skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Structural insights into alternative splicing-mediated desensitization of jasmonate signaling

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [4];  [4];  [5];  [6];  [7];  [8]; ORCiD logo [9]
  1. College of Plant Protection, Nanjing Agricultural University, 210095, Nanjing, Jiangsu Province, China,, Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Laboratory of Structural Sciences, Van Andel Research Institute, Grand Rapids, MI 49503,, Laboratory of Structural Biology and Biochemistry, Van Andel Research Institute, Grand Rapids, MI 49503,, State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan 430072, China,
  2. Laboratory of Structural Sciences, Van Andel Research Institute, Grand Rapids, MI 49503,, Laboratory of Structural Biology and Biochemistry, Van Andel Research Institute, Grand Rapids, MI 49503,
  3. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Plant Biology, Michigan State University, East Lansing, MI 48824,
  4. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,
  5. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824,, Plant Resilience Institute, Michigan State University, East Lansing, MI 48824,
  6. Laboratory of Structural Sciences, Van Andel Research Institute, Grand Rapids, MI 49503,, Key Laboratory of Receptor Research, VARI-SIMM Center, Center for Structure and Function of Drug Targets, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China,
  7. College of Plant Protection, Nanjing Agricultural University, 210095, Nanjing, Jiangsu Province, China,
  8. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Plant Biology, Michigan State University, East Lansing, MI 48824,, Plant Resilience Institute, Michigan State University, East Lansing, MI 48824,, Howard Hughes Medical Institute, Michigan State University, East Lansing, MI 48824
  9. Laboratory of Structural Biology and Biochemistry, Van Andel Research Institute, Grand Rapids, MI 49503,

Jasmonate ZIM-domain (JAZ) transcriptional repressors play a key role in regulating jasmonate (JA) signaling in plants. Below a threshold concentration of jasmonoyl isoleucine (JA-Ile), the active form of JA, the C-terminal Jas motif of JAZ proteins binds MYC transcription factors to repress JA signaling. With increasing JA-Ile concentration, the Jas motif binds to JA-Ile and the COI1 subunit of the SCFCOI1 E3 ligase, which mediates ubiquitination and proteasomal degradation of JAZ repressors, resulting in derepression of MYC transcription factors. JA signaling subsequently becomes desensitized, in part by feedback induction of JAZ splice variants that lack the C-terminal Jas motif but include an N-terminal cryptic MYC-interaction domain (CMID). The CMID sequence is dissimilar to the Jas motif and is incapable of recruiting SCFCOI1, allowing CMID-containing JAZ splice variants to accumulate in the presence of JA and to re-repress MYC transcription factors as an integral part of reestablishing signal homeostasis. The mechanism by which the CMID represses MYC transcription factors remains elusive. Here we describe the crystal structure of the MYC3–CMIDJAZ10 complex. In contrast to the Jas motif, which forms a single continuous helix when bound to MYC3, the CMID adopts a loop–helix–loop–helix architecture with modular interactions with both the Jas-binding groove and the backside of the Jas-interaction domain of MYC3. In conclusion, this clamp-like interaction allows the CMID to bind MYC3 tightly and block access of MED25 (a subunit of the Mediator coactivator complex) to the MYC3 transcriptional activation domain, shedding light on the enigmatic mechanism by which JAZ splice variants desensitize JA signaling.

Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); Michigan State Univ., East Lansing, MI (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
FG02-91ER20021; AC02-06CH11357
OSTI ID:
1341769
Alternate ID(s):
OSTI ID: 1356423
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 114 Journal Issue: 7; ISSN 0027-8424
Publisher:
Proceedings of the National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 47 works
Citation information provided by
Web of Science

References (42)

The Arabidopsis bHLH Transcription Factors MYC3 and MYC4 Are Targets of JAZ Repressors and Act Additively with MYC2 in the Activation of Jasmonate Responses journal February 2011
Refinement of Macromolecular Structures by the Maximum-Likelihood Method journal May 1997
Regulation and Function of Arabidopsis JASMONATE ZIM -Domain Genes in Response to Wounding and Herbivory journal January 2008
The Arabidopsis Mediator Subunit MED25 Differentially Regulates Jasmonate and Abscisic Acid Signaling through Interacting with the MYC2 and ABI5 Transcription Factors journal July 2012
Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling journal August 2015
Coot model-building tools for molecular graphics journal November 2004
Genome-Wide Analysis of Ethylene-Responsive Element Binding Factor-Associated Amphiphilic Repression Motif-Containing Transcriptional Regulators in Arabidopsis journal January 2010
Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors journal July 2015
COI1: An Arabidopsis Gene Required for Jasmonate-Regulated Defense and Fertility journal May 1998
A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein journal September 2008
Jasmonates: Structural Requirements for Lipid-Derived Signals Active in Plant Stress Responses and Development journal December 2009
Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor journal October 2010
Role of NINJA in root jasmonate signaling journal September 2013
The Arabidopsis CORONATINE INSENSITIVE1 Protein Is a Jasmonate Receptor journal August 2009
A Downstream Mediator in the Growth Repression Limb of the Jasmonate Pathway journal August 2007
Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis journal July 2011
Site-Specific Biotinylation of Purified Proteins Using BirA book December 2014
MEDIATOR25 Acts as an Integrative Hub for the Regulation of Jasmonate-Responsive Gene Expression in Arabidopsis journal July 2012
The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins journal July 2009
The JAZ family of repressors is the missing link in jasmonate signalling journal July 2007
Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory journal August 2003
The Oxylipin Signal Jasmonic Acid Is Activated by an Enzyme That Conjugates It to Isoleucine in Arabidopsis journal July 2004
COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine journal May 2008
Negative Feedback Control of Jasmonate Signaling by an Alternative Splice Variant of JAZ10 journal April 2013
Analysis of Arabidopsis JAZ gene expression during Pseudomonas syringae pathogenesis: JAZ gene expression during P. syringae infection journal June 2011
Redundancy and specificity in jasmonate signalling journal October 2016
TOPLESS Regulates Apical Embryonic Fate in Arabidopsis journal June 2006
Alternative splicing expands the repertoire of dominant JAZ repressors of jasmonate signaling: Alternative splicing of Arabidopsis JAZ genes journal August 2010
The CCP4 suite programs for protein crystallography journal September 1994
Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis journal May 2015
Change of a conserved amino acid in the MYC2 and MYC3 transcription factors leads to release of JAZ repression and increased activity journal March 2015
XDS journal January 2010
Jasmonate-Triggered Plant Immunity journal June 2014
Negative regulation of defence and stress genes by EAR-motif-containing repressors journal March 2006
Transcription factor-dependent nuclear localization of a transcriptional repressor in jasmonate hormone signaling journal November 2012
A Critical Role for the TIFY Motif in Repression of Jasmonate Signaling by a Stabilized Splice Variant of the JASMONATE ZIM-Domain Protein JAZ10 in Arabidopsis journal January 2009
(+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate journal April 2009
NINJA connects the co-repressor TOPLESS to jasmonate signalling journal April 2010
Phaser crystallographic software journal July 2007
Jasmonate Passes Muster: A Receptor and Targets for the Defense Hormone journal June 2009
JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling journal July 2007
Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth journal June 2015

Similar Records

Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling
Journal Article · Mon Aug 10 00:00:00 EDT 2015 · Nature (London) · OSTI ID:1341769

Jasmonate Hormone: Regulating Synthesis of Reduced Carbon Compounds in Plants
Technical Report · Fri May 13 00:00:00 EDT 2016 · OSTI ID:1341769

Repression of jasmonate signaling by a non‐TIFY JAZ protein in Arabidopsis
Journal Article · Sat May 09 00:00:00 EDT 2015 · The Plant Journal · OSTI ID:1341769