Home LiteratureArticle Details
PMID: 22936567 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas.

Science (New York, N.Y.) ·Vol. 338 ·No. 6105 ·2012-10-19 ·Pages 390-3

Qiao H, Shen Z, Huang SS, Schmitz RJ, Urich MA, Briggs SP, Ecker JR

Abstract

Ethylene gas is essential for many developmental processes and stress responses in plants. ETHYLENE INSENSITIVE2 (EIN2), an NRAMP-like integral membrane protein, plays an essential role in ethylene signaling, but its function remains enigmatic. Here we report that phosphorylation-regulated proteolytic processing of EIN2 triggers its endoplasmic reticulum (ER)-to-nucleus translocation. ER-tethered EIN2 shows CONSTITUTIVE TRIPLE RESPONSE1 (CTR1) kinase-dependent phosphorylation. Ethylene triggers dephosphorylation at several sites and proteolytic cleavage at one of these sites, resulting in nuclear translocation of a carboxyl-terminal EIN2 fragment (EIN2-C'). Mutations that mimic EIN2 dephosphorylation, or inactivate CTR1, show constitutive cleavage and nuclear localization of EIN2-C' and EIN3 and EIN3-LIKE1-dependent activation of ethylene responses. These findings uncover a mechanism of subcellular communication whereby ethylene stimulates phosphorylation-dependent cleavage and nuclear movement of the EIN2-C' peptide, linking hormone perception and signaling components in the ER with nuclear-localized transcriptional regulators.

MeSH Terms
Active Transport, Cell Nucleus Arabidopsis/drug effects,metabolism Arabidopsis Proteins/genetics,metabolism Cell Nucleus/metabolism Endoplasmic Reticulum/metabolism Ethylenes/metabolism,pharmacology Gases/metabolism,pharmacology Mutation Nuclear Localization Signals/genetics,metabolism Phosphorylation Protein Kinases/metabolism Proteolysis Receptors, Cell Surface/genetics,metabolism
Chemicals
Arabidopsis Proteins EIN2 protein, Arabidopsis Ethylenes Gases Nuclear Localization Signals Receptors, Cell Surface ethylene Protein Kinases CTR1 protein, Arabidopsis
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Qiao Hong
Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
Shen Zhouxin
Huang Shao-shan Carol
Schmitz Robert J
Urich Mark A
Briggs Steven P
Ecker Joseph R
References (22)
22 references, click to expand
  1. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis.
    Sci Signal. 2012 Jun 12;5(228):ra42 PMID: 22692423
  2. Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent.
    Plant Physiol. 2004 Oct;136(2):2921-7 PMID: 15466219
  3. Selected reaction monitoring for quantitative proteomics: a tutorial.
    Mol Syst Biol. 2008;4:222 PMID: 18854821
  4. EIN2, the central regulator of ethylene signalling, is localized at the ER membrane where it interacts with the ethylene receptor ETR1.
    Biochem J. 2009 Oct 23;424(1):1-6 PMID: 19769567
  5. Molecular association of the Arabidopsis ETR1 ethylene receptor and a regulator of ethylene signaling, RTE1.
    J Biol Chem. 2010 Dec 24;285(52):40706-13 PMID: 20952388
  6. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators.
    Science. 1993 Oct 22;262(5133):539-44 PMID: 8211181
  7. Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway.
    Genetics. 1995 Mar;139(3):1393-409 PMID: 7768447
  8. Ethylene receptors function as components of high-molecular-mass protein complexes in Arabidopsis.
    PLoS One. 2010 Jan 08;5(1):e8640 PMID: 20062808
  9. Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis.
    Genes Dev. 2009 Feb 15;23(4):512-21 PMID: 19196655
  10. 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
  11. Proteomic responses in Arabidopsis thaliana seedlings treated with ethylene.
    Mol Biosyst. 2011 Sep;7(9):2637-50 PMID: 21713283
  12. 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
  13. ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 May 12;95(10):5812-7 PMID: 9576967
  14. RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis.
    Cell. 1999 Apr 30;97(3):383-93 PMID: 10319818
  15. Ethylene signaling: new levels of complexity and regulation.
    Curr Opin Plant Biol. 2008 Oct;11(5):479-85 PMID: 18692429
  16. Phosphoproteomic analysis of ethylene-regulated protein phosphorylation in etiolated seedlings of Arabidopsis mutant ein2 using two-dimensional separations coupled with a hybrid quadrupole time-of-flight mass spectrometer.
    Proteomics. 2009 Mar;9(6):1646-61 PMID: 19253305
  17. Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis.
    Plant J. 2003 Jan;33(2):221-33 PMID: 12535337
  18. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana.
    Cell. 1998 Jul 24;94(2):261-71 PMID: 9695954
  19. New paradigm in ethylene signaling: EIN2, the central regulator of the signaling pathway, interacts directly with the upstream receptors.
    Plant Signal Behav. 2011 Jan;6(1):164-6 PMID: 21242723
  20. The biological impact of mass-spectrometry-based proteomics.
    Nature. 2007 Dec 13;450(7172):991-1000 PMID: 18075578
  21. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation.
    Science. 2012 Aug 3;337(6094):587-90 PMID: 22700657
  22. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis.
    Science. 1999 Jun 25;284(5423):2148-52 PMID: 10381874
Article Info
Journal
Science (New York, N.Y.)
Abbr.
Science
ISSN
1095-9203
Published
2012-10-19
Epub
2012-00-30
Pages
390-3
Language
English
Region
United States
NLM ID
0404511
PMCID
PMC3523706
Subset
IM
Grants
NHGRI NIH HHS · F32 HG004830 · United States
Howard Hughes Medical Institute · United States
NHGRI NIH HHS · F32-HG004830 · United States
Corrections
CommentIn
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: product@genelibs.com