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

Major, Ian T.; Yoshida, Yuki; Campos, Marcelo L.; Kapali, George; Xin, Xiu-Fang; Sugimoto, Koichi; de Oliveira Ferreira, Dalton; He, Sheng Yang; Howe, Gregg A.

doi:10.1111/nph.14638

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

Journal Article · Mon Jun 26 00:00:00 EDT 2017 · New Phytologist

DOI:https://doi.org/10.1111/nph.14638· OSTI ID:1425392

Major, Ian T. ^[1]; Yoshida, Yuki ^[1]; Campos, Marcelo L. ^[1]; Kapali, George ^[1]; Xin, Xiu-Fang ^[1]; Sugimoto, Koichi ^[1]; de Oliveira Ferreira, Dalton ^[1]; He, Sheng Yang ^[2]; Howe, Gregg A. ^[3]

Michigan State Univ., East Lansing, MI (United States). Dept. of Energy-Plant Research Lab.
Michigan State Univ., East Lansing, MI (United States). Dept. of Energy-Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology; Michigan State Univ., East Lansing, MI (United States). Howard Hughes Medical Inst.; Michigan State Univ., East Lansing, MI (United States). Plant Resilience Inst.
Michigan State Univ., East Lansing, MI (United States). Dept. of Energy-Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Plant Resilience Inst.; Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology

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.

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Research Organization:: Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); Japan Society for Promotion of Science Research; Brazilian National Council for Scientific and Technological Development

Grant/Contract Number:: FG02-91ER20021

OSTI ID:: 1425392

Journal Information:: New Phytologist, Vol. 215, Issue 4; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 160 works

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The Non-JAZ TIFY Protein TIFY8 from Arabidopsis thaliana Is a Transcriptional Repressor Cuéllar Pérez, Amparo; Nagels Durand, Astrid; Vanden Bossche, Robin PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0084891	journal	January 2014
Temporal Dynamics of Growth and Photosynthesis Suppression in Response to Jasmonate Signaling Attaran, Elham; Major, Ian T.; Cruz, Jeffrey A. Plant Physiology, Vol. 165, Issue 3 https://doi.org/10.1104/pp.114.239004	journal	May 2014
A Basic Helix-Loop-Helix Transcription Factor in Arabidopsis, MYC2, Acts as a Repressor of Blue Light–Mediated Photomorphogenic Growth Yadav, Vandana; Mallappa, Chandrashekara; Gangappa, Sreeramaiah N. The Plant Cell, Vol. 17, Issue 7 https://doi.org/10.1105/tpc.105.032060	journal	May 2005
Plant Stomata Function in Innate Immunity against Bacterial Invasion Melotto, Maeli; Underwood, William; Koczan, Jessica Cell, Vol. 126, Issue 5 https://doi.org/10.1016/j.cell.2006.06.054	journal	September 2006
Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis Yoshida, Y.; Sano, R.; Wada, T. Development, Vol. 136, Issue 6 https://doi.org/10.1242/dev.030585	journal	February 2009
Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis Thireault, Caitlin; Shyu, Christine; Yoshida, Yuki The Plant Journal, Vol. 82, Issue 4 https://doi.org/10.1111/tpj.12841	journal	May 2015
Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany Wasternack, C.; Hause, B. Annals of Botany, Vol. 111, Issue 6 https://doi.org/10.1093/aob/mct067	journal	April 2013
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 Chung, Hoo Sun; Howe, Gregg A. The Plant Cell, Vol. 21, Issue 1 https://doi.org/10.1105/tpc.108.064097	journal	January 2009
Leaf growth in dicots and monocots: so different yet so alike Nelissen, Hilde; Gonzalez, Nathalie; Inzé, Dirk Current Opinion in Plant Biology, Vol. 33 https://doi.org/10.1016/j.pbi.2016.06.009	journal	October 2016
NINJA connects the co-repressor TOPLESS to jasmonate signalling Pauwels, Laurens; Barbero, Gemma Fernández; Geerinck, Jan Nature, Vol. 464, Issue 7289 https://doi.org/10.1038/nature08854	journal	April 2010
Cultivated and wild host plants supporting populations of the cabbage root fly Finch, S.; Ackley, Christine M. Annals of Applied Biology, Vol. 85, Issue 1 https://doi.org/10.1111/j.1744-7348.1977.tb00626.x	journal	January 1977
Transcriptomic analysis of female and male gonads in juvenile snakeskin gourami (Trichopodus pectoralis) Boonanuntanasarn, Surintorn; Jangprai, Araya; Na-Nakorn, Uthairat Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-61738-0	journal	March 2020
Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis Züst, Tobias; Agrawal, Anurag A. Annual Reviews https://doi.org/10.7892/boris.98942	text	January 2017
A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana Paul-Victor, C.; Züst, T.; Rees, M. Wiley-Blackwell https://doi.org/10.5167/uzh-35531	text	January 2010
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Nature Precedings https://doi.org/10.1038/npre.2010.4282.2	journal	April 2010

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Potential of zeolite to control Sclerotinia sclerotiorum and Rhizoctonia solani in lettuce and the induction of defence‐related genes Poulaki, Eirini G.; Gkizi, Danai; Tjamos, Sotirios E. Journal of Phytopathology, Vol. 168, Issue 2 https://doi.org/10.1111/jph.12875	journal	November 2019
APETALA2 control of barley internode elongation Patil, Vrushali; McDermott, Hannah I.; McAllister, Trisha Development, Vol. 146, Issue 11 https://doi.org/10.1242/dev.170373	journal	May 2019
Crosstalk with Jasmonic Acid Integrates Multiple Responses in Plant Development Jang, Geupil; Yoon, Youngdae; Choi, Yang Do International Journal of Molecular Sciences, Vol. 21, Issue 1 https://doi.org/10.3390/ijms21010305	journal	January 2020
Transcriptome Sequencing Analysis Provides Insights Into the Response to Fusarium oxysporum in Lilium pumilum He, Xiangfeng; Li, Wanyue; Zhang, Wenzhu Evolutionary Bioinformatics, Vol. 15 https://doi.org/10.1177/1176934319838818	journal	January 2019
Jasmonates-Mediated Rewiring of Central Metabolism Regulates Adaptive Responses Savchenko, Tatyana V.; Rolletschek, Hardy; Dehesh, Katayoon Plant and Cell Physiology, Vol. 60, Issue 12 https://doi.org/10.1093/pcp/pcz181	journal	September 2019
JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis Guo, Qiang; Yoshida, Yuki; Major, Ian T. Proceedings of the National Academy of Sciences, Vol. 115, Issue 45 https://doi.org/10.1073/pnas.1811828115	journal	October 2018
Dynamic gene expression changes in response to micronutrient, macronutrient, and multiple stress exposures in soybean O’Rourke, Jamie A.; McCabe, Chantal E.; Graham, Michelle A. Functional & Integrative Genomics, Vol. 20, Issue 3 https://doi.org/10.1007/s10142-019-00709-9	journal	October 2019
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Mechanisms of a locally adaptive shift in allocation among growth, reproduction, and herbivore resistance in Mimulus guttatus * Lowry, David B.; Popovic, Damian; Brennan, Darlene J. Evolution, Vol. 73, Issue 6 https://doi.org/10.1111/evo.13699	journal	March 2019
An effector from cotton bollworm oral secretion impairs host plant defense signaling Chen, Chun-Yu; Liu, Yao-Qian; Song, Wei-Meng Proceedings of the National Academy of Sciences, Vol. 116, Issue 28 https://doi.org/10.1073/pnas.1905471116	journal	June 2019
Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis Huot, Bethany; Castroverde, Christian Danve M.; Velásquez, André C. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01674-2	journal	November 2017
MYC5 is Involved in Jasmonate-Regulated Plant Growth, Leaf Senescence and Defense Responses Song, Susheng; Huang, Huang; Wang, Jiaojiao Plant and Cell Physiology, Vol. 58, Issue 10 https://doi.org/10.1093/pcp/pcx112	journal	August 2017
Jasmonate action in plant defense against insects Wang, Jiaojiao; Wu, Dewei; Wang, Youping Journal of Experimental Botany, Vol. 70, Issue 13 https://doi.org/10.1093/jxb/erz174	journal	April 2019
The JA‐pathway MYC transcription factors regulate photomorphogenic responses by targeting HY5 gene expression Ortigosa, Andrés; Fonseca, Sandra; Franco‐Zorrilla, José M. The Plant Journal, Vol. 102, Issue 1 https://doi.org/10.1111/tpj.14618	journal	January 2020
Phytohormones regulate convergent and divergent responses between individual and combined drought and pathogen infection Gupta, Aarti; Sinha, Ranjita; Fernandes, Joel Lars Critical Reviews in Biotechnology, Vol. 40, Issue 3 https://doi.org/10.1080/07388551.2019.1710459	journal	January 2020
A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels Van Moerkercke, Alex; Duncan, Owen; Zander, Mark Proceedings of the National Academy of Sciences, Vol. 116, Issue 46 https://doi.org/10.1073/pnas.1911758116	journal	October 2019
Plant-arthropod interactions: who is the winner? Stahl, Elia; Hilfiker, Olivier; Reymond, Philippe The Plant Journal, Vol. 93, Issue 4 https://doi.org/10.1111/tpj.13773	journal	December 2017
Arabidopsis MYB24 Regulates Jasmonate-Mediated Stamen Development Huang, Huang; Gao, Hua; Liu, Bei Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01525	journal	September 2017
Construction and characterization of a high-quality cDNA library of Cymbidium faberi suitable for yeast one- and two-hybrid assays Xu, Yanqin; Zhou, Junjiang; Liu, Qingqing BMC Biotechnology, Vol. 20, Issue 1 https://doi.org/10.1186/s12896-020-0599-2	journal	January 2020
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Full-length transcriptome sequencing and methyl jasmonate-induced expression profile analysis of genes related to patchoulol biosynthesis and regulation in Pogostemon cablin Chen, Xiuzhen; Li, Junren; Wang, Xiaobing BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-1884-x	journal	June 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 Yang, Jing; Duan, Guihua; Li, Chunqin Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01349	journal	October 2019
Mechanisms of a locally adaptive shift in allocation among growth, reproduction, and herbivore resistance in Mimulus guttatus Lowry, David B.; Popovic, Damian; Brennan, Darlene J. https://doi.org/10.1101/400523	posted_content	January 2019
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Stimulation of Insect Herbivory by Elevated Temperature Outweighs Protection by the Jasmonate Pathway Havko, Nathan E.; Kapali, George; Das, Michael R. Plants, Vol. 9, Issue 2 https://doi.org/10.3390/plants9020172	journal	February 2020

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

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