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Title: Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs

Abstract

Plants resist infection and herbivory with innate immune responses that are often associated with reduced growth. Despite the importance of growth-defense tradeoffs in shaping plant productivity in natural and agricultural ecosystems, the molecular mechanisms that link growth and immunity are poorly understood. Here, we demonstrate that growth-defense tradeoffs mediated by the hormone jasmonate are uncoupled in an Arabidopsis mutant (jazQ phyB) lacking a quintet of Jasmonate ZIM-domain transcriptional repressors and the photoreceptor phyB. Analysis of epistatic interactions between jazQ and phyB reveal that growth inhibition associated with enhanced anti-insect resistance is likely not caused by diversion of photoassimilates from growth to defense but rather by a conserved transcriptional network that is hardwired to attenuate growth upon activation of jasmonate signalling. Furthermore, the ability to unlock growth-defense tradeoffs through relief of transcription repression provides an approach to assemble functional plant traits in new and potentially useful ways.

Authors:
 [1];  [2];  [3];  [3];  [4];  [4];  [3];  [4];  [5];  [6];  [4]
  1. Dept. of Energy - Plant Research Lab., East Lansing, MI (United States); Univ. de Brasilia, Brasilia (Brazil)
  2. Dept. of Energy - Plant Research Lab., East Lansing, MI (United States); The Univ. of Tokyo, Tokyo (Japan)
  3. Dept. of Energy - Plant Research Lab., East Lansing, MI (United States)
  4. Dept. of Energy - Plant Research Lab., East Lansing, MI (United States); Michigan State Univ., East Lansing, MI (United States)
  5. Boyce Thompson Institute for Plant Research, Ithaca, NY (United States)
  6. Michigan State Univ., East Lansing, MI (United States)
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1362017
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; herbivory; jasmonic acid; light responses; plant signalling

Citation Formats

Campos, Marcelo L., Yoshida, Yuki, Major, Ian T., de Oliveira Ferreira, Dalton, Weraduwage, Sarathi M., Froehlich, John E., Johnson, Brendan F., Kramer, David M., Jander, Georg, Sharkey, Thomas D., and Howe, Gregg A. Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. United States: N. p., 2016. Web. doi:10.1038/ncomms12570.
Campos, Marcelo L., Yoshida, Yuki, Major, Ian T., de Oliveira Ferreira, Dalton, Weraduwage, Sarathi M., Froehlich, John E., Johnson, Brendan F., Kramer, David M., Jander, Georg, Sharkey, Thomas D., & Howe, Gregg A. Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. United States. https://doi.org/10.1038/ncomms12570
Campos, Marcelo L., Yoshida, Yuki, Major, Ian T., de Oliveira Ferreira, Dalton, Weraduwage, Sarathi M., Froehlich, John E., Johnson, Brendan F., Kramer, David M., Jander, Georg, Sharkey, Thomas D., and Howe, Gregg A. Tue . "Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs". United States. https://doi.org/10.1038/ncomms12570. https://www.osti.gov/servlets/purl/1362017.
@article{osti_1362017,
title = {Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs},
author = {Campos, Marcelo L. and Yoshida, Yuki and Major, Ian T. and de Oliveira Ferreira, Dalton and Weraduwage, Sarathi M. and Froehlich, John E. and Johnson, Brendan F. and Kramer, David M. and Jander, Georg and Sharkey, Thomas D. and Howe, Gregg A.},
abstractNote = {Plants resist infection and herbivory with innate immune responses that are often associated with reduced growth. Despite the importance of growth-defense tradeoffs in shaping plant productivity in natural and agricultural ecosystems, the molecular mechanisms that link growth and immunity are poorly understood. Here, we demonstrate that growth-defense tradeoffs mediated by the hormone jasmonate are uncoupled in an Arabidopsis mutant (jazQ phyB) lacking a quintet of Jasmonate ZIM-domain transcriptional repressors and the photoreceptor phyB. Analysis of epistatic interactions between jazQ and phyB reveal that growth inhibition associated with enhanced anti-insect resistance is likely not caused by diversion of photoassimilates from growth to defense but rather by a conserved transcriptional network that is hardwired to attenuate growth upon activation of jasmonate signalling. Furthermore, the ability to unlock growth-defense tradeoffs through relief of transcription repression provides an approach to assemble functional plant traits in new and potentially useful ways.},
doi = {10.1038/ncomms12570},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {Tue Aug 30 00:00:00 EDT 2016},
month = {Tue Aug 30 00:00:00 EDT 2016}
}

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  • Communicative & Integrative Biology, Vol. 12, Issue 1
  • DOI: 10.1080/19420889.2019.1625661

A Vitis vinifera basic helix-loop-helix transcription factor enhances plant cell size, vegetative biomass and reproductive yield
journal, April 2018

  • Lim, Sung Don; Yim, Won Choel; Liu, Degao
  • Plant Biotechnology Journal, Vol. 16, Issue 9
  • DOI: 10.1111/pbi.12898

A plant's balance of growth and defense - revisited
journal, August 2017


The common bean COK-4 and the Arabidopsis FER kinase domain share similar functions in plant growth and defence: COK-4 functions in plant growth and defence
journal, March 2018

  • Azevedo, Rafhael Felipin; Gonçalves-Vidigal, Maria Celeste; Oblessuc, Paula Rodrigues
  • Molecular Plant Pathology, Vol. 19, Issue 7
  • DOI: 10.1111/mpp.12659

Orthogonal regulation of phytochrome B abundance by stress-specific plastidial retrograde signaling metabolite
journal, July 2019


A rationally designed JAZ subtype-selective agonist of jasmonate perception
journal, September 2018


An effector from cotton bollworm oral secretion impairs host plant defense signaling
journal, June 2019

  • Chen, Chun-Yu; Liu, Yao-Qian; Song, Wei-Meng
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 28
  • DOI: 10.1073/pnas.1905471116

The IMMUNE-ASSOCIATED NUCLEOTIDE-BINDING 9 protein is a regulator of basal immunity in Arabidopsis thaliana
journal, June 2018

  • Wang, Yuanzheng; Li, Yansha; Rosas-Diaz, Tabata
  • Molecular Plant-Microbe Interactions
  • DOI: 10.1101/277269

Constitutive activity of the Arabidopsis MAP Kinase 3 confers resistance to Pseudomonas syringae and drives robust immune responses
journal, August 2017


Heritable plant phenotypes track light and herbivory levels at fine spatial scales
journal, March 2018


Exploring growth‐defence trade‐offs in Arabidopsis: phytochrome B inactivation requires JAZ10 to suppress plant immunity but not to trigger shade‐avoidance responses
journal, February 2017

  • Cerrudo, Ignacio; Caliri‐Ortiz, M. Emilia; Keller, Mercedes M.
  • Plant, Cell & Environment, Vol. 40, Issue 5
  • DOI: 10.1111/pce.12877

An effector from cotton bollworm oral secretion impairs host plant defense signaling
journal, June 2019

  • Chen, Chun-Yu; Liu, Yao-Qian; Song, Wei-Meng
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 28
  • DOI: 10.1073/pnas.1905471116

Unraveling the Genetic Elements Involved in Shoot and Root Growth Regulation by Jasmonate in Rice Using a Genome-Wide Association Study
journal, September 2019


Functional variation in a key defense gene structures herbivore communities and alters plant performance
journal, June 2018


The IMMUNE-ASSOCIATED NUCLEOTIDE-BINDING 9 Protein Is a Regulator of Basal Immunity in Arabidopsis thaliana
journal, January 2019

  • Wang, Yuanzheng; Li, Yansha; Rosas-Diaz, Tabata
  • Molecular Plant-Microbe Interactions®, Vol. 32, Issue 1
  • DOI: 10.1094/mpmi-03-18-0062-r

Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future
journal, July 2018

  • Sharifi, Rouhallah; Ryu, Choong-Min
  • Annals of Botany, Vol. 122, Issue 3
  • DOI: 10.1093/aob/mcy108

Jasmonate action in plant defense against insects
journal, April 2019

  • Wang, Jiaojiao; Wu, Dewei; Wang, Youping
  • Journal of Experimental Botany, Vol. 70, Issue 13
  • DOI: 10.1093/jxb/erz174

The JA‐pathway MYC transcription factors regulate photomorphogenic responses by targeting HY5 gene expression
journal, January 2020

  • Ortigosa, Andrés; Fonseca, Sandra; Franco‐Zorrilla, José M.
  • The Plant Journal, Vol. 102, Issue 1
  • DOI: 10.1111/tpj.14618

Jasmonate action in plant growth and development
journal, February 2017

  • Huang, Huang; Liu, Bei; Liu, Liangyu
  • Journal of Experimental Botany, Vol. 68, Issue 6
  • DOI: 10.1093/jxb/erw495

Isoprene: New insights into the control of emission and mediation of stress tolerance by gene expression
journal, August 2019

  • Lantz, Alexandra T.; Allman, Joshua; Weraduwage, Sarathi M.
  • Plant, Cell & Environment, Vol. 42, Issue 10
  • DOI: 10.1111/pce.13629

Ecological interactions shape the adaptive value of plant defence: Herbivore attack versus competition for light
journal, November 2018


Ticagrelor induces paraoxonase-1 (PON1) and better protects hypercholesterolemic mice against atherosclerosis compared to clopidogrel
journal, June 2019


Advances on plant-pathogen interactions from molecular toward systems biology perspectives
journal, February 2017

  • Peyraud, Rémi; Dubiella, Ullrich; Barbacci, Adelin
  • The Plant Journal, Vol. 90, Issue 4
  • DOI: 10.1111/tpj.13429

A comprehensive in vitro fluorescence anisotropy assay system for screening ligands of the jasmonate COI1–JAZ co-receptor in plants
journal, February 2019

  • Takaoka, Yousuke; Nagumo, Keina; Azizah, Ika Nurul
  • Journal of Biological Chemistry, Vol. 294, Issue 13
  • DOI: 10.1074/jbc.ra118.006639

Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module
journal, June 2017

  • Major, Ian T.; Yoshida, Yuki; Campos, Marcelo L.
  • New Phytologist, Vol. 215, Issue 4
  • DOI: 10.1111/nph.14638

Heritable plant phenotypes track light and herbivory levels at fine spatial scales
journal, October 2017

  • Humphrey, P. T.; Gloss, A. D.; Frazier, J.
  • Oecologia
  • DOI: 10.1101/210765

Risk of herbivore attack and heritability of ontogenetic trajectories in plant defense
journal, February 2018


SmJAZ8 acts as a core repressor regulating JA-induced biosynthesis of salvianolic acids and tanshinones in Salvia miltiorrhiza hairy roots
journal, December 2017

  • Pei, Tianlin; Ma, Pengda; Ding, Kai
  • Journal of Experimental Botany, Vol. 69, Issue 7
  • DOI: 10.1093/jxb/erx484

Regulation of Lignin Biosynthesis and Its Role in Growth-Defense Tradeoffs
journal, September 2018


Stimulation of Insect Herbivory by Elevated Temperature Outweighs Protection by the Jasmonate Pathway
journal, February 2020


Plant immunity in signal integration between biotic and abiotic stress responses
journal, July 2019

  • Saijo, Yusuke; Loo, Eliza Po‐iian
  • New Phytologist, Vol. 225, Issue 1
  • DOI: 10.1111/nph.15989

Regulation of Lignin Biosynthesis and Its Role in Growth-Defense Tradeoffs
journal, September 2018


A light-dependent molecular link between competition cues and defence responses in plants
journal, March 2020

  • Fernández-Milmanda, Guadalupe L.; Crocco, Carlos D.; Reichelt, Michael
  • Nature Plants, Vol. 6, Issue 3
  • DOI: 10.1038/s41477-020-0604-8

Editorial: Plant Responses to Phytophagous Mites/Thrips and Search for Resistance
journal, July 2019

  • Sperotto, Raul A.; Grbic, Vojislava; Pappas, Maria L.
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00866

To defend or to grow: lessons from Arabidopsis C24
journal, March 2018

  • Bechtold, Ulrike; Ferguson, John N.; Mullineaux, Philip M.
  • Journal of Experimental Botany, Vol. 69, Issue 11
  • DOI: 10.1093/jxb/ery106

Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors
journal, January 2020


Editorial: Plant Responses to Phytophagous Mites/Thrips and Search for Resistance
journal, July 2019

  • Sperotto, Raul A.; Grbic, Vojislava; Pappas, Maria L.
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00866

Mechanisms of a locally adaptive shift in allocation among growth, reproduction, and herbivore resistance in Mimulus guttatus *
journal, March 2019

  • Lowry, David B.; Popovic, Damian; Brennan, Darlene J.
  • Evolution, Vol. 73, Issue 6
  • DOI: 10.1111/evo.13699

Ticagrelor induces paraoxonase-1 (PON1) and better protects hypercholesterolemic mice against atherosclerosis compared to clopidogrel
journal, June 2019


MYC5 is Involved in Jasmonate-Regulated Plant Growth, Leaf Senescence and Defense Responses
journal, August 2017

  • Song, Susheng; Huang, Huang; Wang, Jiaojiao
  • Plant and Cell Physiology, Vol. 58, Issue 10
  • DOI: 10.1093/pcp/pcx112

Functional variation in a key defense gene structures herbivore communities and alters plant performance
journal, June 2018


Distinct Morphological, Physiological, and Biochemical Responses to Light Quality in Barley Leaves and Roots
journal, August 2019

  • Klem, Karel; Gargallo-Garriga, Albert; Rattanapichai, Wutthida
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.01026

Epistatic Transcription Factor Networks Differentially Modulate Arabidopsis Growth and Defense
journal, June 2019

  • Li, Baohua; Tang, Michelle; Caseys, Céline
  • Genetics
  • DOI: 10.1101/583047

Molecular mechanisms controlling plant growth during abiotic stress
journal, May 2018

  • Bechtold, Ulrike; Field, Benjamin
  • Journal of Experimental Botany, Vol. 69, Issue 11
  • DOI: 10.1093/jxb/ery157

Recalculating growth and defense strategies under competition: key roles of photoreceptors and jasmonates
journal, May 2019

  • Ballaré, Carlos L.; Austin, Amy T.
  • Journal of Experimental Botany, Vol. 70, Issue 13
  • DOI: 10.1093/jxb/erz237

Rapid and independent evolution of ancestral and novel defenses in a genus of toxic plants ( Erysimum , Brassicaceae)
journal, September 2019

  • Züst, Tobias; Strickler, Susan R.; Powell, Adrian F.
  • eLife
  • DOI: 10.1101/761569

Ecological interactions shape the adaptive value of plant defence: Herbivore attack versus competition for light
journal, November 2018


Cry1Ac production is costly for native plants attacked by non-Cry1Ac-targeted herbivores in the field
journal, May 2018

  • McGale, Erica; Diezel, Celia; Schuman, Meredith C.
  • New Phytologist, Vol. 219, Issue 2
  • DOI: 10.1111/nph.15207

Epistatic Transcription Factor Networks Differentially ModulateArabidopsisGrowth and Defense
journal, February 2020