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Title: JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America

Plant immune responses mediated by the hormone jasmonoyl-L-isoleucine (JA-Ile) are metabolically costly and often linked to reduced growth. Although it is known that JA-Ile activates defense responses by triggering the degradation of JASMONATE ZIM DOMAIN (JAZ) transcriptional repressor proteins, expansion of the JAZ gene family in vascular plants has hampered efforts to understand how this hormone impacts growth and other physiological tasks over the course of ontogeny. Here, we combined mutations within the 13-member Arabidopsis JAZ gene family to investigate the effects of chronic JAZ deficiency on growth, defense, and reproductive output. A higher-order mutant (jaz decuple, jazD) defective in 10 JAZ genes (JAZ1–7, -9, -10, and -13) exhibited robust resistance to insect herbivores and fungal pathogens, which was accompanied by slow vegetative growth and poor reproductive performance. Metabolic phenotypes of jazD discerned from global transcript and protein profiling were indicative of elevated carbon partitioning to amino acid-, protein-, and endoplasmic reticulum body-based defenses controlled by the JA-Ile and ethylene branches of immunity. Resource allocation to a strong defense sink in jazD leaves was associated with increased respiration and hallmarks of carbon starvation but no overt changes in photosynthetic rate. Depletion of the remaining JAZ repressors in jazD further exaggerated growth stunting, nearly abolished seed production and, under extreme conditions, caused spreading necrotic lesions and tissue death. Our results demonstrate that JAZ proteins promote growth and reproductive success at least in part by preventing catastrophic metabolic effects of an unrestrained immune response.

Research Organization:
Michigan State Univ., East Lansing, MI (United States). DOE Plant Research laboratory
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
FG02-91ER20021
OSTI ID:
1478446
Alternate ID(s):
OSTI ID: 1603655
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. 115 Journal Issue: 45; ISSN 0027-8424
Publisher:
National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 143 works
Citation information provided by
Web of Science

References (75)

MATE Transporter-Dependent Export of Hydroxycinnamic Acid Amides journal January 2016
Arabidopsis Coordinates the Diurnal Regulation of Carbon Allocation and Growth across a Wide Range of Photoperiods journal January 2014
Trade-Offs Between Plant Growth and Defense Against Insect Herbivory: An Emerging Mechanistic Synthesis journal April 2017
Accumulation of hydroxycinnamic acid amides induced by pathogen infection and identification of agmatine coumaroyltransferase in Arabidopsis thaliana journal June 2009
Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses against Botrytis cinerea Infection journal September 2017
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
Ethylene-Regulated Glutamate Dehydrogenase Fine-Tunes Metabolism during Anoxia-Reoxygenation journal September 2016
Modularity in Jasmonate Signaling for Multistress Resilience journal April 2018
Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods journal July 2009
Arabidopsis Basic Helix-Loop-Helix Transcription Factors MYC2, MYC3, and MYC4 Regulate Glucosinolate Biosynthesis, Insect Performance, and Feeding Behavior journal August 2013
Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling journal August 2015
Regulation of Jasmonate-Induced Leaf Senescence by Antagonism between bHLH Subgroup IIIe and IIId Factors in Arabidopsis journal June 2015
Wound-Induced Endogenous Jasmonates Stunt Plant Growth by Inhibiting Mitosis journal November 2008
Plant Immunity to Insect Herbivores journal June 2008
Salt and methyl jasmonate aggravate growth inhibition and senescence in Arabidopsis seedlings via the JA signaling pathway journal August 2017
Male sterility in Arabidopsis induced by overexpression of a MYC5-SRDX chimeric repressor journal February 2015
Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis journal July 2011
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
Control of Carbon Assimilation and Partitioning by Jasmonate: An Accounting of Growth–Defense Tradeoffs journal January 2016
Two Abscisic Acid-Responsive Plastid Lipase Genes Involved in Jasmonic Acid Biosynthesis in Arabidopsis thaliana journal April 2018
Induced Responses to Herbivory and Increased Plant Performance journal February 1998
Regulation of Jasmonate-Mediated Stamen Development and Seed Production by a bHLH-MYB Complex in Arabidopsis journal May 2015
PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants journal October 2016
Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module journal June 2017
New Insights into Plant Responses to the Attack from Insect Herbivores journal December 2010
Biosynthesis and Defensive Function of N δ -Acetylornithine, a Jasmonate-Induced Arabidopsis Metabolite journal September 2011
Coordination of carbon supply and plant growth journal September 2007
Sulfur-Enhanced Defence: Effects of Sulfur Metabolism, Nitrogen Supply, and Pathogen Lifestyle journal September 2007
Isolation and Identification of a Senescence-promoting Substance from Wormwood ( Artemisia absinthium L.) journal August 1980
DELLAs Modulate Jasmonate Signaling via Competitive Binding to JAZs journal December 2010
Resolution of growth–defense conflict: mechanistic insights from jasmonate signaling journal August 2018
Unique Defense Strategy by the Endoplasmic Reticulum Body in Plants journal November 2011
Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid journal May 2017
Jasmonate Passes Muster: A Receptor and Targets for the Defense Hormone journal June 2009
Detritivorous crustaceans become herbivores on jasmonate-deficient plants journal January 2009
JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling journal July 2007
Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi journal January 2002
Interaction between MYC2 and ETHYLENE INSENSITIVE3 Modulates Antagonism between Jasmonate and Ethylene Signaling in Arabidopsis journal January 2014
JAZ8 Lacks a Canonical Degron and Has an EAR Motif That Mediates Transcriptional Repression of Jasmonate Responses in Arabidopsis journal February 2012
Primary Metabolism and Plant Defense—Fuel for the Fire journal May 2009
NAD(H)-dependent glutamate dehydrogenase is essential for the survival of Arabidopsis thaliana during dark-induced carbon starvation journal February 2008
Arabidopsis Phosphoglycerate Dehydrogenase1 of the Phosphoserine Pathway Is Essential for Development and Required for Ammonium Assimilation and Tryptophan Biosynthesis journal December 2013
Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs journal August 2016
Dark-inducible genes from Arabidopsisthaliana are associated with leaf senescence and repressed by sugars journal March 2001
JASMONATE-INSENSITIVE1 Encodes a MYC Transcription Factor Essential to Discriminate between Different Jasmonate-Regulated Defense Responses in Arabidopsis journal June 2004
Jasmonic acid/ethylene signaling coordinates hydroxycinnamic acid amides biosynthesis through ORA59 transcription factor journal June 2018
Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1 journal December 1998
Mechanisms to Mitigate the Trade-Off between Growth and Defense journal March 2017
Herbivory-induced jasmonates constrain plant sugar accumulation and growth by antagonizing gibberellin signaling and not by promoting secondary metabolite production journal May 2017
JAZ2 controls stomata dynamics during bacterial invasion journal December 2016
Hydrogen Peroxide Acts as a Second Messenger for the Induction of Defense Genes in Tomato Plants in Response to Wounding, Systemin, and Methyl Jasmonate journal January 2001
Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana journal December 2009
Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species journal April 2007
The Role of Arabidopsis Rubisco Activase in Jasmonate-Induced Leaf Senescence journal December 2010
A Downstream Mediator in the Growth Repression Limb of the Jasmonate Pathway journal August 2007
Ethylene Response Factors: A Key Regulatory Hub in Hormone and Stress Signaling journal June 2015
A central integrator of transcription networks in plant stress and energy signalling journal August 2007
MEDIATOR25 Acts as an Integrative Hub for the Regulation of Jasmonate-Responsive Gene Expression in Arabidopsis journal July 2012
MYC2: The Master in Action journal May 2013
Redundancy and specificity in jasmonate signalling journal October 2016
The AP2/ERF Domain Transcription Factor ORA59 Integrates Jasmonic Acid and Ethylene Signals in Plant Defense journal May 2008
Temporal Dynamics of Growth and Photosynthesis Suppression in Response to Jasmonate Signaling journal May 2014
NaJAZh Regulates a Subset of Defense Responses against Herbivores and Spontaneous Leaf Necrosis in Nicotiana attenuata Plants journal April 2012
Leaf-herbivore attack reduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling journal August 2013
Jasmonate-induced responses are costly but benefit plants under attack in native populations journal July 1998
Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis journal May 2015
PYK10 myrosinase reveals a functional coordination between endoplasmic reticulum bodies and glucosinolates in Arabidopsis thaliana journal December 2016
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
Jasmonate-Triggered Plant Immunity journal June 2014
The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana: HIG1 and glucosinolate biosynthesis journal April 2007
Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis: Metabolism regulated by jasmonates in Arabidopsis journal October 2005
NINJA connects the co-repressor TOPLESS to jasmonate signalling journal April 2010
Plant hormones are versatile chemical regulators of plant growth journal April 2009
Networking by small-molecule hormones in plant immunity journal April 2009