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Title: Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling

Abstract

The plant hormone jasmonate plays crucial roles in regulating plant responses to herbivorous insects and microbial pathogens and is an important regulator of plant growth and development. Key mediators of jasmonate signalling include MYC transcription factors, which are repressed by jasmonate ZIM-domain (JAZ) transcriptional repressors in the resting state. In the presence of active jasmonate, JAZ proteins function as jasmonate co-receptors by forming a hormone-dependent complex with COI1, the F-box subunit of an SCF-type ubiquitin E3 ligase. The hormone-dependent formation of the COI1–JAZ co-receptor complex leads to ubiquitination and proteasome-dependent degradation of JAZ repressors and release of MYC proteins from transcriptional repression. The mechanism by which JAZ proteins repress MYC transcription factors and how JAZ proteins switch between the repressor function in the absence of hormone and the co-receptor function in the presence of hormone remain enigmatic. In this paper, we show that Arabidopsis MYC3 undergoes pronounced conformational changes when bound to the conserved Jas motif of the JAZ9 repressor. The Jas motif, previously shown to bind to hormone as a partly unwound helix, forms a complete α-helix that displaces the amino (N)-terminal helix of MYC3 and becomes an integral part of the MYC N-terminal fold. In this position, themore » Jas helix competitively inhibits MYC3 interaction with the MED25 subunit of the transcriptional Mediator complex. Finally, our structural and functional studies elucidate a dynamic molecular switch mechanism that governs the repression and activation of a major plant hormone pathway.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [3];  [7];  [8];  [5];  [9];  [10];  [3];  [11]
  1. Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Biology and Biochemistry. Lab. of Structural Sciences; Michigan State Univ., East Lansing, MI (United States). DOE Plant Research Lab.; Nanjing Agricultural Univ. (China). College of Plant Protection
  2. Michigan State Univ., East Lansing, MI (United States). DOE Plant Research Lab.; Western Michigan Univ., Kalamazoo, MI (United States). Dept. of Biological Sciences
  3. Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Biology and Biochemistry. Lab. of Structural Sciences
  4. Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology. DOE Plant Research Lab.
  5. Scripps Research Inst., Jupiter, FL (United States). Dept. of Molecular Therapeutics. Translational Research Inst.
  6. Michigan State Univ., East Lansing, MI (United States). DOE Plant Research Lab.
  7. Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Biology and Biochemistry. Lab. of Structural Sciences; Zhejiang Sci-Tech Univ., Hangzhou (China). College of Life Sciences
  8. Northwestern Univ., Argonne, IL (United States). Synchrotron Research Center. Life Sciences Collaborative Access Team. Dept. of Molecular Pharmacology and Biological Chemistry
  9. Nanjing Agricultural Univ. (China). College of Plant Protection
  10. Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Biology and Biochemistry. Lab. of Structural Sciences; Chinese Academy of Sciences (CAS), Shanghai (China). Shanghai Inst. for Biological Sciences. Shanghai Inst. of Materia Medica. Center for Structure and Function of Drug Targets. VARI-SIMM Center. Key Lab. of Receptor Research
  11. Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology. DOE Plant Research Lab. Howard Hughes Medical Inst.
Publication Date:
Research Org.:
Van Andel Research Inst. (VARI), Grand Rapids, MI (United States); Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); Gordon and Betty Moore Foundation (United States); Van Andel Research Inst. (United States); Michigan Economic Development Corporation (United States); Michigan Technology Tri-Corridor (United States); Chinese Scholarship Council
Contributing Org.:
Nanjing Agricultural Univ. (China); Western Michigan Univ., Kalamazoo, MI (United States); Scripps Research Inst., Jupiter, FL (United States); Zhejiang Sci-Tech Univ., Hangzhou (China); Northwestern Univ., Argonne, IL (United States); Chinese Academy of Sciences (CAS), Shanghai (China)
OSTI Identifier:
1221449
Grant/Contract Number:  
FG02-91ER20021; AC02-06CH11357; R01 GM102545; R01AI060761; GBMF3037; 085P1000817
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Volume: 525; Journal Issue: 7568; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; Plant hormones; Structural biology; Plant signalling

Citation Formats

Zhang, Feng, Yao, Jian, Ke, Jiyuan, Zhang, Li, Lam, Vinh Q., Xin, Xiu-Fang, Zhou, X. Edward, Chen, Jian, Brunzelle, Joseph, Griffin, Patrick R., Zhou, Mingguo, Xu, H. Eric, Melcher, Karsten, and He, Sheng Yang. Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. United States: N. p., 2015. Web. doi:10.1038/nature14661.
Zhang, Feng, Yao, Jian, Ke, Jiyuan, Zhang, Li, Lam, Vinh Q., Xin, Xiu-Fang, Zhou, X. Edward, Chen, Jian, Brunzelle, Joseph, Griffin, Patrick R., Zhou, Mingguo, Xu, H. Eric, Melcher, Karsten, & He, Sheng Yang. Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. United States. https://doi.org/10.1038/nature14661
Zhang, Feng, Yao, Jian, Ke, Jiyuan, Zhang, Li, Lam, Vinh Q., Xin, Xiu-Fang, Zhou, X. Edward, Chen, Jian, Brunzelle, Joseph, Griffin, Patrick R., Zhou, Mingguo, Xu, H. Eric, Melcher, Karsten, and He, Sheng Yang. 2015. "Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling". United States. https://doi.org/10.1038/nature14661. https://www.osti.gov/servlets/purl/1221449.
@article{osti_1221449,
title = {Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling},
author = {Zhang, Feng and Yao, Jian and Ke, Jiyuan and Zhang, Li and Lam, Vinh Q. and Xin, Xiu-Fang and Zhou, X. Edward and Chen, Jian and Brunzelle, Joseph and Griffin, Patrick R. and Zhou, Mingguo and Xu, H. Eric and Melcher, Karsten and He, Sheng Yang},
abstractNote = {The plant hormone jasmonate plays crucial roles in regulating plant responses to herbivorous insects and microbial pathogens and is an important regulator of plant growth and development. Key mediators of jasmonate signalling include MYC transcription factors, which are repressed by jasmonate ZIM-domain (JAZ) transcriptional repressors in the resting state. In the presence of active jasmonate, JAZ proteins function as jasmonate co-receptors by forming a hormone-dependent complex with COI1, the F-box subunit of an SCF-type ubiquitin E3 ligase. The hormone-dependent formation of the COI1–JAZ co-receptor complex leads to ubiquitination and proteasome-dependent degradation of JAZ repressors and release of MYC proteins from transcriptional repression. The mechanism by which JAZ proteins repress MYC transcription factors and how JAZ proteins switch between the repressor function in the absence of hormone and the co-receptor function in the presence of hormone remain enigmatic. In this paper, we show that Arabidopsis MYC3 undergoes pronounced conformational changes when bound to the conserved Jas motif of the JAZ9 repressor. The Jas motif, previously shown to bind to hormone as a partly unwound helix, forms a complete α-helix that displaces the amino (N)-terminal helix of MYC3 and becomes an integral part of the MYC N-terminal fold. In this position, the Jas helix competitively inhibits MYC3 interaction with the MED25 subunit of the transcriptional Mediator complex. Finally, our structural and functional studies elucidate a dynamic molecular switch mechanism that governs the repression and activation of a major plant hormone pathway.},
doi = {10.1038/nature14661},
url = {https://www.osti.gov/biblio/1221449}, journal = {Nature (London)},
issn = {0028-0836},
number = 7568,
volume = 525,
place = {United States},
year = {Mon Aug 10 00:00:00 EDT 2015},
month = {Mon Aug 10 00:00:00 EDT 2015}
}

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Structural basis for RNA recognition by a dimeric PPR-protein complex
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Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade
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Dominant Alleles of the Basic Helix-Loop-Helix Transcription Factor ATR2 Activate Stress-Responsive Genes in Arabidopsis
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Multifarious Roles of Intrinsic Disorder in Proteins Illustrate Its Broad Impact on Plant Biology
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The OsJAZ1 degron modulates jasmonate signaling sensitivity during rice development
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Salt-inducible expression of OsJAZ8 improves resilience against salt-stress
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ZmMADS47 Regulates Zein Gene Transcription through Interaction with Opaque2
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A Novel Sweetpotato Transcription Factor Gene IbMYB116 Enhances Drought Tolerance in Transgenic Arabidopsis
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An effector from cotton bollworm oral secretion impairs host plant defense signaling
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Alternative splicing of OsLG3b controls grain length and yield in japonica rice
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PatJAZ6 Acts as a Repressor Regulating JA-Induced Biosynthesis of Patchouli Alcohol in Pogostemon Cablin
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Overexpression of OsMYC2 Results in the Up-Regulation of Early JA-Rresponsive Genes and Bacterial Blight Resistance in Rice
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The JA‐pathway MYC transcription factors regulate photomorphogenic responses by targeting HY5 gene expression
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Salt stress response triggers activation of the jasmonate signaling pathway leading to inhibition of cell elongation in Arabidopsis primary root
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The plant Mediator complex and its role in jasmonate signaling
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Differential expression of microRNAs in tomato leaves treated with different light qualities
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Comparative functional genomics analysis of bHLH gene family in rice, maize and wheat
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A Novel Sweetpotato Transcription Factor Gene IbMYB116 Enhances Drought Tolerance in Transgenic Arabidopsis
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Reconstitution of the Jasmonate Signaling Pathway in Plant Protoplasts
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Signaling Crosstalk between Salicylic Acid and Ethylene/Jasmonate in Plant Defense: Do We Understand What They Are Whispering?
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