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. Botany 87:455–462CrossRefGoogle Scholar
  36. Collins NC, Tardieu F, Tuberosa R (2008) Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiol 147:469–486PubMedPubMedCentralCrossRefGoogle Scholar
  37. Contreras-Cornejo HA, Macías-Rodríguez L, Alfaro-Cuevas R, López-Bucio J (2014) Trichoderma spp. improve growth of Arabidopsis seedlings under salt stress through enhanced root development, osmolite production, and Na+ elimination through root exudates. Molec Plant-Microbe Interact 27:503–514CrossRefGoogle Scholar
  38. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Ann rev. Plant Biol 61:651–679CrossRefGoogle Scholar
  39. Daneshmand F, Arvin MJ, Kalantari KM (2010) Physiological responses to NaCl stress in three wild species of potato in vitro. Acta Physiol Plant 32:91–101CrossRefGoogle Scholar
  40. Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: a review. Environ Exp Bot 115:49–57CrossRefGoogle Scholar
  41. Daszkowska-Golec A, Szarejko I (2013) Open or close the gate – stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138PubMedPubMedCentralCrossRefGoogle Scholar
  42. Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379PubMedPubMedCentralCrossRefGoogle Scholar
  43. Del Rio L (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837PubMedCrossRefGoogle Scholar
  44. Di Cori P, Lucioli S, Frattarelli A, Nota P, Tel-Or E, Benyamini E, Gottlieb H, Caboni E, Forni C (2013) Characterization of the response of in vitro cultured Myrtus communis L. plants to high concentrations of NaCl. Plant Physiol Biochem 73:420–426PubMedCrossRefGoogle Scholar
  45. Dodd IC, Pérez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63:3415–3428PubMedCrossRefGoogle Scholar
  46. Dodd IC, Zinovkina NY, Safronova VI, Belimov AA (2010) Rhizobacterial mediation of plant hormone status. Ann Appl Biol 157:361–379CrossRefGoogle Scholar
  47. Dolferus R (2014) To grow or not to grow: a stressful decision for plants. Plant Sci 229:247–261PubMedCrossRefGoogle Scholar
  48. Dong FC, Wang PT, Song CP (2001) The role of hydrogen peroxide in salicylic acid-induced stomatal closure in Vicia faba guard cells. Acta Phytophysiol Sin 27:296–302Google Scholar
  49. Dong W, Wang M, Xu F, Quan T, Peng K, Xiao L, Xia G (2013) Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging. Plant Physiol 161:1217–1228PubMedPubMedCentralCrossRefGoogle Scholar
  50. Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci U S A 105:8790–8794PubMedPubMedCentralCrossRefGoogle Scholar
  51. Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864CrossRefGoogle Scholar
  52. Egamberdieva D, Kucharova Z, Davranov K, Berg G, Makarova N, Azarova T, Chebotar V, Tikhonovich I, Kamilova F, Validov SZ, Lugtenberg B (2011) Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol Fertil Soils 47:197–205CrossRefGoogle Scholar
  53. Egamberdieva D, Jabborova D, Mamadalieva N (2013) Salt-tolerant Pseudomonas extremorintalis able to stimulate growth of Silybum marianum under salt stress. Med Arom Plant Sci Biotechnol 7:7–10Google Scholar
  54. Egamberdieva D, Jabborova D, Hashem A (2015) Pseudomonas induces salinity tolerance in cotton (Gossypium hirsutum) and resistance to Fusarium root rot through the modulation of indole-3-acetic acid. Saudi J Biol Sci: in pressGoogle Scholar
  55. Elfving N, Davoine C, Benlloch R, Blomberg J, Brännstrӧm K, Müller D, Nilsson A, Ulfstedt M, Ronne H, Wingsle G, Nilsson O, Bjӧrklund S (2011) The Arabidopsis thaliana Med25 mediator subunit integrates environmental cues to control plant development. Proc Nat Acad Sci USA 108:8245–8250PubMedPubMedCentralCrossRefGoogle Scholar
  56. Ferdous J, Hussain SS, Shi B-J (2015) Role of microRNAs in plant drought tolerance. Plant Biotechnol J 13:293–305PubMedCrossRefGoogle Scholar
  57. Forni C, Braglia R, Harren FJM, Cristescu SM (2012) Stress responses of duckweed (Lemna minor L.) and water velvet (Azolla filiculoides lam.) to anionic surfactant sodium-dodecyl-sulphate (SDS). Aquat Toxicol 110–111: 107–113Google Scholar
  58. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488PubMedPubMedCentralCrossRefGoogle Scholar
  59. Gamalero E, Berta G, Massa N, Glick BR, Lingua G (2010) Interactions between Pseudomonas putida UW4 and Gigaspora rosea BEG9 and their consequences on the growth of cucumber under salt stress conditions. J Appl Microbiol 108:236–245PubMedCrossRefGoogle Scholar
  60. Gepstein S, Glick BR (2013) Strategies to ameliorate abiotic stress-induced plant senescence. Plant Molec. Biol 82:623–633Google Scholar
  61. Ghanem ME, Albacete A, Smigocki AC, Frébort I, Pospisilova H, Martinez-Andùjar C, Acosta M, Sánchez-Bravo J, Dodd IC, Pérez-Alfocea F (2011) Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 62:125–140PubMedCrossRefGoogle Scholar
  62. Ghorai S, Pal KK, Dey R (2015) Alleviation of salinity stress in groundnut by application of PGPR. Int res. J Eng Technol 2:742–750Google Scholar
  63. Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5(1):26–33PubMedPubMedCentralCrossRefGoogle Scholar
  64. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012(Article ID 963401):15. doi: 10.6064/2012/963401 Google Scholar
  65. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J Theor Biol 190:63–68PubMedCrossRefGoogle Scholar
  66. Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-containing soil bacteria. Eur J Plant Pathol 119:329–339CrossRefGoogle Scholar
  67. Golldack D, Lüking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30:1383–1391PubMedCrossRefGoogle Scholar
  68. Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5, art 151: 1–10. doi: 10.3389/fpls.2014.00151
  69. Han S, Yu B, Wang Y, Liu Y (2011) Role of plant autophagy in stress response. Protein Cell 2:784–791PubMedPubMedCentralCrossRefGoogle Scholar
  70. 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 25:1119–1128PubMedCrossRefGoogle Scholar
  71. Huang D, Wu W, Abrams SR, Cutler AJ (2008) The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 59:2991–3007PubMedPubMedCentralCrossRefGoogle Scholar
  72. Huang G-T, Ma S-L, Bai L-P, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo Z-F (2012) Signal transduction during cold, salt, and drought stresses in plants. Molec Biol Rep 39:969–987Google Scholar
  73. Javid MG, Sorooshzadeh A, Moradi F, Modarres Sanavy SAM, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Austral. J Crop Sci 5:726–734Google Scholar
  74. Jeong D-H, Green PJ (2013) The role of rice microRNAs in abiotic stress responses. Plant Biol 56:187–197CrossRefGoogle Scholar
  75. Jha Y, Subramanian RB (2013) Paddy plants inoculated with PGPR show better growth physiology and nutrient content under saline conditions. Chil J Agri Res 73:213–219CrossRefGoogle Scholar
  76. Jiménez-Bremont JF, Ruiz OA, Rodriguez-Kessler M (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821PubMedCrossRefGoogle Scholar
  77. Joo GJ, Kim YM, Kim JT, Rhee IK, Kim JH, Lee IJ (2005) Gibberellins-producing rhizobacteria increase endogenous gibberellins content and promote growth of red peppers. J Microbiol 43:510–515PubMedGoogle Scholar
  78. Jung JH, Park CM (2011) Auxin modulation of salt stress signaling in Arabidopsis seed germination. Plant Signal Behav 6:1198–1200PubMedPubMedCentralCrossRefGoogle Scholar
  79. Kang G, Li G, Zheng B, Han Q, Wang C, Zhu Y, Guo T (2012) Proteomic analysis on salicylic acid-induced salt tolerance in common wheat seedlings (Triticum aestivum L.). Biochim Biophys Acta 1824:1324–1333PubMedCrossRefGoogle Scholar
  80. Kasotia A, Jain S, Vaishnav A, Kumari S (2012) Soybean growth-promotion by Pseudomonas sp. strain VS1 under salt stress. Pak J Biol Sci 15:698–701PubMedCrossRefGoogle Scholar
  81. Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 10:219–229CrossRefGoogle Scholar
  82. Khan K, Agarwal P, Shanware A, Sane VA (2015) Heterologous expression of two Jatropha aquaporins imparts drought and salt tolerance and improves seed viability in transgenic Arabidopsis thaliana. PLoS One 10(6):e0128866. doi: 10.1371/journal.pone.0128866 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Kiani MZ, Ali A, Sultan T, Ahmad R, Hydar SI (2015) Plant growth promoting rhizobacteria having 1-aminocyclopropane-1-carboxylic acid deaminase to induce salt tolerance in sunflower (Helianthus annus L.). Nat Resour 6:391–397Google Scholar
  84. Kim JS, Mizoi J, Kidokoro S, Maruyama K, Nakajima J, Nakashima K, Mitsuda N, Takiguchi Y, Ohme-Takagi M, Kondou Y, Yoshizumi T, Matsui M, Shinozaki K, Yamaguchi-Shinozaki K (2012) Arabidopsis growth-regulating factor7 functions as a transcriptional repressor of abscisic acid- and osmotic stress-responsive genes, including DREB2A. Plant Cell 24:3393–3405PubMedPubMedCentralCrossRefGoogle Scholar
  85. Kim K, Jang Y-J, Lee S-M, B-T O, Chae J-C, Lee K-J (2014) Alleviation of salt stress by Enterobacter sp. EJ01 in tomato and Arabidopsis is accompanied by up-regulation of conserved salinity responsive factors in plants. Mol Cells 37:109–117PubMedPubMedCentralCrossRefGoogle Scholar
  86. Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203PubMedPubMedCentralCrossRefGoogle Scholar
  87. Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JFH (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141PubMedPubMedCentralCrossRefGoogle Scholar
  88. Kroemer G, Mariño G, Levine B (2010) Autophagy and the integrated stress response. Mol Cell 40:280–293PubMedPubMedCentralCrossRefGoogle Scholar
  89. Kumar M, Mishra S, Dixit V, Kumar M, Agarwal L, Singh P, Chauhan PS, Nautiyal CS (2015) Synergistic effect of Pseudomonas putida and Bacillus amyloliquefaciens ameliorates drought stress in chickpea (Cicer arietinum L.). Plant Signal Behav. doi: 10.1080/15592324.2015.1071004 Google Scholar
  90. Lee GW, Lee K-J, Chae J-C (2015) Herbaspirillum sp. strain GW103 alleviates salt stress Brassica rapa L. ssp. pekinensis. Protoplasma. doi: 10.1007/s00709-015-0872-8 Google Scholar
  91. Li C, Ng CK-Y, Fan L-M (2015) MYB transcription factors, active players in abiotic stress signaling. Environ Exper Bot 114:80–91CrossRefGoogle Scholar
  92. Lim J-J, Kim S-D (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J 29:201–208PubMedPubMedCentralCrossRefGoogle Scholar
  93. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and 1308 the plant cell low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406PubMedPubMedCentralCrossRefGoogle Scholar
  94. Liu X, Meng FX, Zhang SQ, Lou CH (2003) Ca2+ is involved in the signal transduction during stomatal movement induced by salicylic acid in Vicia faba. J Plant Physiol Mol Biol 1:59–64Google Scholar
  95. Liu Y, Shi Z, Yao L, Yue H, Li H, Li C (2013) Effect of IAA produced by Klebsiella oxytoca Rs-5 on cotton growth under salt stress. J Gen Appl Microbiol 59:59–65PubMedCrossRefGoogle Scholar
  96. Liu W, Li R-J, Han T-T, Cai W, Z-W F, Y-T L (2015) Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol 168:343–356PubMedPubMedCentralCrossRefGoogle Scholar
  97. Luo ZB, Janz D, Jiang X, Göbel C, Wildhagen H, Tan Y, Rennenberg H, Feussner I, Polle A (2009) Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol 151:1902–1917PubMedPubMedCentralCrossRefGoogle Scholar
  98. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158PubMedCrossRefGoogle Scholar
  99. Mayak S, Tirosh T, Glick BR (2004a) Plant growth-promoting bacteria that confer resistance to water stress in tomato and pepper. Plant Sci 166:525–530CrossRefGoogle Scholar
  100. Mayak S, Tirosh T, Glick BR (2004b) Plant growth-promoting bacteria that confer resistance in tomato to salt stress. Plant Physiol Biochem 42:565–572PubMedCrossRefGoogle Scholar
  101. McNutt M (2014) The drought you can’t see. Science 345:1543PubMedCrossRefGoogle Scholar
  102. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedCrossRefGoogle Scholar
  103. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467PubMedCrossRefGoogle Scholar
  104. Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:1–12CrossRefGoogle Scholar
  105. Moons A, Prinsen E, Bauw G, Montagu MV (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9:2243–2259PubMedPubMedCentralCrossRefGoogle Scholar
  106. Morgan PW, He CJ, De Greef JA, De Proft MP (1990) Does water deficit stress promote ethylene synthesis by intact plants? Plant Physiol 94:1616–1624PubMedPubMedCentralCrossRefGoogle Scholar
  107. Moya JL, Primo-Millo E, Talon M (1999) Morphological factors determining salt tolerance in citrus seedling: the shoot-to-root ratio modulates passive root uptake of chloride ions and their accumulation in leaves. Plant Cell Environ 22:1425–1433CrossRefGoogle Scholar
  108. Munne-Bosch S, Penuelas J (2003) Photo-and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown. Phillyrea angustifolia plants. Planta 217:758–766PubMedCrossRefGoogle Scholar
  109. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  110. Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95PubMedPubMedCentralCrossRefGoogle Scholar
  111. 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
  112. Narayana I, Lalonde S, Saini HS (1991) Water-stress-induced ethylene production in wheat: a fact or artifact? Plant Physiol 96:406–410PubMedPubMedCentralCrossRefGoogle Scholar
  113. Nautiyal CS, Srivastava S, Chauhan PS, Seem K, Mishra A, Sopory SK (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol Biochem 66:1–9PubMedCrossRefGoogle Scholar
  114. Nawaz K, Ashraf M (2010) Exogenous application of glycine betaine modulates activities of antioxidants in maize plants subjected to salt stress. J Agron Crop Sci 196:28–37CrossRefGoogle Scholar
  115. Nichols SN, Hofmann RW, Williams WM (2015) Physiological drought resistance and accumulation of leaf phenolics in white clover interspecific hybrids. Environ Exp Botany 119:40–47CrossRefGoogle Scholar
  116. Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183PubMedPubMedCentralCrossRefGoogle Scholar
  117. Nishiyama R, Le DT, Watanabe Y, Matsui A, Tanaka M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS One 7: e32124Google Scholar
  118. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefGoogle Scholar
  119. Nonami H, Boyer JS (1990) Primary events regulating stem growth at low water potentials. Plant Physiol 94:1601–1609CrossRefGoogle Scholar
  120. Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4, art 428:1–16Google Scholar
  121. Pandolfi C, Pottosin I, Cuin T, Mancuso S, Shabala S (2010) Specificity of polyamine effects on NaCl-induced ion flux kinetics and salt stress amelioration in plants. Plant Cell Physiol 51(3):422–434PubMedCrossRefGoogle Scholar
  122. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedCrossRefGoogle Scholar
  123. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:1–6CrossRefGoogle Scholar
  124. Petrusa LM, Winicov I (1997) Proline status in salt tolerant and salt sensitive alfalfa cell lines and plants in response to NaCl. Plant Physiol Biochem 35:303–310Google Scholar
  125. Qin S, Zhang Y-J, Yuan B, P-Y X, Xing K, Wang J, Jiang J-H (2014) Isolation of ACC deaminase-producing habitat-adapted symbiotic bacteria associated with halophyte Limonium sinense (Girard) Kuntze and evaluating their plant growth-promoting activity under salt stress. Plant Soil 374:753–766CrossRefGoogle Scholar
  126. Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208PubMedCrossRefGoogle Scholar
  127. 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. Springer Plus 2:6PubMedPubMedCentralCrossRefGoogle Scholar
  128. Redillas MCFR, Park S-H, Lee JW, Kim YS, Jeong JS, Jung H, Bang SW, Hahn T-R, Kim J-K (2012) Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress. Plant Biotechnol Rep 6:89–96CrossRefGoogle Scholar
  129. Reina-Bueno M, Argandoña M, Nieto JJ, Hidalgo-García A, Iglesias-Guerra F, Delgado MJ, Vargas C (2012) Role of trehalose in heat and desiccation tolerance in the soil bacterium Rhizobium etli. BMC Microbiol 12:207PubMedPubMedCentralCrossRefGoogle Scholar
  130. Rodriguez-Salazar J, Suarez R, Caballero-Mellado J, Iturriaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296:52–59PubMedCrossRefGoogle Scholar
  131. Ryu H, Cho Y-C (2015) Plant hormones in salt stress tolerance. J Plant Biol 58:147–155CrossRefGoogle Scholar
  132. Sadrnia M, Maksimava N, Khromsova E, Stanislavich S, Owlia P, Arjomandzadegan M (2011) Study of the effect of bacterial 1-aminocyclopropane-1-carboxylte deaminase (ACC) deaminase on resistance to salt stress in tomato plant. Anal Univ Oradea Fas. Biol 18:120–123Google Scholar
  133. Saghafi K, Ahmadi J, Asgharzadeh A, Bakhtiari S (2013) The effect of microbial inoculants on physiological responses of two wheat cultivars under salt stress. Int J Adv Biol. Biomed Res 1:421–431Google Scholar
  134. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci U S A 103:18822–18827PubMedPubMedCentralCrossRefGoogle Scholar
  135. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006b) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309PubMedPubMedCentralCrossRefGoogle Scholar
  136. Sakuraba Y, Kim Y-S, Han S-H, Lee B-D, Paek N-C (2015) The Arabidopsis transcription factor NAC016 promotes drought stress responses by repressing AREB1 transcription through a trifurcate feed-forward regulatory loop involving NAP. Plant Cell 27(6):1771–1787. doi: 10.1105/tpc.15.00222; www.plantcell.org/cgi/
  137. Salamone IEG, Hynes RK, Nelson LM (2001) Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can J Microbiol 47:404–411CrossRefGoogle Scholar
  138. Saleem AR, Bangash N, Mahmood T, Khalid A, Centritto M, Siddique MT (2015) Rhizobacteria capable of producing ACC deaminase promote growth of velvet bean (Mucuna pruriens) under water stress conditions. Int J Agri. Biol 17:663–667Google Scholar
  139. Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292PubMedCrossRefGoogle Scholar
  140. Schoenborn L, Yates PS, Grinton BE, Hugenholtz P, Janssen PH (2004) Liquid serial dilution is inferior to solid media for isolation of cultures representative of the phylum-level diversity of soil bacteria. Appl Environ Microbiol 70:4363–4366PubMedPubMedCentralCrossRefGoogle Scholar
  141. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292PubMedCrossRefGoogle Scholar
  142. Serraj R, Sinclair TR (2002) Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant Cell Environ 25:333–341PubMedCrossRefGoogle Scholar
  143. Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regulat 46:209–221CrossRefGoogle Scholar
  144. Sharp RE, Hsiao TC, Silk WK (1988) Growth of the maize primary root at low water potentials. I spatial distribution of expansive growth. Plant Physiol 87:50–57PubMedPubMedCentralCrossRefGoogle Scholar
  145. Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334PubMedPubMedCentralCrossRefGoogle Scholar
  146. Siddikee MA, Glick BR, Chauhan PS, Yim W-J, Sa T (2011) Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing ACC deaminase activity. Plant Physiol Biochem 49:427–434PubMedCrossRefGoogle Scholar
  147. Siddikee MA, Sunderem S, Chandrasekaran M, Kim K, Selvakumar G, Sa T (2015) Halotolerant bacteria with ACC deaminase activity alleviate salt stress in canola seed germination. J Korean Soc Appl Biol Chem 58:237–241CrossRefGoogle Scholar
  148. Slavikova S, Ufaz S, Avin-Wittenberg T, Levanony H, Galili G (2008) An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. J Exp Bot 59:4029–4043PubMedPubMedCentralCrossRefGoogle Scholar
  149. Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold spring Harb Persp. Biol 3:#4Google Scholar
  150. Suarez R, Wong A, Ramirez M, Barraza A, Orozco MC, 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 21:958–966PubMedCrossRefGoogle Scholar
  151. Suarez C, Cardinale M, Ratering S, Steffens D, Jung S, Montoya AMZ, Geissler-Plaum R, Schnell S (2015) Plant growth-promoting effects of Hartmannibacter diazotrophicus on summer barley (Hordeum vulgare L.) under salt stress. Appl Soil Ecol 95:23–30CrossRefGoogle Scholar
  152. Sukweenadhi J, Kim Y-J, Choi E-S, Koh S-CLee S-W, Kim Y-J, Yang DC (2015) Paenibacillusyonginensis DCY84T induces changes in Arabidopsis thaliana gene expression against aluminum, drought, and salt stress. Microbiol Res 172:7–15PubMedCrossRefGoogle Scholar
  153. Sun J, Chen S-L, Dai S-X, Wang R-G, Li N-Y, Shen X, Zhou X-Y, C–F L, Zheng X-J, Z-M H, Zhang Z-K, Song J, Xu Y (2009) Ion flux profiles and plant ion homeostasis control under salt stress. Plant Signal Behav 4:261–264PubMedPubMedCentralCrossRefGoogle Scholar
  154. Takahashi S, Seki M, Ishida J, Satou M, Sakurai T, Narusaka M, Kamiya A, Nakajima M, Enju A, Akiyama K (2004) Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray. Plant Mol Biol 56:29–55PubMedCrossRefGoogle Scholar
  155. Tardieu F (2005) Plant tolerance to water deficit: physical limits and possibilities for progress. C R Geosci 337:57–67CrossRefGoogle Scholar
  156. Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl ions in soil solution have simultaneous detrimental effects on growth of fava bean under salinity stress. J Exp Bot 61:4449–4459PubMedPubMedCentralCrossRefGoogle Scholar
  157. Tewari S, Arora NK (2014) Multifunctional exopolysaccharides from Pseudomonas aeruginosa PF23 involved in plant growth stimulation, biocontrol and stress amelioration in sunflower under saline conditions. Curr Microbiol 69:484–494PubMedCrossRefGoogle Scholar
  158. Timmusk S, Paalme V, Pavlicek T, Bergquist J, Vangala A, Danilas T, Nevo E (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS One 6:e17968PubMedPubMedCentralCrossRefGoogle Scholar
  159. Timmusk S, Abd El-Daim IA, Copolovici L, Tanilas T, Kännaste A, Behers L, Nevo E, Seisenbaeva G, Stenström E, Niinemets U (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS ONE 9:e96086PubMedPubMedCentralCrossRefGoogle Scholar
  160. Tittabutr P, Piromyou P, Longtonglang A, Noisa-Ngiam R, Boonkerd N, Teaumroong N (2013) Alleviation of the effect of environmental stresses using co-inoculation of mungbean by Bradyrhizobium and rhizobacteria containing stress-induced ACC deaminase enzyme. Soil Sci Plant Nutr 59:559–571CrossRefGoogle Scholar
  161. Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2010) Role of cytokinin responsive two-component system in ABA and osmotic stress signaling. Plant Signal Behav 5:148–150PubMedPubMedCentralCrossRefGoogle Scholar
  162. Türkan I, Demiral T (2009) Recent development in understanding salinity tolerance. Environ Experim. Botany 67:2–9Google Scholar
  163. Tuteja N, Mahajan S (2007) Calcium signaling network in plants. An overview. Plant Signaling Behav 2: 79–85Google Scholar
  164. Tuteja N, Banu SA, Huda KMK, Gill SS, Jain P, Pham XH, Tuteja R (2014a) A) pea p68, a DEAD-box helicase, provides salinity stress tolerance in transgenic tobacco by reducing oxidative stress and improving photosynthesis machinery. PLoS One 9:e98287. doi: 10.1371/journal.pone.0098287 PubMedPubMedCentralCrossRefGoogle Scholar
  165. Tuteja N, Tarique M, Banu MS, Ahmad M, Tuteja R (2014b) Pisum sativum p68 DEAD-box protein is ATP-dependent RNA helicase and unique bipolar DNA helicase. Plant Mol Biol 85:639–651PubMedCrossRefGoogle Scholar
  166. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971PubMedPubMedCentralCrossRefGoogle Scholar
  167. Vacheron J, Desbrosses G, Bouffaud M-L, 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:article 356. doi: 10.3389/fpls.2013.00356 PubMedCrossRefGoogle Scholar
  168. Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu J-K (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539PubMedCrossRefGoogle Scholar
  169. Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166:1637–1645PubMedCrossRefGoogle Scholar
  170. Wang Q, Dodd IC, Belimov AA, Jiang F (2016) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na + accumulation. Function. Plant Biol 43:161–172Google Scholar
  171. Xu J, Li X-L, Luo L (2012) Effects of engineered Sinorhizobium meliloti on cytokinin synthesis and tolerance of alfalfa to extreme drought stress. Appl Environ Microbiol 78:8056–8061PubMedPubMedCentralCrossRefGoogle Scholar
  172. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu rev. Plant Biol 57:781–803CrossRefGoogle Scholar
  173. Yan J, Smith MD, Glick BR, Liang Y (2014) Effects of ACC deaminase-containing rhizobacteria on plant growth and expression of toc GTPases in tomato (Solanum lycopersicum) under salt stress. Botany 92:775–781CrossRefGoogle Scholar
  174. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and required ABA for full activation. Plant J 61:672–685PubMedCrossRefGoogle Scholar
  175. Yoshida T, Mogami J, Yamaguchi-Sninozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139PubMedCrossRefGoogle Scholar
  176. Yue H, Mo W, Li C, Zheng Y, Li H (2007) The salt stress relief and growth promotion effect of Rs-5 on cotton. Plant Soil 297:139–145CrossRefGoogle Scholar
  177. Zafar-ul-Hye M, Farooq HM, Zahir ZA, Hussain M, Hussain A (2014) Application of ACC-deaminase containing rhizobacteria with fertilizer improves maize production under drought and salinity stress. Int J Agric Biol 16:591–596Google Scholar
  178. Zapata PJ, Serrano MPretel MT, Amoros A, Botella MA (2004) Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci 167:781–788CrossRefGoogle Scholar
  179. Zhao Y, Dong W, Zhang N, Al X, Wang M, Huang Z, Xiao L, Xia G (2014) A wheat allene oxide cyclase gene enhances salinity tolerance via jasmonate signaling. Plant Physiol 164:1068–1076PubMedCrossRefGoogle Scholar
  180. Zhou S, Hu W, Deng X, Ma Z, Chen L, Huang C, Wang C, Wnag J, He Y, Yang G, He G (2012) Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLOS ONE 7(12):e52439. doi: 10.1371/journal.pone.0052439 PubMedPubMedCentralCrossRefGoogle Scholar
  181. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71PubMedCrossRefGoogle Scholar
  182. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 53:247–273CrossRefGoogle Scholar
  183. Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis. Evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Dipartimento di BiologiaUniversità degli Studi di Roma “Tor Vergata”, Via della Ricerca ScientificaRomeItaly
  2. 2.Department of BiologyUniversity of WaterlooWaterlooCanada

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