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.
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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 311:91–94
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 26:2538–2553
Amtmann A, Sanders D (1999) Mechanisms of Na+ uptake by plant cells. Adv Bot Res 29:75–112
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
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 143:707–719
Cao YR, Chen SY, Zhang JS (2008) Ethylene signaling regulates salt stress response. Plant Signal Behav 3:761–763
Cheeseman JM (2015) The evolution of halophytes, glycophytes and crops, and its implications for food security under saline conditions. New Phytol 206:557–570
Chen YF, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Ann Bot 95:901–915
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 33:1815–1827
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 162:1566–1582
Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi HZ (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379
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 47:907–916
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 10:151
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 62:4875–4887
Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Ann Rev Plant Physiol 28:89–121
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 422:442–446
Frommer WB, Ludewig U, Rentsch D (1999) Taking transgenic plants with a pinch of salt. Science 285:1222–1223
Gallie DR (2015) Appearance and elaboration of the ethylene receptor family during land plant evolution. Plant Mol Biol 87:521–539
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 12:1117–1126
Greenway H, Munns RA (1980) Mechanisms of salt tolerance in non-halophytes. Annu Rev Plant Physiol 31:149–190
Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49
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 21:1328–1339
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 62:2657–2666
Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14:660–668
Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271
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 2014:1–12
Jayakumar B, Ana RM, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257
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 6:275–286
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 31:4359–4370
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 25:3535–3552
Ju C, Chang C (2015) Mechanistic insights in ethylene perception and signal transduction. Plant Physiol 169:85–95
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 109:19486–19491
Jung JY, Shin R, Schachtman DP (2009) Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. Plant Cell 21:607–621
Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229
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 153:191–195
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 22:2623–2633
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 34:1678–1692
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 65:907–921
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 163:670–683
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 66:2041–2054
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 21:1607–1619
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 63:305–317
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 531:157–161
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 49:1135–1149
Merchante C, Alonso JM, Stepanova AN (2013) Ethylene signaling: simple ligand, complex regulation. Curr Opin Plant Biol 16:554–560
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 163:684–697
Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467
Mittler R, Vanderauwera S, Gollery M, Van BF (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
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 16:300–309
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 21:2163–2178
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 135:702–708
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Murata Y, Mori IC, Munemasa S (2015) Diverse stomatal signaling and the signal integration mechanism. Annu Rev Plant Biol 66:369–392
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:e1004664
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 65:1271–1283
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 338:390–393
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 99:8436–8441
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124
Schachtman DP (2015) The role of ethylene in plant responses to K+ deficiency. Front Plant Sci 6:1153
Schachtman DP, Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370:655–658
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669
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 97:6896–6901
Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832
Shinozaki K, Dennis ES (2003) Cell signalling and gene regulation: global analyses of signal transduction and gene expression profiles. Curr Opin Plant Biol 6:405–409
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 583:2982–2986
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 York
Steffens B (2014) The role of ethylene and ROS in salinity, heavy metal, and flooding. Front Plant Sci 5:685
Steinhorst L, Kudla J (2014) Signaling in cells and organisms—calcium holds the line. Curr Opin Plant Biol 22:14–21
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 134:1536–1545
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 33:943–958
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 44:928–938
Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2015) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138:2337–2343
Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Method Enzymol 428:419–438
Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl 1):S131–S151
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 64:633–644
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 22:1613–1616
Wilkinson S, Davies WJ (2009) Ozone suppresses soil drying- and abscisic acid (ABA)-induced stomatal closure via an ethylene-dependent mechanism. Plant Cell Environ 32:949–959
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 165:1353–1366
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 148:1953–1963
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 66:2839–2856
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 15:1971–1984
Xu H, Liu Q, Yao T, Fu X (2014) Shedding light on integrative GA signaling. Curr Opin Plant Biol 21:89–95
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 2:22–31
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 86:60–69
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 169:148–165
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 220:262–270
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 30:775–785
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 157:854–865
Zhao Q, Guo HW (2011) Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol Plant 4:626–634
Zheng Y, Zhu Z (2016) Relaying the ethylene signal: new roles for EIN2. Trends Plant Sci 21:2–4
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 26:1166–1182
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445
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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.).
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MZ, CJ, JACS and NPH conceived and wrote the paper.
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Zhang, M., Smith, J.A.C., Harberd, N.P. et al. The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol Biol 91, 651–659 (2016). https://doi.org/10.1007/s11103-016-0488-1
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DOI: https://doi.org/10.1007/s11103-016-0488-1