Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling

Zhou, X. Edward; Zhang, Yaguang; Yao, Jian; Zheng, Jie; Zhou, Yuxin; He, Qing; Moreno, Javier; Lam, Vinh Q.; Cao, Xiaoman; Sugimoto, Koichi; Vanegas-Cano, Leidy; Kariapper, Leena; Suino-Powell, Kelly; Zhu, Yuanye; Novick, Scott; Griffin, Patrick R.; Zhang, Feng; Howe, Gregg A.; Melcher, Karsten

doi:10.1016/j.xplc.2023.100639

Title: Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling

Abstract

Jasmonates (JAs) are plant hormones with crucial roles in development and stress resilience. They activate MYC transcription factors by mediating the proteolysis of MYC inhibitors called JAZ proteins. In the absence of JA, JAZ proteins bind and inhibit MYC through the assembly of MYC–JAZ–Novel Interactor of JAZ (NINJA)–TPL repressor complexes. However, JAZ and NINJA are predicted to be largely intrinsically unstructured, which has precluded their experimental structure determination. Through a combination of biochemical, mutational, and biophysical analyses and AlphaFold-derived ColabFold modeling, we characterized JAZ–JAZ and JAZ–NINJA interactions and generated models with detailed, high-confidence domain interfaces. We demonstrate that JAZ, NINJA, and MYC interface domains are dynamic in isolation and become stabilized in a stepwise order upon complex assembly. By contrast, most JAZ and NINJA regions outside of the interfaces remain highly dynamic and cannot be modeled in a single conformation. Our data indicate that the small JAZ Zinc finger expressed in Inflorescence Meristem (ZIM) motif mediates JAZ–JAZ and JAZ–NINJA interactions through separate surfaces, and our data further suggest that NINJA modulates JAZ dimerization. This study advances our understanding of JA signaling by providing insights into the dynamics, interactions, and structure of the JAZ–NINJA core of the JA repressor complex.

Authors:

Zhou, X. Edward ^[1]; Zhang, Yaguang ^[2]; Yao, Jian ^[3]; Zheng, Jie ^[4]; Zhou, Yuxin ^[5]; He, Qing ^[1]; Moreno, Javier ^[3]; Lam, Vinh Q. ^[4]; Cao, Xiaoman ^[2]; Sugimoto, Koichi ^[6]; Vanegas-Cano, Leidy ^[3]; Kariapper, Leena ^[1]; Suino-Powell, Kelly ^[1]; Zhu, Yuanye ^[7]; Novick, Scott ^[4]; Griffin, Patrick R. ^[4]; Zhang, Feng ^[7]; Howe, Gregg A. ^[3];

^[1]

Van Andel Institute, Grand Rapids, MI (United States)
Nanjing Agricultural University (China)
Michigan State University, East Lansing, MI (United States)
UF Scripps Biomedical Research, Jupiter, FL (United States)
Van Andel Institute, Grand Rapids, MI (United States); Nanjing Agricultural University (China); Jiangsu Province and Chinese Academy of Sciences, Nanjing (China)
Michigan State University, East Lansing, MI (United States); University of Tsukuba (Japan)
Van Andel Institute, Grand Rapids, MI (United States); Nanjing Agricultural University (China)

Publication Date:: Wed Jun 14 00:00:00 EDT 2023

Research Org.:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

OSTI Identifier:: 2229523

Grant/Contract Number:: FG02-91ER20021

Resource Type:: Accepted Manuscript

Journal Name:: Plant Communications

Additional Journal Information:: Journal Volume: 4; Journal Issue: 6; Journal ID: ISSN 2590-3462

Publisher:: Cell Press

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; JAZ protein; NINJA; AlphaFold; ColabFold; MYC; hydrogen-deuterium exchange

Citation Formats


                    Zhou, X. Edward, Zhang, Yaguang, Yao, Jian, Zheng, Jie, Zhou, Yuxin, He, Qing, Moreno, Javier, Lam, Vinh Q., Cao, Xiaoman, Sugimoto, Koichi, Vanegas-Cano, Leidy, Kariapper, Leena, Suino-Powell, Kelly, Zhu, Yuanye, Novick, Scott, Griffin, Patrick R., Zhang, Feng, Howe, Gregg A., and Melcher, Karsten. Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling.  United States: N. p., 2023. 
Web.  doi:10.1016/j.xplc.2023.100639.

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                    Zhou, X. Edward, Zhang, Yaguang, Yao, Jian, Zheng, Jie, Zhou, Yuxin, He, Qing, Moreno, Javier, Lam, Vinh Q., Cao, Xiaoman, Sugimoto, Koichi, Vanegas-Cano, Leidy, Kariapper, Leena, Suino-Powell, Kelly, Zhu, Yuanye, Novick, Scott, Griffin, Patrick R., Zhang, Feng, Howe, Gregg A., & Melcher, Karsten. Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling.  United States.  https://doi.org/10.1016/j.xplc.2023.100639

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                    Zhou, X. Edward, Zhang, Yaguang, Yao, Jian, Zheng, Jie, Zhou, Yuxin, He, Qing, Moreno, Javier, Lam, Vinh Q., Cao, Xiaoman, Sugimoto, Koichi, Vanegas-Cano, Leidy, Kariapper, Leena, Suino-Powell, Kelly, Zhu, Yuanye, Novick, Scott, Griffin, Patrick R., Zhang, Feng, Howe, Gregg A., and Melcher, Karsten. Wed .  
"Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling".  United States.  https://doi.org/10.1016/j.xplc.2023.100639.  https://www.osti.gov/servlets/purl/2229523.

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@article{osti_2229523,

  title        = {Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling},

  author       = {Zhou, X. Edward and Zhang, Yaguang and Yao, Jian and Zheng, Jie and Zhou, Yuxin and He, Qing and Moreno, Javier and Lam, Vinh Q. and Cao, Xiaoman and Sugimoto, Koichi and Vanegas-Cano, Leidy and Kariapper, Leena and Suino-Powell, Kelly and Zhu, Yuanye and Novick, Scott and Griffin, Patrick R. and Zhang, Feng and Howe, Gregg A. and Melcher, Karsten},

  abstractNote = {Jasmonates (JAs) are plant hormones with crucial roles in development and stress resilience. They activate MYC transcription factors by mediating the proteolysis of MYC inhibitors called JAZ proteins. In the absence of JA, JAZ proteins bind and inhibit MYC through the assembly of MYC–JAZ–Novel Interactor of JAZ (NINJA)–TPL repressor complexes. However, JAZ and NINJA are predicted to be largely intrinsically unstructured, which has precluded their experimental structure determination. Through a combination of biochemical, mutational, and biophysical analyses and AlphaFold-derived ColabFold modeling, we characterized JAZ–JAZ and JAZ–NINJA interactions and generated models with detailed, high-confidence domain interfaces. We demonstrate that JAZ, NINJA, and MYC interface domains are dynamic in isolation and become stabilized in a stepwise order upon complex assembly. By contrast, most JAZ and NINJA regions outside of the interfaces remain highly dynamic and cannot be modeled in a single conformation. Our data indicate that the small JAZ Zinc finger expressed in Inflorescence Meristem (ZIM) motif mediates JAZ–JAZ and JAZ–NINJA interactions through separate surfaces, and our data further suggest that NINJA modulates JAZ dimerization. This study advances our understanding of JA signaling by providing insights into the dynamics, interactions, and structure of the JAZ–NINJA core of the JA repressor complex.},

  doi          = {10.1016/j.xplc.2023.100639},

  journal      = {Plant Communications},

  number       = 6,

  volume       = 4,

  place        = {United States},

  year         = {Wed Jun 14 00:00:00 EDT 2023},

  month        = {Wed Jun 14 00:00:00 EDT 2023}

}

Copy to clipboard

Journal Article:

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Title: Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling

Abstract

Citation Formats

The tify family previously known as ZIM journal, June 2007

The Oxylipin Pathways: Biochemistry and Function journal, April 2018

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

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Resolution of growth–defense conflict: mechanistic insights from jasmonate signaling journal, August 2018

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

JAZ8 Lacks a Canonical Degron and Has an EAR Motif That Mediates Transcriptional Repression of Jasmonate Responses in Arabidopsis journal, February 2012

What's next for AlphaFold and the AI protein-folding revolution journal, April 2022

Assessing PDB macromolecular crystal structure confidence at the individual amino acid residue level journal, October 2022

Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors journal, July 2015

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

Mediator subunit MED25 links the jasmonate receptor to transcriptionally active chromatin journal, October 2017

Arabidopsis ECAP Is a New Adaptor Protein that Connects JAZ Repressors with the TPR2 Co-repressor to Suppress Jasmonate-Responsive Anthocyanin Accumulation journal, February 2020

Role of NINJA in root jasmonate signaling journal, September 2013

ColabFold: making protein folding accessible to all journal, May 2022

A Downstream Mediator in the Growth Repression Limb of the Jasmonate Pathway journal, August 2007

MEDIATOR25 Acts as an Integrative Hub for the Regulation of Jasmonate-Responsive Gene Expression in Arabidopsis journal, July 2012

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana journal, December 1998

Critical assessment of protein intrinsic disorder prediction journal, April 2021

Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis journal, May 2015

cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination journal, February 2017

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

Probing Protein Ligand Interactions by Automated Hydrogen/Deuterium Exchange Mass Spectrometry journal, February 2006

Protein secondary structure prediction based on position-specific scoring matrices 1 1Edited by G. Von Heijne journal, September 1999

The tify family previously known as ZIM
journal, June 2007

The Oxylipin Pathways: Biochemistry and Function
journal, April 2018

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

Modularity in Jasmonate Signaling for Multistress Resilience
journal, April 2018

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

I-TASSER: a unified platform for automated protein structure and function prediction
journal, March 2010

Structural insights into alternative splicing-mediated desensitization of jasmonate signaling
journal, January 2017

Accurate prediction of protein structures and interactions using a three-track neural network
journal, July 2021

Intrinsically unstructured proteins and their functions
journal, March 2005

Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor
journal, October 2010

Integrated multi-omics framework of the plant response to jasmonic acid
journal, March 2020

The accuracy of protein structures in solution determined by AlphaFold and NMR
journal, July 2022

JASMONATE-ZIM DOMAIN proteins engage Polycomb chromatin modifiers to modulate Jasmonate signaling in Arabidopsis
journal, May 2021

Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix
journal, October 2019

Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis
journal, July 2011

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

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

Highly accurate protein structure prediction with AlphaFold
journal, July 2021

DISOPRED3: precise disordered region predictions with annotated protein-binding activity
journal, November 2014

Regulation of jasmonate signaling by reversible acetylation of TOPLESS in Arabidopsis
journal, August 2022

TOPLESS Regulates Apical Embryonic Fate in Arabidopsis
journal, June 2006

The I-TASSER Suite: protein structure and function prediction
journal, December 2014

AlphaFold and Implications for Intrinsically Disordered Proteins
journal, October 2021

I-TASSER server for protein 3D structure prediction
journal, January 2008

UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004

Resolution of growth–defense conflict: mechanistic insights from jasmonate signaling
journal, August 2018

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

JAZ8 Lacks a Canonical Degron and Has an EAR Motif That Mediates Transcriptional Repression of Jasmonate Responses in Arabidopsis
journal, February 2012

What's next for AlphaFold and the AI protein-folding revolution
journal, April 2022

Assessing PDB macromolecular crystal structure confidence at the individual amino acid residue level
journal, October 2022

Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors
journal, July 2015

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

Mediator subunit MED25 links the jasmonate receptor to transcriptionally active chromatin
journal, October 2017

Arabidopsis ECAP Is a New Adaptor Protein that Connects JAZ Repressors with the TPR2 Co-repressor to Suppress Jasmonate-Responsive Anthocyanin Accumulation
journal, February 2020

Role of NINJA in root jasmonate signaling
journal, September 2013

ColabFold: making protein folding accessible to all
journal, May 2022

A Downstream Mediator in the Growth Repression Limb of the Jasmonate Pathway
journal, August 2007

MEDIATOR25 Acts as an Integrative Hub for the Regulation of Jasmonate-Responsive Gene Expression in Arabidopsis
journal, July 2012

Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998

Critical assessment of protein intrinsic disorder prediction
journal, April 2021

Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis
journal, May 2015

cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination
journal, February 2017

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

Probing Protein Ligand Interactions by Automated Hydrogen/Deuterium Exchange Mass Spectrometry
journal, February 2006

Protein secondary structure prediction based on position-specific scoring matrices 1 1Edited by G. Von Heijne
journal, September 1999