Home LiteratureArticle Details
PMID: 21737749 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis.

Zhu Z, An F, Feng Y, Li P, Xue L, A M, Jiang Z, Kim JM, To TK, Li W, Zhang X, Yu Q, Dong Z, Chen WQ, Seki M, Zhou JM, Guo H

Abstract

Jasmonate (JA) and ethylene (ET) are two major plant hormones that synergistically regulate plant development and tolerance to necrotrophic fungi. Both JA and ET induce the expression of several pathogenesis-related genes, while blocking either signaling pathway abolishes the induction of these genes by JA and ET alone or in combination. However, the molecular basis of JA/ET coaction and signaling interdependency is largely unknown. Here, we report that two Arabidopsis ET-stabilized transcription factors (EIN3 and EIL1) integrate ET and JA signaling in the regulation of gene expression, root development, and necrotrophic pathogen defense. Further studies reveal that JA enhances the transcriptional activity of EIN3/EIL1 by removal of JA-Zim domain (JAZ) proteins, which physically interact with and repress EIN3/EIL1. In addition, we find that JAZ proteins recruit an RPD3-type histone deacetylase (HDA6) as a corepressor that modulates histone acetylation, represses EIN3/EIL1-dependent transcription, and inhibits JA signaling. Our studies identify EIN3/EIL1 as a key integration node whose activation requires both JA and ET signaling, and illustrate transcriptional derepression as a common mechanism to integrate diverse signaling pathways in the regulation of plant development and defense.

MeSH Terms
Arabidopsis/genetics,growth & development,metabolism,microbiology Arabidopsis Proteins/genetics,metabolism Base Sequence Botrytis/pathogenicity Cyclopentanes/metabolism DNA, Plant/genetics DNA-Binding Proteins Ethylenes/metabolism Histone Deacetylases/metabolism Models, Biological Nuclear Proteins/genetics,metabolism Oxylipins/metabolism Plant Growth Regulators/metabolism Plant Roots/growth & development,metabolism Plants, Genetically Modified Repressor Proteins/genetics,metabolism Signal Transduction Transcription Factors/genetics,metabolism Two-Hybrid System Techniques
Chemicals
Arabidopsis Proteins Cyclopentanes DNA, Plant DNA-Binding Proteins EIL1 protein, Arabidopsis EIN3 protein, Arabidopsis Ethylenes Nuclear Proteins Oxylipins Plant Growth Regulators Repressor Proteins Transcription Factors jasmonic acid ethylene HDA6 protein, Arabidopsis Histone Deacetylases
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Zhu Ziqiang
College of Life Sciences, Peking University, Beijing 100871, China.
An Fengying
Feng Ying
Li Pengpeng
Xue Li
A Mu
Jiang Zhiqiang
Kim Jong-Myong
To Taiko Kim
Li Wei
Zhang Xinyan
Yu Qiang
Dong Zhi
Chen Wen-Qian
Seki Motoaki
Zhou Jian-Min
Guo Hongwei
References (50)
50 references, click to expand
  1. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses.
    Plant Cell. 2011 Feb;23(2):701-15 PMID: 21335373
  2. SA, JA, ethylene, and disease resistance in plants.
    Curr Opin Plant Biol. 1998 Aug;1(4):316-23 PMID: 10066607
  3. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins.
    Nature. 2008 Jan 24;451(7177):475-9 PMID: 18216856
  4. Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance.
    Proc Natl Acad Sci U S A. 2008 Mar 25;105(12):4945-50 PMID: 18356294
  5. Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis.
    PLoS Genet. 2009 Mar;5(3):e1000440 PMID: 19325888
  6. The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination.
    Plant Physiol. 2008 Jan;146(1):149-61 PMID: 18024558
  7. Why so repressed? Turning off transcription during plant growth and development.
    Curr Opin Plant Biol. 2009 Oct;12(5):628-36 PMID: 19700365
  8. COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis.
    Plant J. 2002 Nov;32(4):457-66 PMID: 12445118
  9. The role of ethylene in host-pathogen interactions.
    Annu Rev Phytopathol. 2006;44:393-416 PMID: 16602950
  10. Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation.
    Proc Natl Acad Sci U S A. 2004 Apr 27;101(17):6803-8 PMID: 15090654
  11. The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis.
    Plant Cell. 2011 Mar;23(3):1000-13 PMID: 21447791
  12. Multilevel interactions between ethylene and auxin in Arabidopsis roots.
    Plant Cell. 2007 Jul;19(7):2169-85 PMID: 17630276
  13. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases.
    Cell. 1993 Feb 12;72(3):427-41 PMID: 8431946
  14. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine.
    Proc Natl Acad Sci U S A. 2008 May 13;105(19):7100-5 PMID: 18458331
  15. Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-box 1 and 2 that requires EIN2 in Arabidopsis.
    Plant Cell. 2010 Jul;22(7):2384-401 PMID: 20647342
  16. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis.
    Plant Cell. 2007 Jul;19(7):2225-45 PMID: 17616737
  17. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis.
    Plant Cell. 2004 Aug;16(8):2117-27 PMID: 15258265
  18. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor.
    Nature. 2010 Nov 18;468(7322):400-5 PMID: 20927106
  19. The bHLH transcription factor MYC3 interacts with the Jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis.
    Mol Plant. 2011 Mar;4(2):279-88 PMID: 21242320
  20. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility.
    Science. 1998 May 15;280(5366):1091-4 PMID: 9582125
  21. NINJA connects the co-repressor TOPLESS to jasmonate signalling.
    Nature. 2010 Apr 1;464(7289):788-91 PMID: 20360743
  22. HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis.
    Plant Cell. 2005 Apr;17(4):1196-204 PMID: 15749761
  23. A downstream mediator in the growth repression limb of the jasmonate pathway.
    Plant Cell. 2007 Aug;19(8):2470-83 PMID: 17675405
  24. Regulation of gene expression by jasmonate hormones.
    Phytochemistry. 2009 Sep;70(13-14):1560-70 PMID: 19796781
  25. EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings.
    Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21431-6 PMID: 19948955
  26. Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis.
    Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2992-7 PMID: 12606727
  27. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense.
    Plant Cell. 2003 Jan;15(1):165-78 PMID: 12509529
  28. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.
    Nature. 2007 Aug 9;448(7154):661-5 PMID: 17637677
  29. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor.
    Cell. 2003 Dec 12;115(6):667-77 PMID: 14675532
  30. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor.
    Plant Cell. 2009 Aug;21(8):2220-36 PMID: 19717617
  31. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis.
    Plant Cell. 2004 Jul;16(7):1938-50 PMID: 15208388
  32. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway.
    Plant Cell. 1996 Dec;8(12):2309-23 PMID: 8989885
  33. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1.
    Genes Dev. 1998 Dec 1;12(23):3703-14 PMID: 9851977
  34. Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis.
    J Exp Bot. 2011 Mar;62(6):2143-54 PMID: 21321051
  35. HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis.
    J Exp Bot. 2008;59(2):225-34 PMID: 18212027
  36. Regulation of flowering time by histone acetylation in Arabidopsis.
    Science. 2003 Dec 5;302(5651):1751-4 PMID: 14593187
  37. Histone acetylation affects expression of cellular patterning genes in the Arabidopsis root epidermis.
    Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14469-74 PMID: 16176989
  38. The JAZ family of repressors is the missing link in jasmonate signalling.
    Nature. 2007 Aug 9;448(7154):666-71 PMID: 17637675
  39. The jasmonate signal pathway.
    Plant Cell. 2002;14 Suppl:S153-64 PMID: 12045275
  40. EIN3-dependent regulation of plant ethylene hormone signaling by two arabidopsis F box proteins: EBF1 and EBF2.
    Cell. 2003 Dec 12;115(6):679-89 PMID: 14675533
  41. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis.
    Science. 1999 Jun 25;284(5423):2148-52 PMID: 10381874
  42. The ethylene signaling pathway: new insights.
    Curr Opin Plant Biol. 2004 Feb;7(1):40-9 PMID: 14732440
  43. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate.
    Nat Chem Biol. 2009 May;5(5):344-50 PMID: 19349968
  44. Jasmonate passes muster: a receptor and targets for the defense hormone.
    Annu Rev Plant Biol. 2009;60:183-205 PMID: 19025383
  45. A molecular framework for light and gibberellin control of cell elongation.
    Nature. 2008 Jan 24;451(7177):480-4 PMID: 18216857
  46. Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response.
    J Exp Bot. 2010 Jul;61(12):3345-53 PMID: 20519338
  47. Plant hormones and signaling: common themes and new developments.
    Dev Cell. 2008 Apr;14(4):467-73 PMID: 18410724
  48. Interactions between jasmonates and ethylene in the regulation of root hair development in Arabidopsis.
    J Exp Bot. 2006;57(6):1299-308 PMID: 16531464
  49. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins.
    Cell. 1997 Jun 27;89(7):1133-44 PMID: 9215635
  50. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi.
    Plant J. 2002 Jan;29(1):23-32 PMID: 12060224
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2011-07-26
Epub
2011-00-07
Pages
12539-44
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3145709
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]