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Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.14638· OSTI ID:1425392
 [1];  [2];  [2];  [2];  [2];  [2];  [2];  [3];  [4]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Department of Energy-Plant Research Laboratory, Michigan State University, East Lansing, MI 48824
  2. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
  3. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory and Plant Resilience Institute; Howard Hughes Medical Inst., East Lansing, MI (United States)
  4. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory and Plant Resilience Institute
The plant hormone jasmonate (JA) promotes the degradation of JASMONATE ZIM-DOMAIN (JAZ) proteins to relieve repression on diverse transcription factors (TFs) that execute JA responses. However, little is known about how combinatorial complexity among JAZ–TF interactions maintains control over myriad aspects of growth, development, reproduction, and immunity. We used loss-of-function mutations to define epistatic interactions within the core JA signaling pathway and to investigate the contribution of MYC TFs to JA responses in Arabidopsis thaliana. Constitutive JA signaling in a jaz quintuple mutant (jazQ) was largely eliminated by mutations that block JA synthesis or perception. Comparison of jazQ and a jazQ myc2 myc3 myc4 octuple mutant validated known functions of MYC2/3/4 in root growth, chlorophyll degradation,and susceptibility to the pathogen Pseudomonas syringae. We found that MYC TFs also control both the enhanced resistance of jazQ leaves to insect herbivory and restricted leaf growth of jazQ. Epistatic transcriptional profiles mirrored these phenotypes and further showed that triterpenoid biosynthetic and glucosinolate catabolic genes are up-regulated in jazQ independently of MYC TFs. Lastly, our study highlights the utility of genetic epistasis to unravel the complexities of JAZ–TF interactions and demonstrates that MYC TFs exert master control over a JAZ-repressible transcriptional hierarchy that governs growth–defense balance.
Research Organization:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Organization:
Brazilian National Council for Scientific and Technological Development; Japan Society for Promotion of Science Research; National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
FG02-91ER20021
OSTI ID:
1425392
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 4 Vol. 215; ISSN 0028-646X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (112)

Characterizing Jasmonate Regulation of Male Fertility in Arabidopsis book January 2013
Elicitation of Jasmonate-Mediated Defense Responses by Mechanical Wounding and Insect Herbivory book January 2013
The role of JAR1 in Jasmonoyl-l-isoleucine production during Arabidopsis wound response journal February 2008
Jasmonate-Triggered Plant Immunity journal June 2014
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy journal August 1989
Plant Stomata Function in Innate Immunity against Bacterial Invasion journal September 2006
Coronatine Promotes Pseudomonas syringae Virulence in Plants by Activating a Signaling Cascade that Inhibits Salicylic Acid Accumulation journal June 2012
Evolutionary and Environmental Forces Sculpting Leaf Development journal April 2016
DELLAs Modulate Jasmonate Signaling via Competitive Binding to JAZs journal December 2010
Leaf growth in dicots and monocots: so different yet so alike journal October 2016
Redundancy and specificity in jasmonate signalling journal October 2016
The wound hormone jasmonate journal September 2009
False idolatry of the mythical growth versus immunity tradeoff in molecular systems plant pathology journal July 2016
The tify family previously known as ZIM journal June 2007
JAZ repressors and the orchestration of phytohormone crosstalk journal January 2012
Transcriptional machineries in jasmonate-elicited plant secondary metabolism journal June 2012
Origin and evolutionary analysis of the plant-specific TIFY transcription factor family journal August 2011
JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling journal July 2007
The JAZ family of repressors is the missing link in jasmonate signalling journal July 2007
NINJA connects the co-repressor TOPLESS to jasmonate signalling journal April 2010
Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor journal October 2010
Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling journal August 2015
(+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate journal April 2009
Networking by small-molecule hormones in plant immunity journal April 2009
Plant hormones are versatile chemical regulators of plant growth journal April 2009
GAME9 regulates the biosynthesis of steroidal alkaloids and upstream isoprenoids in the plant mevalonate pathway journal February 2016
Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs journal August 2016
Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance journal January 2017
Differential expression analysis for sequence count data journal April 2010
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources journal December 2008
Transcriptomic analysis of female and male gonads in juvenile snakeskin gourami (Trichopodus pectoralis) journal March 2020
A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis journal July 2002
Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway journal November 2003
Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells journal January 2008
COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine journal May 2008
Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade journal April 2012
Role of NINJA in root jasmonate signaling journal September 2013
Structural insights into alternative splicing-mediated desensitization of jasmonate signaling journal January 2017
Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. journal March 1992
Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany journal April 2013
Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis journal July 2009
Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis journal February 2011
Growth–Defense Tradeoffs in Plants: A Balancing Act to Optimize Fitness journal August 2014
Delineation of metabolic gene clusters in plant genomes by chromatin signatures journal February 2016
Up-regulation of Soyasaponin Biosynthesis by Methyl Jasmonate in Cultured Cells of Glycyrrhiza glabra journal April 2003
The Arabidopsis thaliana JASMONATE INSENSITIVE 1 Gene Is Required for Suppression of Salicylic Acid-Dependent Defenses During Infection by Pseudomonas syringae journal July 2006
Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis journal July 2004
The Role of Arabidopsis Rubisco Activase in Jasmonate-Induced Leaf Senescence journal December 2010
Jasmonate Controls Polypeptide Patterning in Undamaged Tissue in Wounded Arabidopsis Leaves journal June 2011
MEDIATOR25 Acts as an Integrative Hub for the Regulation of Jasmonate-Responsive Gene Expression in Arabidopsis journal July 2012
Jasmonate Controls Leaf Growth by Repressing Cell Proliferation and the Onset of Endoreduplication while Maintaining a Potential Stand-By Mode journal February 2013
Negative Feedback Control of Jasmonate Signaling by an Alternative Splice Variant of JAZ10 journal April 2013
Temporal Dynamics of Growth and Photosynthesis Suppression in Response to Jasmonate Signaling journal May 2014
Promoter-Based Integration in Plant Defense Regulation journal October 2014
The COP9 Signalosome Interacts Physically with SCF COI1 and Modulates Jasmonate Responses journal April 2003
JASMONATE-INSENSITIVE1 Encodes a MYC Transcription Factor Essential to Discriminate between Different Jasmonate-Regulated Defense Responses in Arabidopsis journal June 2004
The Oxylipin Signal Jasmonic Acid Is Activated by an Enzyme That Conjugates It to Isoleucine in Arabidopsis journal July 2004
A Basic Helix-Loop-Helix Transcription Factor in Arabidopsis, MYC2, Acts as a Repressor of Blue Light–Mediated Photomorphogenic Growth journal May 2005
MYC2 Differentially Modulates Diverse Jasmonate-Dependent Functions in Arabidopsis journal July 2007
A Downstream Mediator in the Growth Repression Limb of the Jasmonate Pathway journal August 2007
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
The Arabidopsis CORONATINE INSENSITIVE1 Protein Is a Jasmonate Receptor journal August 2009
Jasmonate and Phytochrome A Signaling in Arabidopsis Wound and Shade Responses Are Integrated through JAZ1 Stability journal April 2010
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
The Jasmonate-ZIM-Domain Proteins Interact with the WD-Repeat/bHLH/MYB Complexes to Regulate Jasmonate-Mediated Anthocyanin Accumulation and Trichome Initiation in Arabidopsis thaliana journal May 2011
The JAZ Proteins: A Crucial Interface in the Jasmonate Signaling Cascade journal September 2011
The Basic Helix-Loop-Helix Transcription Factor MYC2 Directly Represses PLETHORA Expression during Jasmonate-Mediated Modulation of the Root Stem Cell Niche in Arabidopsis journal September 2011
JAZ8 Lacks a Canonical Degron and Has an EAR Motif That Mediates Transcriptional Repression of Jasmonate Responses in Arabidopsis journal February 2012
The Arabidopsis Mediator Subunit MED25 Differentially Regulates Jasmonate and Abscisic Acid Signaling through Interacting with the MYC2 and ABI5 Transcription Factors journal July 2012
Arabidopsis MYC2 Interacts with DELLA Proteins in Regulating Sesquiterpene Synthase Gene Expression journal June 2012
A bHLH-Type Transcription Factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, Acts as a Repressor to Negatively Regulate Jasmonate Signaling in Arabidopsis journal May 2013
Predicting Gene Function from Uncontrolled Expression Variation among Individual Wild-Type Arabidopsis Plants journal August 2013
Arabidopsis Basic Helix-Loop-Helix Transcription Factors MYC2, MYC3, and MYC4 Regulate Glucosinolate Biosynthesis, Insect Performance, and Feeding Behavior journal August 2013
Repression of Jasmonate-Dependent Defenses by Shade Involves Differential Regulation of Protein Stability of MYC Transcription Factors and Their JAZ Repressors in Arabidopsis journal May 2014
Regulation of Jasmonate-Induced Leaf Senescence by Antagonism between bHLH Subgroup IIIe and IIId Factors in Arabidopsis journal June 2015
Regulation of Jasmonate-Mediated Stamen Development and Seed Production by a bHLH-MYB Complex in Arabidopsis journal May 2015
FILAMENTOUS FLOWER Is a Direct Target of JAZ3 and Modulates Responses to Jasmonate journal November 2015
Mechanisms to Mitigate the Trade-Off between Growth and Defense journal March 2017
Analysis of Arabidopsis JAZ gene expression during Pseudomonas syringae pathogenesis: JAZ gene expression during P. syringae infection journal June 2011
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
A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis journal September 2009
Alternative splicing expands the repertoire of dominant JAZ repressors of jasmonate signaling: Alternative splicing of Arabidopsis JAZ genes journal August 2010
A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana journal June 2010
Cultivated and wild host plants supporting populations of the cabbage root fly journal January 1977
To grow or defend? Low red : far-red ratios reduce jasmonate sensitivity in Arabidopsis seedlings by promoting DELLA degradation and increasing JAZ10 stability journal August 2014
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
Plant metabolic clusters – from genetics to genomics journal April 2016
JAZ2 controls stomata dynamics during bacterial invasion journal December 2016
Male sterility in Arabidopsis induced by overexpression of a MYC5-SRDX chimeric repressor journal February 2015
Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis journal May 2015
Jasmonic acid promotes degreening via MYC2/3/4- and ANAC019/055/072-mediated regulation of major chlorophyll catabolic genes journal October 2015
Metabolic Diversification--Independent Assembly of Operon-Like Gene Clusters in Different Plants journal April 2008
Biosynthesis, regulation, and domestication of bitterness in cucumber journal November 2014
COI1: An Arabidopsis Gene Required for Jasmonate-Regulated Defense and Fertility journal May 1998
Trade-Offs Between Plant Growth and Defense Against Insect Herbivory: An Emerging Mechanistic Synthesis journal April 2017
New Insights into Plant Responses to the Attack from Insect Herbivores journal December 2010
Jasmonate Passes Muster: A Receptor and Targets for the Defense Hormone journal June 2009
Biology and Biochemistry of Glucosinolates journal June 2006
Plant Immunity to Insect Herbivores journal June 2008
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome journal August 2011
Differential expression analysis for sequence count data journal October 2010
The Arabidopsis Thaliana-Pseudomonas Syringae Interaction journal January 2002
Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis journal February 2009
Jasmonate regulates juvenile-to-adult phase transition in rice journal August 2016
The bHLH Subgroup IIId Factors Negatively Regulate Jasmonate-Mediated Plant Defense and Development journal July 2013
Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth journal June 2015
Wound-Induced Endogenous Jasmonates Stunt Plant Growth by Inhibiting Mitosis journal November 2008
The Non-JAZ TIFY Protein TIFY8 from Arabidopsis thaliana Is a Transcriptional Repressor journal January 2014
Social Network: JAZ Protein Interactions Expand Our Knowledge of Jasmonate Signaling journal January 2012
Control of Carbon Assimilation and Partitioning by Jasmonate: An Accounting of Growth–Defense Tradeoffs journal January 2016
A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana text January 2010
Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis text January 2017

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Comparison of gene co-networks reveals the molecular mechanisms of the rice (Oryza sativa L.) response to Rhizoctonia solani AG1 IA infection journal May 2018
Construction and characterization of a high-quality cDNA library of Cymbidium faberi suitable for yeast one- and two-hybrid assays journal January 2020
APETALA2 control of barley internode elongation journal May 2019
The Crosstalks Between Jasmonic Acid and Other Plant Hormone Signaling Highlight the Involvement of Jasmonic Acid as a Core Component in Plant Response to Biotic and Abiotic Stresses journal October 2019
Stimulation of Insect Herbivory by Elevated Temperature Outweighs Protection by the Jasmonate Pathway journal February 2020
Dynamic gene expression changes in response to micronutrient, macronutrient, and multiple stress exposures in soybean journal October 2019
Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis journal November 2017
JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis journal October 2018
An effector from cotton bollworm oral secretion impairs host plant defense signaling journal June 2019
A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels journal October 2019
Phytohormones regulate convergent and divergent responses between individual and combined drought and pathogen infection journal January 2020
SmJAZ8 acts as a core repressor regulating JA-induced biosynthesis of salvianolic acids and tanshinones in Salvia miltiorrhiza hairy roots journal December 2017
Jasmonate action in plant defense against insects journal April 2019
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Mechanisms of a locally adaptive shift in allocation among growth, reproduction, and herbivore resistance in Mimulus guttatus posted_content January 2019
Mechanisms of a locally adaptive shift in allocation among growth, reproduction, and herbivore resistance in Mimulus guttatus * journal March 2019
Potential of zeolite to control Sclerotinia sclerotiorum and Rhizoctonia solani in lettuce and the induction of defence‐related genes journal November 2019
A plant's balance of growth and defense - revisited journal August 2017
Plant-arthropod interactions: who is the winner? journal December 2017
The JA‐pathway MYC transcription factors regulate photomorphogenic responses by targeting HY5 gene expression journal January 2020
Transcriptome Sequencing Analysis Provides Insights Into the Response to Fusarium oxysporum in Lilium pumilum journal January 2019
Full-length transcriptome sequencing and methyl jasmonate-induced expression profile analysis of genes related to patchoulol biosynthesis and regulation in Pogostemon cablin journal June 2019
Arabidopsis MYB24 Regulates Jasmonate-Mediated Stamen Development journal September 2017
Crosstalk with Jasmonic Acid Integrates Multiple Responses in Plant Development journal January 2020

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