Journal of Plant Growth Regulation

, Volume 26, Issue 2, pp 118–130 | Cite as

Ethylene Receptors: Ethylene Perception and Signal Transduction

  • Brenda P. Hall
  • Samina N. Shakeel
  • G. Eric SchallerEmail author


Ethylene is sensed by a family of receptors that can be divided into two subfamilies based on phylogenetic analysis and some shared structural features. In this review we focus on the mechanistic aspects of how the receptors function in plants to transduce the ethylene signal. Recent work has led to new insights into how ethylene binds to the receptors and how this binding may induce a conformational change to regulate signaling. Additional studies point to several possible mechanisms for signal output by the receptors, which may involve changes in enzymatic activity and/or conformational changes. Other studies indicate the importance of interactions, both physical and genetic, between the receptors and early components of the signaling pathway, in particular, the Raf-like kinase CTR1, which functions as an integral component of the ethylene receptor signaling complex. The current model for signaling in Arabidopsis supports differing contributions from the receptors, with subfamily-1 receptors playing a more significant role than the subfamily-2 receptors in transmitting the ethylene signal.


Ethylene Receptors Signal transduction 



The authors thank the Department of Energy (DE-FG02-05ER15704), the National Science Foundation (MCB-0430191), and the USDA-NRICGP (2004-35304-14907) for their research support.


  1. Abeles FB, Morgan PW, Saltveit ME Jr. 1992. Ethylene in Plant Biology. San Diego: Academic PressGoogle Scholar
  2. Baker MD, Wolanin PM, Stock JB. 2006. Signal transduction in bacterial chemotaxis. Bioessays 28:9–22PubMedCrossRefGoogle Scholar
  3. Barry CS, Giovannoni JJ. 2006. Ripening in the tomato Green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling. Proc Natl Acad Sci U S A 103:7923–7928PubMedCrossRefGoogle Scholar
  4. Barry CS, McQuinn RP, Thompson AJ, Seymour GB, Grierson D, Giovannoni JJ. 2005. Ethylene insensitivity conferred by the Green-ripe and Never-ripe 2 ripening mutants of tomato. Plant Physiol 138:267–275PubMedCrossRefGoogle Scholar
  5. Beyer JEM. 1976. Silver ion, a potent inhibitor of ethylene action in plants. Plant Physiol 58:268–271PubMedGoogle Scholar
  6. Binder BM, Mortimore LA, Stepanova AN, Ecker JR, Bleecker AB. 2004a. Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent. Plant Physiol 136:2921–2927PubMedCrossRefGoogle Scholar
  7. Binder BM, O’Malley RC, Wang W, Moore JM, Parks BM, Spalding EP, Bleecker AB. 2004b. Arabidopsis seedling growth response and recovery to ethylene. A kinetic analysis. Plant Physiol 136:2913–2920Google Scholar
  8. Bleecker AB. 1999. Ethylene perception and signaling: an evolutionary perspective. Trends Plant Sci 4:269–274PubMedCrossRefGoogle Scholar
  9. Bleecker AB, Estelle MA, Somerville C, Kende H. 1988. Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241:1086–1089CrossRefPubMedGoogle Scholar
  10. Burg SP, Burg EA. 1967. Molecular requirements for the biological activity of ethylene. Plant Physiol 42:144–152PubMedCrossRefGoogle Scholar
  11. Cancel JD, Larsen PB. 2002. Loss-of-function mutations in the ethylene receptor ETR1 cause enhanced sensitivity and exaggerated response to ethylene in Arabidopsis. Plant Physiol 129:1557–1567PubMedCrossRefGoogle Scholar
  12. Chang C, Stadler R. 2001. Ethylene hormone receptor action in Arabidopsis. Bioessays 23:619–627PubMedCrossRefGoogle Scholar
  13. Chang C, Kwok SF, Bleecker AB, Meyerowitz EM. 1993. Arabidopsis ethylene response gene ETR1: Similarity of product to two-component regulators. Science 262:539–544PubMedCrossRefGoogle Scholar
  14. Chen YF, Randlett MD, Findell JL, Schaller GE. 2002. Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J Biol Chem 277:19861–19866PubMedCrossRefGoogle Scholar
  15. Clark KL, Larsen PB, Wang X, Chang C. 1998. Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS1 ethylene receptors. Proc Natl Acad Sci U S A 95:5401–5406PubMedCrossRefGoogle Scholar
  16. Diaz J, Alvarez-Buylla ER. 2006. A model of the ethylene signaling pathway and its gene response in Arabidopsis thaliana: pathway cross-talk and noise-filtering properties. Chaos 16:023112PubMedCrossRefGoogle Scholar
  17. Gamble RL, Coonfield ML, Schaller GE. 1998. Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc Natl Acad Sci U S A 95:7825–7829PubMedCrossRefGoogle Scholar
  18. Gamble RL, Qu X, Schaller GE. 2002. Mutational analysis of the ethylene receptor ETR1: Role of the Histidine Kinase Domain In Dominant Ethylene Insensitivity. Plant Physiol 128:1428–1438PubMedCrossRefGoogle Scholar
  19. Gao Z, Chen YF, Randlett MD, Zhao XC, Findell JL, Kieber JJ, Schaller GE. 2003. Localization of the Raf-like kinase CTR1 to the endoplasmic reticulum of Arabidopsis through participation in ethylene receptor signaling complexes. J Biol Chem 278:34725–34732PubMedCrossRefGoogle Scholar
  20. Gilbert HF. 1997. Protein disulfide isomerase and assisted protein folding. J Biol Chem 272:29399–29402PubMedCrossRefGoogle Scholar
  21. Guzmán P, Ecker JR. 1990. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523PubMedCrossRefGoogle Scholar
  22. Hall AE, Bleecker AB. 2003. Analysis of combinatorial loss-of-function mutants in the Arabidopsis ethylene receptors reveals that the ers1 etr1 double mutant has severe developmental defects that are EIN2 dependent. Plant Cell 15:2032–2041PubMedCrossRefGoogle Scholar
  23. Hall AE, Chen QG, Findell JL, Schaller GE, Bleecker AB. 1999. The relationship between ethylene binding and dominant insensitivity conferred by mutant forms of the ETR1 ethylene receptor. Plant Physiol 121:291–299PubMedCrossRefGoogle Scholar
  24. Hall AE, Findell JL, Schaller GE, Sisler EC, Bleecker AB. 2000. Ethylene perception by the ERS1 protein in Arabidopsis. Plant Physiol 123:1449–1458PubMedCrossRefGoogle Scholar
  25. Hara-Nishimura I, Matsushima R. 2003. A wound-inducible organelle derived from endoplasmic reticulum: a plant strategy against environmental stresses? Curr Opin Plant Biol 6:583–588PubMedCrossRefGoogle Scholar
  26. Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, Yoo SD, Hwang I, Zhu T, Schafer E, Kudla J, Harter K. 2004. The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J 23:3290–3302PubMedCrossRefGoogle Scholar
  27. Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, Nourizadeh S, Alonso JM, Dailey WP, Dancis A, Ecker JR. 1999. RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97:383–393PubMedCrossRefGoogle Scholar
  28. Hiromura M, Yano M, Mori H, Inoue M, Kido H. 1998. Intrinsic ADP-ATP exchange activity is a novel function of the molecular chaperone, Hsp70. J Biol Chem 273:5435–5438PubMedCrossRefGoogle Scholar
  29. Hua J, Meyerowitz EM. 1998. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271PubMedCrossRefGoogle Scholar
  30. Hua J, Chang C, Sun Q, Meyerowitz EM. 1995. Ethylene sensitivity conferred by Arabidopsis ERS gene. Science 269:1712–1714PubMedCrossRefGoogle Scholar
  31. Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB, Ecker JR, Meyerowitz EM. 1998. Ein4 and ERS2 are members of the putative ethylene receptor family in Arabidopsis. Plant Cell 10:1321–1332PubMedCrossRefGoogle Scholar
  32. Huang Y, Li H, Hutchison CE, Laskey J, Kieber JJ. 2003. Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J 33:221–233PubMedCrossRefGoogle Scholar
  33. Hwang I, Chen HC, Sheen J. 2002. Two-component signal transduction pathways in Arabidopsis. Plant Physiol 129:500–515PubMedCrossRefGoogle Scholar
  34. Kieber JJ, Rothenberg M, Roman G, Feldman KA, Ecker JR. 1993. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:427–441PubMedCrossRefGoogle Scholar
  35. Klee HJ. 2004. Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiol 135:660–667PubMedCrossRefGoogle Scholar
  36. Lu Y, Hu Q, Yang C, Gao F. 2006. Histidine 89 is an essential residue for Hsp70 in the phosphate transfer reaction. Cell Stress Chaperones 11:148–153PubMedCrossRefGoogle Scholar
  37. Ma B, Cui ML, Sun HJ, Takada K, Mori H, Kamada H, Ezura H. 2006. Subcellular localization and membrane topology of the melon ethylene receptor CmERS1. Plant Physiol 141:587–597PubMedCrossRefGoogle Scholar
  38. Mason MG, Schaller GE. 2005. Histidine kinase activity and the regulation of ethylene signal transduction. Can J Bot 83:563–570CrossRefGoogle Scholar
  39. Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, Alonso JM, Ecker JR, Schaller GE. 2005. Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17:3007–3018PubMedCrossRefGoogle Scholar
  40. Moussatche P, Klee HJ. 2004. Autophosphorylation activity of the Arabidopsis ethylene receptor multigene family. J Biol Chem 279:48734–48741PubMedCrossRefGoogle Scholar
  41. Muller-Dieckmann HJ, Grantz AA, Kim SH. 1999. The structure of the signal receiver domain of the Arabidopsis thaliana ethylene receptor ETR1. Structure Fold Des 7:1547–1556PubMedCrossRefGoogle Scholar
  42. Neljubov DN. 1901. Uber die horizontale Nutation der Stengel von Pisum sativum und einiger anderen Pflanzen. Beih Bot Centralbl 10:128–139Google Scholar
  43. O’Malley RC, Rodriguez FI, Esch JJ, Binder BM, O’Donnell P, Klee HJ, Bleecker AB. 2005. Ethylene-binding activity, gene expression levels, and receptor system output for ethylene receptor family members from Arabidopsis and tomato. Plant J 41:651–659PubMedCrossRefGoogle Scholar
  44. Qu X, Schaller GE. 2004. Requirement of the histidine kinase domain for signal transduction by the ethylene receptor ETR1. Plant Physiol 136:2961–2970PubMedCrossRefGoogle Scholar
  45. Qu X, Hall BP, Gao Z, Schaller GE. 2007. A strong constitutive ethylene response phenotype conferred on Arabidopsis plants containing null mutations in the ethylene receptors ETR1 and ERS1. BMC Plant Biol 7:3PubMedCrossRefGoogle Scholar
  46. Resnick JS, Wen CK, Shockey JA, Chang C. 2006. REVERSION-TO-ETHYLENE SENSITIVITY1, a conserved gene that regulates ethylene receptor function in Arabidopsis. Proc Natl Acad Sci U S A 103:7917–7922PubMedCrossRefGoogle Scholar
  47. Rodriguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB. 1999. A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283:996–998PubMedCrossRefGoogle Scholar
  48. Sakai H, Hua J, Chen QG, Chang C, Medrano LJ, Bleecker AB, Meyerowitz EM. 1998. ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. Proc Natl Acad Sci U S A 95:5812–5817PubMedCrossRefGoogle Scholar
  49. Schaller GE, Bleecker AB. 1995. Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science 270:1809–1811PubMedCrossRefGoogle Scholar
  50. Schaller GE, Kieber JJ. 2002. Ethylene. In: Somerville C, Meyerowitz E. (eds). The Arabidopsis Book. Rockville, MD: American Society of Plant BiologistsGoogle Scholar
  51. Schaller GE, Ladd AN, Lanahan MB, Spanbauer JM, Bleecker AB. 1995. The ethylene response mediator ETR1 from Arabidopsis forms a disulfide-linked dimer. J Biol Chem 270:12526–12530PubMedCrossRefGoogle Scholar
  52. Schaller GE, Mathews DE, Gribskov M, Walker JC 2002. Two-component signaling elements and histidyl-aspartyl phosphorelays. In: Somerville C, Meyerowitz E. (eds). The Arabidopsis Book. Rockville, MD: American Society of Plant Biologists, pp 1–9Google Scholar
  53. Sisler EC, Serek M, Dupille E. 1996. Comparison of cyclopropenes, 1-methylcyclopropene and 3,3-dimethylcyclopropene, as an ethylene antagonist in plants. J Plant Growth Regul 18:169–174CrossRefGoogle Scholar
  54. Sisler EC, Alwain T, Goren R, Serek M, Apelbaum A. 2003. 1-substituted cyclopropenes: effective blocking agents for ethylene action in plants. J Plant Growth Regul 40:223–228CrossRefGoogle Scholar
  55. Staehelin LA. 1997. The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J 11:1151–1165PubMedCrossRefGoogle Scholar
  56. Stock AM, Robinson VL, Goudreau PN. 2000. Two-component signal transduction. Annu Rev Biochem 69:183–215PubMedCrossRefGoogle Scholar
  57. Takahashi H, Kobayashi T, Sato-Nara K, Tomita KO, Ezura H. 2002. Detection of ethylene receptor protein Cm-ERS1 during fruit development in melon (Cucumis melo L.). J Exp Bot 53:415–422PubMedCrossRefGoogle Scholar
  58. Tieman DM, Taylor MG, Ciardi JA, Klee HJ. 2000. The tomato ethylene receptors NR and LeETR4 are negative regulators of ethylene response and exhibit functional compensation within a multigene family. Proc Natl Acad Sci U S A 97:5663–5668PubMedCrossRefGoogle Scholar
  59. Vitale A, Denecke J. 1999. The endoplasmic reticulum-gateway of the secretory pathway. Plant Cell 11:615–628PubMedCrossRefGoogle Scholar
  60. Wang W, Hall AE, O’Malley R, Bleecker AB. 2003. Canonical histidine kinase activity of the transmitter domain of the ETR1 ethylene receptor from Arabidopsis is not required for signal transmission. Proc Natl Acad Sci U S A 100:352–357PubMedCrossRefGoogle Scholar
  61. Wang W, Esch JJ, Shiu S-H, Agula H, Binder BM, Chang C, Patterson SE, Bleecker AB. 2006. Identification of important regions for ethylene binding and signaling in the transmembrane domain of the ETR1 ethylene receptor of Arabidopsis. Plant Cell 18(12):3429–3442PubMedCrossRefGoogle Scholar
  62. Wilkinson JQ, Lanahan MB, Clark DG, Bleecker AB, Chang C, Meyerowitz EM, Klee HJ. 1997. A dominant mutant receptor from Arabidopsis confers ethylene insensitivity in heterologous plants. Nat Biotechnol 15:444–447PubMedCrossRefGoogle Scholar
  63. Woeste KE, Kieber JJ. 2000. A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. Plant Cell 12:443–455PubMedCrossRefGoogle Scholar
  64. Xie C, Zhang JS, Zhou HL, Li J, Zhang ZG, Wang DW, Chen SY. 2003. Serine/threonine kinase activity in the putative histidine kinase-like ethylene receptor NTHK1 from tobacco. Plant J 33:385–393PubMedCrossRefGoogle Scholar
  65. Xie F, Liu Q, Wen C-K. 2006. Receptor signal output mediated by the ETR1 N-terminus is primarily subfamily I receptors-dependent. Plant Physiol 142:492–508PubMedCrossRefGoogle Scholar
  66. Yau CP, Wang L, Yu M, Zee SY, Yip WK. 2004. Differential expression of three genes encoding an ethylene receptor in rice during development, and in response to indole-3-acetic acid and silver ions. J Exp Bot 55:547–556PubMedCrossRefGoogle Scholar
  67. Zhang ZG, Zhou HL, Chen T, Gong Y, Cao WH, Wang YJ, Zhang JS, Chen SY. 2004. Evidence for serine/threonine and histidine kinase activity in the tobacco ethylene receptor protein NTHK2. Plant Physiol 136:2971–2981PubMedCrossRefGoogle Scholar
  68. Zhao XC, Qu X, Mathews DE, Schaller GE. 2002. Effect of ethylene pathway mutations upon expression of the ethylene receptor ETR1 from arabidopsis. Plant Physiol 130:1983-1991PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Brenda P. Hall
    • 1
  • Samina N. Shakeel
    • 1
  • G. Eric Schaller
    • 1
    Email author
  1. 1.Department of Biological SciencesDartmouth CollegeHanoverUSA

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