Plant Molecular Biology

, Volume 64, Issue 6, pp 633–644

Arabidopsis EIN2 modulates stress response through abscisic acid response pathway

  • Youning Wang
  • Chuang Liu
  • Kexue Li
  • Feifei Sun
  • Haizhou Hu
  • Xia Li
  • Yankun Zhao
  • Chunyu Han
  • Wensheng Zhang
  • Yunfeng Duan
  • Mengyu Liu
  • Xia Li


The nuclear protein ETHYLENE INSENSITIVE2 (EIN2) is a central component of the ethylene signal transduction pathway in plants, and plays an important role in mediating cross-links between several hormone response pathways, including abscisic acid (ABA). ABA mediates stress responses in plants, but there is no report on the role of EIN2 on plant response to salt and osmotic stresses. Here, we show that EIN2 gene regulates plant response to osmotic and salt stress through an ABA-dependent pathway in Arabidopsis. The expression of the EIN2 gene is down-regulated by salt and osmotic stress. An Arabidopsis EIN2 null mutant was supersensitive to both salt and osmotic stress conditions. Disruption of EIN2 specifically altered the expression pattern of stress marker gene RD29B in response to the stresses, but not the stress- or ABA-responsive genes RD29A and RD22, suggesting EIN2 modulates plant stress responses through the RD29B branch of the ABA response. Furthermore, disruption of EIN2 caused substantial increase in ABA. Lastly, our data showed that mutations of other key genes in ethylene pathway also had altered sensitivity to abiotic stresses, indicating that the intact ethylene may involve in the stress response. Taken together, the results identified EIN2 as a cross-link node in ethylene, ABA and stress signaling pathways, and EIN2 is necessary to induce developmental arrest during seed germination, and seedling establishment, as well as subsequent vegetative growth, thereby allowing the survival and growth of plants under the adverse environmental conditions.


Stress signaling pathway Ethylene Insensitive 2 Ethylene Abscisic acid ABA Gene expression Arabidopsis thaliana 



Abscisic acid


Ethylene Responsive 1


Constitutive Triple Response 1


Ethylene Insensitive 2


Ethylene Insensitive 3


9-cis-epoxycarotenoid dioxygenase3


Desiccation responsive genes

RD29B/ RD22

ABA responsive genes


ABA insensitive 3


ABA insensitive 5


ABA insensitive 8


Zeaxanthin epoxidase


  1. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Shinozaki K (1997) Role of MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868PubMedCrossRefGoogle Scholar
  2. Abe H, Urao T, Ito T, Seki S, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78PubMedCrossRefGoogle Scholar
  3. Abeles FB, Morgan PW, Saltveit ME Jr (1992) Ethylene in plant biology, 2nd edn. Academic Press, San DiegoGoogle Scholar
  4. Achard P, Hui C, 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 311:91–94PubMedCrossRefGoogle Scholar
  5. Alonso JM, Stepanova AN (2004) The ethylene signaling pathway. Science 306:1513–1515PubMedCrossRefGoogle Scholar
  6. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152PubMedCrossRefGoogle Scholar
  7. Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12:1103–1115PubMedCrossRefGoogle Scholar
  8. Bent AF, Innes RW, Ecker JR, Staskawicz BJ (1992) Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Mol Plant-Microbe Interact 5:372–378PubMedGoogle Scholar
  9. Blatt MR (2000) Cellular signaling and volume control in stomatal movements in plants. Annu Rev Cell Dev Biol 16:221–241PubMedCrossRefGoogle Scholar
  10. Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, MD, pp 1158–1249Google Scholar
  11. Brocard-Gifford I, Lynch TJ, Garcia ME, Malhotra B, Finkelstein RR (2004) The Arabidopsis thaliana ABSCISIC ACID-INSENSITIVE8 locus encodes a novel protein mediating abscisic acid and sugar responses essential for growth. Plant Cell 16:406–421PubMedCrossRefGoogle Scholar
  12. Cao WH, Liu J, He XJ, Mu RL, Zhou H, Chen SY, Zhang JS (2006) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143:707–719PubMedCrossRefGoogle Scholar
  13. Cary AJ, Liu W, Howell SH (1995) Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol 107:1075–1082PubMedCrossRefGoogle Scholar
  14. Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89:1133–1144PubMedCrossRefGoogle Scholar
  15. Fujimoto S, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404PubMedCrossRefGoogle Scholar
  16. Fujita H, Syono K (1996) Genetic analysis of the effects of polar auxin transport inhibitors on root growth in Arabidopsis thaliana. Plant Cell Physiol 37:1094–1101PubMedGoogle Scholar
  17. 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 12:1117–1126PubMedCrossRefGoogle Scholar
  18. Gosti F, Bertauche N, Vartanian N, Giraudat J (1995) Abscisic acid-dependent and -independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol Gen Genet 246:10–18PubMedCrossRefGoogle Scholar
  19. Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49PubMedCrossRefGoogle Scholar
  20. Hamilton DW, Hills A, Kohler B, Blatt MR (2000) Ca21 channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4967–4972PubMedCrossRefGoogle Scholar
  21. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedCrossRefGoogle Scholar
  22. Ishitani M, Xiong L, Stevenson B, Zhu JK (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9:1935–1949PubMedCrossRefGoogle Scholar
  23. Kang J, Choi H, Im M, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357PubMedCrossRefGoogle Scholar
  24. Khan AA, Huang XL (1988) Synergistic enhancement of ethylene production and germination with kinetin and 1-aminocyclopropane-1-carboxylic acid in lettuce seeds exposed to salinity stress. Plant Physiol 87:847–852PubMedGoogle Scholar
  25. Kim CY, Liu Y, Thorne ET, Yang H, Fukushige H, Gassmann W, Hildebrand D, Sharp RE, Zhang S (2003) Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 15:2707–2708PubMedCrossRefGoogle Scholar
  26. Kohler B, Blatt MR (2002) Protein phosphorylation activates the guard cell Ca2+ channel and is a prerequisite for gating by abscisic acid. Plant J 32:185–194PubMedCrossRefGoogle Scholar
  27. Lopez-Molina L, Mongrand S, Chua N-H (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98:4782–4787PubMedCrossRefGoogle Scholar
  28. Lorenzo O, Piqueras R, Sanchez-Serrano J, Solano R (2003) ETHYLENE RESPONSE FACTOR1integrates signals from ethylene and jasmonate pathway in plant defense. Plant Cell 15:165–178PubMedCrossRefGoogle Scholar
  29. Ma S, Gong Q, Bohnert HJ (2006) Dissecting salt stress pathways. J Exp Bot 57:1097–1107PubMedCrossRefGoogle Scholar
  30. MacRobbie EA (2000) ABA activates multiple Ca(2+) fluxes in stomatal guard cells, triggering vacuolar K(+)(Rb(+)) release. Proc Natl Acad Sci USA 97:12361–12368PubMedCrossRefGoogle Scholar
  31. Mizoguchi T, Ichimura K, Shinozaki K (1997) Environmental stress response in plants: the role of mitogen-activated protein kinases. Trends Biotechnol 15:15–19PubMedCrossRefGoogle Scholar
  32. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497CrossRefGoogle Scholar
  33. Nakashima K, Fujita Y, Katsura K, Maruyama K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Transcriptional regulation of ABI3- and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol Biol 60:51–68PubMedCrossRefGoogle Scholar
  34. Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress: the central role of ‘‘redox’’ and abscisic acid-mediated controls. Plant Physiol 129:460–468PubMedCrossRefGoogle Scholar
  35. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734PubMedCrossRefGoogle Scholar
  36. Ruggiero B, Koiwa H, Manabe H, Quist TM, Inan G, Saccardo F, Joly RT, Hasegawa PM, Bressan RA, Maggio A (2004) Uncoupling the effects of abscisic acid on plant growth and water relations. analysis of sto1/nced3, an abscisic acid-deficient but salt stress-tolerant mutant in Arabidopsis. Plant Physiol 136:3134–3147PubMedCrossRefGoogle Scholar
  37. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658PubMedCrossRefGoogle Scholar
  38. Sharp RE (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ 25:211–222PubMedCrossRefGoogle Scholar
  39. Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 53:33–37PubMedCrossRefGoogle Scholar
  40. Sharp RE, LeNoble ME, Else MA, Thorne ET, Gherardi F (2000) Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene. J Exp Bot 51:1575–1584PubMedCrossRefGoogle Scholar
  41. Shibuya K, Barry KG, Ciardi JA, Loucas HM, Underwood BA, Nourizadeh S, Ecker JR, Klee HJ, Clark DG (2004) The central role of PhEIN2 in ethylene responses throughout plant development in Petunia. Plant Physiol 136:2900–2912PubMedCrossRefGoogle Scholar
  42. Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223PubMedGoogle Scholar
  43. Spollen WG, LeNoble ME, Samuels TD, Bernstein N, Sharp RE (2000) Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiol 122:967–976PubMedCrossRefGoogle Scholar
  44. Su W, Howell SH (1992) A single genetic locus ckr1, defines Arabidopsis mutants in which root growth is resistant to low concentrations of cytokinin. Plant Physiol 99:1569–1574PubMedCrossRefGoogle Scholar
  45. Tang D, Christiansen KM, Innes RW (2005) Regulation of plant disease resistance, stress responses, cell death and ethylene signaling in Arabidopsis by the EDR1 protein kinase. Plant Physiol 138:1018–1026PubMedCrossRefGoogle Scholar
  46. Tena G, Asai T, Chiu WL, Sheen J (2001) Plant mitogen-activated protein kinase signaling cascades. Curr Opin Plant Biol 4:392–400PubMedCrossRefGoogle Scholar
  47. Thomma BP, Eggermont K, Tierens KF, Broekaert WF (1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol 121:1093–1102PubMedCrossRefGoogle Scholar
  48. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637PubMedCrossRefGoogle Scholar
  49. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14S:165–183Google Scholar
  50. Yamaguchi-Shinozaki K, Shinozaki K (1993) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 238:17–25PubMedGoogle Scholar
  51. Yamaguchi-Shinozaki K, Shinozaki K (1994) A nove1 cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264PubMedCrossRefGoogle Scholar
  52. Yang YM, Xu CN, Wang BM, Jia JZ (2001) Effects of plant growth regulators on secondary wall thickening of cotton fibers. Plant Growth Regul 35:233–237CrossRefGoogle Scholar
  53. Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6:520–527PubMedCrossRefGoogle Scholar
  54. Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448PubMedCrossRefGoogle Scholar
  55. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCrossRefGoogle Scholar
  56. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Youning Wang
    • 1
  • Chuang Liu
    • 1
  • Kexue Li
    • 1
  • Feifei Sun
    • 1
  • Haizhou Hu
    • 2
  • Xia Li
    • 1
  • Yankun Zhao
    • 1
  • Chunyu Han
    • 1
  • Wensheng Zhang
    • 1
  • Yunfeng Duan
    • 1
  • Mengyu Liu
    • 1
  • Xia Li
    • 1
  1. 1.The State Key Laboratory of Plant Cell and Chromosome Engineering, Center for Agricultural Resources, Institute of Genetics and Developmental BiologyChinese Academy of ScienceShijiazhuangP.R. China
  2. 2.College of AgronomyShandong Agricultural UniversityTai’anP.R. China

Personalised recommendations