Plant Molecular Biology

, Volume 91, Issue 6, pp 651–659 | Cite as

The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses

Article

Abstract

Soil salinity is one of the most commonly encountered environmental stresses affecting plant growth and crop productivity. Accordingly, plants have evolved a variety of morphological, physiological and biochemical strategies that enable them to adapt to saline growth conditions. For example, it has long been known that salinity-stress increases both the production of the gaseous stress hormone ethylene and the in planta accumulation of reactive oxygen species (ROS). Recently, there has been significant progress in understanding how the fine-tuning of ethylene biosynthesis and signaling transduction can promote salinity tolerance, and how salinity-induced ROS accumulation also acts as a signal in the mediation of salinity tolerance. Furthermore, recent advances have indicated that ethylene signaling modulates salinity responses largely via regulation of ROS-generating and ROS-scavenging mechanisms. This review focuses on these recent advances in understanding the linked roles of ethylene and ROS in salt tolerance.

Keywords

Ethylene ROS Salt stress Salt tolerance 

Notes

Acknowledgments

The authors acknowledge financial support from the Chinese Universities Scientific Fund (Grant 2014RC021 to C.J.); the National Natural Science Foundation of China (Grant 31470350 to C.J.); and the UK Biotechnological and Biological Sciences Research Council (Grant BB/F020759/1 to N.P.H.).

Author contribution

MZ, CJ, JACS and NPH conceived and wrote the paper.

References

  1. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94CrossRefPubMedGoogle Scholar
  2. Ai LF, Li CH, Wang G, Zhao JL, Zhang LQ, Han YF, Sun DY, Zhang SW, Sun Y (2014) The receptor-like kinase SIT1 mediates salt sensitivity by activating MAPK3/6 and regulating ethylene homeostasis in rice. Plant Cell 26:2538–2553CrossRefPubMedPubMedCentralGoogle Scholar
  3. Amtmann A, Sanders D (1999) Mechanisms of Na+ uptake by plant cells. Adv Bot Res 29:75–112CrossRefGoogle Scholar
  4. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefPubMedGoogle Scholar
  5. Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143:707–719CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cao YR, Chen SY, Zhang JS (2008) Ethylene signaling regulates salt stress response. Plant Signal Behav 3:761–763CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cheeseman JM (2015) The evolution of halophytes, glycophytes and crops, and its implications for food security under saline conditions. New Phytol 206:557–570CrossRefPubMedGoogle Scholar
  8. Chen YF, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Ann Bot 95:901–915CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chen D, Ma X, Li C, Zhang W, Xia G, Wang M (2014) A wheat aminocyclopropane-1-carboxylate oxidase gene, TaACO1, negatively regulates salinity stress in Arabidopsis thaliana. Plant Cell Rep 33:1815–1827CrossRefPubMedGoogle Scholar
  10. Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162:1566–1582CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi HZ (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565CrossRefPubMedGoogle Scholar
  12. Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379CrossRefPubMedPubMedCentralGoogle Scholar
  13. Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47:907–916CrossRefPubMedGoogle Scholar
  14. Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:151CrossRefPubMedPubMedCentralGoogle Scholar
  15. Dong H, Zhen Z, Peng J, Chang L, Gong Q, Wang NN (2011) Loss of ACS7 confers abiotic stress tolerance by modulating ABA sensitivity and accumulation in Arabidopsis. J Exp Bot 62:4875–4887CrossRefPubMedPubMedCentralGoogle Scholar
  16. Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Ann Rev Plant Physiol 28:89–121CrossRefGoogle Scholar
  17. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446CrossRefPubMedGoogle Scholar
  18. Frommer WB, Ludewig U, Rentsch D (1999) Taking transgenic plants with a pinch of salt. Science 285:1222–1223CrossRefPubMedGoogle Scholar
  19. Gallie DR (2015) Appearance and elaboration of the ethylene receptor family during land plant evolution. Plant Mol Biol 87:521–539CrossRefPubMedGoogle Scholar
  20. Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126CrossRefPubMedPubMedCentralGoogle Scholar
  21. Greenway H, Munns RA (1980) Mechanisms of salt tolerance in non-halophytes. Annu Rev Plant Physiol 31:149–190CrossRefGoogle Scholar
  22. Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49CrossRefPubMedGoogle Scholar
  23. Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell 21:1328–1339CrossRefPubMedPubMedCentralGoogle Scholar
  24. He J, Yue X, Wang R, Zhang Y (2011) Ethylene mediates UV-B-induced stomatal closure via peroxidase-dependent hydrogen peroxide synthesis in Vicia faba L. J Exp Bot 62:2657–2666CrossRefPubMedGoogle Scholar
  25. Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14:660–668CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271CrossRefPubMedGoogle Scholar
  27. Imen K, Pirrello J, Riahi L, Bernadac A, Cherif A, Bouzayen M, Bouzid S (2014) Ethylene response factor Sl-ERF.B.3 is responsive to abiotic stresses and mediates salt and cold stress response regulation in tomato. Sci World J 2014:1–12Google Scholar
  28. Jayakumar B, Ana RM, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257CrossRefGoogle Scholar
  29. Ji H, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant 6:275–286CrossRefPubMedGoogle Scholar
  30. Jiang C, Belfield EJ, Mithani A, Visscher A, Ragoussis J, Mott R, Smith JAC, Harberd NP (2012) ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis. EMBO J 31:4359–4370CrossRefPubMedPubMedCentralGoogle Scholar
  31. Jiang C, Belfield EJ, Cao Y, Smith JAC, Harberd NP (2013) An Arabidopsis soil salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 25:3535–3552CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ju C, Chang C (2015) Mechanistic insights in ethylene perception and signal transduction. Plant Physiol 169:85–95CrossRefPubMedGoogle Scholar
  33. Ju C, Yoon GM, Shemansky JM, Lin DY, Ying ZI, Chang J, Garrett WM, Kessenbrock M, Groth G, Tucker ML, Cooper B, Kieber JJ, Chang C (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc Natl Acad Sci USA 109:19486–19491CrossRefPubMedPubMedCentralGoogle Scholar
  34. Jung JY, Shin R, Schachtman DP (2009) Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. Plant Cell 21:607–621CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229CrossRefPubMedGoogle Scholar
  36. Kimura S, Kawarazaki T, Nibori H, Michikawa M, Imai A, Kaya H, Kuchitsu K (2013) The CBL-interacting protein kinase CIPK26 is a novel interactor of Arabidopsis NADPH oxidase AtRbohF that negatively modulates its ROS-producing activity in a heterologous expression system. J Biochem 153:191–195CrossRefPubMedGoogle Scholar
  37. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lei G, Shen M, Li ZG, Zhang B, Duan KX, Wang N, Cao YR, Zhang WK, Ma B, Ling HQ, Chen SY, Zhang JS (2011) EIN2 regulates salt stress response and interacts with a MA3 domain-containing protein ECIP1 in Arabidopsis. Plant Cell Environ 34:1678–1692CrossRefPubMedGoogle Scholar
  39. León J, Castillo MC, Coego A, Lozano-Juste J, Mir R (2014) Diverse functional interactions between nitric oxide and abscisic acid in plant development and responses to stress. J Exp Bot 65:907–921CrossRefPubMedGoogle Scholar
  40. Li W, Ma M, Feng Y, Li H, Wang Y, Ma Y, Li M, An F, Guo H (2015a) EIN2-directed translational regulation of ethylene signaling in Arabidopsis. Cell 163:670–683CrossRefPubMedGoogle Scholar
  41. Li G, Xu W, Kronzucker HJ, Shi W (2015b) Ethylene is critical to the maintenance of primary root growth and Fe homeostasis under Fe stress in Arabidopsis. J Exp Bot 66:2041–2054CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lin H, Yang Y, Quan R, Mendoza I, Wu Y, Du W, Zhao S, Schumaker KS, Pardo JM, Guo Y (2009) Phosphorylation of SOS3-LIKE CALCIUM BINDING PROTEIN8 by SOS2 protein kinase stabilizes their protein complex and regulates salt tolerance in Arabidopsis. Plant Cell 21:1607–1619CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, Hao F (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63:305–317CrossRefPubMedGoogle Scholar
  44. Mäser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagami M, Yamaguchi K, Nishimura M, Uozumi N, Robertson W, Sussman MR, Schroeder JI (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531:157–161CrossRefPubMedGoogle Scholar
  45. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49:1135–1149CrossRefPubMedGoogle Scholar
  46. Merchante C, Alonso JM, Stepanova AN (2013) Ethylene signaling: simple ligand, complex regulation. Curr Opin Plant Biol 16:554–560CrossRefPubMedGoogle Scholar
  47. Merchante C, Brumos J, Yun J, Hu Q, Spencer KR, Enríquez P, Binder BM, Heber S, Stepanova AN, Alonso JM (2015) Gene-specific translation regulation mediated by the hormone-signaling molecule EIN2. Cell 163:684–697CrossRefPubMedGoogle Scholar
  48. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489CrossRefPubMedGoogle Scholar
  49. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467CrossRefPubMedGoogle Scholar
  50. Mittler R, Vanderauwera S, Gollery M, Van BF (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefPubMedGoogle Scholar
  51. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: The new wave? Trends Plant Sci 16:300–309CrossRefPubMedGoogle Scholar
  52. Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178CrossRefPubMedPubMedCentralGoogle Scholar
  53. Mori IC, Schroeder JI (2004) Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol 135:702–708CrossRefPubMedPubMedCentralGoogle Scholar
  54. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  55. Murata Y, Mori IC, Munemasa S (2015) Diverse stomatal signaling and the signal integration mechanism. Annu Rev Plant Biol 66:369–392CrossRefPubMedGoogle Scholar
  56. Peng J, Li Z, Wen X, Li W, Shi H, Yang L, Zhu H, Guo H (2014) Salt-induced stabilization of EIN3/EIL1 confers salinity tolerance by deterring ROS accumulation in Arabidopsis. PLoS Genet 10:e1004664CrossRefPubMedPubMedCentralGoogle Scholar
  57. Pottosin I, Buendía AMV, Bose J, Jazo IZ, Shabala S, Dobrovinskaya O (2014) Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot 65:1271–1283CrossRefPubMedGoogle Scholar
  58. Qiao H, Shen Z, Huang SS, Schmitz RJ, Urich MA, Briggs SP, Ecker JR (2012) Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338:390–393CrossRefPubMedPubMedCentralGoogle Scholar
  59. Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441CrossRefPubMedPubMedCentralGoogle Scholar
  60. Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124CrossRefPubMedGoogle Scholar
  61. Schachtman DP (2015) The role of ethylene in plant responses to K+ deficiency. Front Plant Sci 6:1153CrossRefPubMedPubMedCentralGoogle Scholar
  62. Schachtman DP, Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370:655–658CrossRefPubMedGoogle Scholar
  63. Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669CrossRefPubMedGoogle Scholar
  64. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901CrossRefPubMedPubMedCentralGoogle Scholar
  65. Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832CrossRefPubMedPubMedCentralGoogle Scholar
  66. Shinozaki K, Dennis ES (2003) Cell signalling and gene regulation: global analyses of signal transduction and gene expression profiles. Curr Opin Plant Biol 6:405–409CrossRefPubMedGoogle Scholar
  67. Sirichandra C, Gu D, Hu HC, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S, Kwak JM (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583:2982–2986CrossRefPubMedGoogle Scholar
  68. Smith AM, Coupland G, Dolan L, Harberd N, Jones J, Martin C, Sablowski R, Amey A (2010) Plant biology. USA Garland Science, Taylor & Francis Group, LLC, New YorkGoogle Scholar
  69. Steffens B (2014) The role of ethylene and ROS in salinity, heavy metal, and flooding. Front Plant Sci 5:685CrossRefPubMedPubMedCentralGoogle Scholar
  70. Steinhorst L, Kudla J (2014) Signaling in cells and organisms—calcium holds the line. Curr Opin Plant Biol 22:14–21CrossRefPubMedGoogle Scholar
  71. Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545CrossRefPubMedPubMedCentralGoogle Scholar
  72. Sun J, Wang MJ, Ding MQ, Deng SR, Liu MQ, Lu CF, Zhou XY, Shen X, Zheng XJ, Zhang ZK, Song J, Hu ZM, Xu Y, Chen SL (2010) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ 33:943–958CrossRefPubMedGoogle Scholar
  73. Sunarpi Horie T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938CrossRefPubMedGoogle Scholar
  74. Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2015) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138:2337–2343CrossRefGoogle Scholar
  75. Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Method Enzymol 428:419–438CrossRefGoogle Scholar
  76. Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl 1):S131–S151PubMedPubMedCentralGoogle Scholar
  77. Wang Y, Liu C, Li K, Sun F, Hu H, Li X, Zhao Y, Han C, Zhang W, Duan Y, Liu M, Li X (2007) Arabidopsis EIN2 modulates stress response through abscisic acid response pathway. Plant Mol Biol 64:633–644CrossRefPubMedGoogle Scholar
  78. Wen X, Zhang C, Ji Y, Zhao Q, He W, An F, Jiang L, Guo H (2012) Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Res 22:1613–1616CrossRefPubMedPubMedCentralGoogle Scholar
  79. Wilkinson S, Davies WJ (2009) Ozone suppresses soil drying- and abscisic acid (ABA)-induced stomatal closure via an ethylene-dependent mechanism. Plant Cell Environ 32:949–959CrossRefPubMedGoogle Scholar
  80. Wilson RL, Kim H, Bakshi A, Binder BM (2014) The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiol 165:1353–1366CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wu L, Zhang Z, Zhang H, Wang XC, Huang R (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiol 148:1953–1963CrossRefPubMedPubMedCentralGoogle Scholar
  82. Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66:2839–2856CrossRefPubMedGoogle Scholar
  83. Xiong L, Lee Bh, Ishitani M, Lee H, Zhang C, Zhu JK (2001) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes 15:1971–1984CrossRefGoogle Scholar
  84. Xu H, Liu Q, Yao T, Fu X (2014) Shedding light on integrative GA signaling. Curr Opin Plant Biol 21:89–95CrossRefPubMedGoogle Scholar
  85. Yang Q, Chen ZZ, Zhou XF, Yin HB, Li X, Xin XF, Hong XH, Zhu JK, Gong Z (2009) Overexpression of SOS (salt overly sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2:22–31CrossRefPubMedGoogle Scholar
  86. Yang L, Zu YG, Tang ZH (2013) Ethylene improves Arabidopsis salt tolerance mainly via retaining K+ in shoots and roots rather than decreasing tissue Na+ content. Environ Exp Bot 86:60–69CrossRefGoogle Scholar
  87. Yang C, Ma B, He SJ, Xiong Q, Duan KX, Yin CC, Chen H, Lu X, Chen SY, Zhang JS (2015) MAOHUZI6/ETHYLENE INSENSITIVE3-LIKE1 and ETHYLENE INSENSITIVE3-LIKE2 regulate ethylene response of roots and coleoptiles and negatively affect salt tolerance in rice. Plant Physiol 169:148–165CrossRefPubMedPubMedCentralGoogle Scholar
  88. Zhang H, Huang Z, Xie B, Chen Q, Tian X, Zhang X, Zhang H, Lu X, Huang D, Huang R (2004) The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220:262–270CrossRefPubMedGoogle Scholar
  89. Zhang F, Wang Y, Yang Y, Wu H, Wang D, Liu J (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30:775–785CrossRefPubMedGoogle Scholar
  90. Zhang L, Li ZF, Quan RD, Li GJ, Wang RG, Huang RF (2011) An AP2 domain-containing gene, ESE1, targeted by the ethylene signaling component EIN3 is important for the salt response in Arabidopsis. Plant Physiol 157:854–865CrossRefPubMedPubMedCentralGoogle Scholar
  91. Zhao Q, Guo HW (2011) Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol Plant 4:626–634CrossRefPubMedGoogle Scholar
  92. Zheng Y, Zhu Z (2016) Relaying the ethylene signal: new roles for EIN2. Trends Plant Sci 21:2–4CrossRefPubMedGoogle Scholar
  93. Zhou H, Lin H, Chen S, Becker K, Yang Y, Zhao J, Kudla J, Schumaker KS, Guo Y (2015) Inhibition of the Arabidopsis salt overly sensitive pathway by 14-3-3 proteins. Plant Cell 26:1166–1182CrossRefGoogle Scholar
  94. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273CrossRefPubMedPubMedCentralGoogle Scholar
  95. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.State Key Laboratory of Plant Physiology and Biochemistry, College of Biological SciencesChina Agricultural UniversityBeijingChina
  2. 2.Department of Plant SciencesUniversity of OxfordOxfordUK

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