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Title: CPR5 modulates salicylic acid and the unfolded protein response to manage tradeoffs between plant growth and stress responses

Abstract

We report that completion of a plant's life cycle depends on successful prioritization of signaling favoring either growth or defense. Although hormones are pivotal regulators of growth-defense tradeoffs, the underlying signaling mechanisms remain obscure. The unfolded protein response (UPR) is essential for physiological growth as well as management of endoplasmic reticulum (ER) stress in unfavorable growth conditions. The plant UPR transducers are the kinase and ribonuclease IRE1 and the transcription factors bZIP28 and bZIP60. We analyzed management of the tradeoff between growth and ER stress defense by the stress response hormone salicylic acid (SA) and the UPR, which is modulated by SA via unknown mechanisms. We show that the plant growth and stress regulator CPR5, which represses accumulation of SA, favors growth in physiological conditions through inhibition of the SA-dependent IRE1-bZIP60 arm that antagonizes organ growth; CPR5 also favors growth in stress conditions through repression of ER stress-induced bZIP28/IRE1-bZIP60 arms. By demonstrating a physical interaction of CPR5 with bZIP60 and bZIP28, we provide mechanistic insights into CPR5-mediated modulation of UPR signaling. In conclusion, these findings define a critical surveillance strategy for plant growth-ER stress defense tradeoffs based on CPR5 and SA-modulated UPR signaling, whereby CPR5 acts as a positive modulatormore » of growth in physiological conditions and in stress by antagonizing SA-dependent growth inhibition through UPR modulation.« less

Authors:
 [1];  [2];  [3];  [2]
  1. Michigan State Univ., East Lansing, MI (United States); China Agricultural Univ., Beijing (China)
  2. Michigan State Univ., East Lansing, MI (United States)
  3. China Agricultural Univ., Beijing (China)
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Institutes of Health (NIH)
OSTI Identifier:
1596279
Alternate Identifier(s):
OSTI ID: 1401716
Grant/Contract Number:  
FG02-91ER20021; GM101038
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 89; Journal Issue: 3; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; CPR5; ER stress response; plant defense tradeoffs; salicylic acid; unfolded protein response; Arabidopsis thaliana

Citation Formats

Meng, Zhe, Ruberti, Cristina, Gong, Zhizhong, and Brandizzi, Federica. CPR5 modulates salicylic acid and the unfolded protein response to manage tradeoffs between plant growth and stress responses. United States: N. p., 2016. Web. doi:10.1111/tpj.13397.
Meng, Zhe, Ruberti, Cristina, Gong, Zhizhong, & Brandizzi, Federica. CPR5 modulates salicylic acid and the unfolded protein response to manage tradeoffs between plant growth and stress responses. United States. https://doi.org/10.1111/tpj.13397
Meng, Zhe, Ruberti, Cristina, Gong, Zhizhong, and Brandizzi, Federica. Sun . "CPR5 modulates salicylic acid and the unfolded protein response to manage tradeoffs between plant growth and stress responses". United States. https://doi.org/10.1111/tpj.13397. https://www.osti.gov/servlets/purl/1596279.
@article{osti_1596279,
title = {CPR5 modulates salicylic acid and the unfolded protein response to manage tradeoffs between plant growth and stress responses},
author = {Meng, Zhe and Ruberti, Cristina and Gong, Zhizhong and Brandizzi, Federica},
abstractNote = {We report that completion of a plant's life cycle depends on successful prioritization of signaling favoring either growth or defense. Although hormones are pivotal regulators of growth-defense tradeoffs, the underlying signaling mechanisms remain obscure. The unfolded protein response (UPR) is essential for physiological growth as well as management of endoplasmic reticulum (ER) stress in unfavorable growth conditions. The plant UPR transducers are the kinase and ribonuclease IRE1 and the transcription factors bZIP28 and bZIP60. We analyzed management of the tradeoff between growth and ER stress defense by the stress response hormone salicylic acid (SA) and the UPR, which is modulated by SA via unknown mechanisms. We show that the plant growth and stress regulator CPR5, which represses accumulation of SA, favors growth in physiological conditions through inhibition of the SA-dependent IRE1-bZIP60 arm that antagonizes organ growth; CPR5 also favors growth in stress conditions through repression of ER stress-induced bZIP28/IRE1-bZIP60 arms. By demonstrating a physical interaction of CPR5 with bZIP60 and bZIP28, we provide mechanistic insights into CPR5-mediated modulation of UPR signaling. In conclusion, these findings define a critical surveillance strategy for plant growth-ER stress defense tradeoffs based on CPR5 and SA-modulated UPR signaling, whereby CPR5 acts as a positive modulator of growth in physiological conditions and in stress by antagonizing SA-dependent growth inhibition through UPR modulation.},
doi = {10.1111/tpj.13397},
journal = {The Plant Journal},
number = 3,
volume = 89,
place = {United States},
year = {Sun Oct 16 00:00:00 EDT 2016},
month = {Sun Oct 16 00:00:00 EDT 2016}
}

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Works referenced in this record:

Interaction of CPR5 with Cell Cycle Regulators UVI4 and OSD1 in Arabidopsis
journal, June 2014


Spatial separation of Golgi and ER during mitosis protects SREBP from unregulated activation
journal, March 2008

  • Bartz, René; Sun, Li-Ping; Bisel, Blaine
  • The EMBO Journal, Vol. 27, Issue 7
  • DOI: 10.1038/emboj.2008.36

Analysis of Resistance Gene-Mediated Defense Responses in Arabidopsis thaliana Plants Carrying a Mutation in CPR5
journal, December 1998

  • Boch, Jens; Verbsky, Michelle L.; Robertson, Tara L.
  • Molecular Plant-Microbe Interactions, Vol. 11, Issue 12
  • DOI: 10.1094/MPMI.1998.11.12.1196

The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance.
journal, September 1997


Constitutive Expressor of Pathogenesis-Related Genes5 affects cell wall biogenesis and trichome development
journal, January 2008

  • Brininstool, Ginger; Kasili, Remmy; Simmons, L. Alice
  • BMC Plant Biology, Vol. 8, Issue 1
  • DOI: 10.1186/1471-2229-8-58

SIZ1-Dependent Post-Translational Modification by SUMO Modulates Sugar Signaling and Metabolism in Arabidopsis thaliana
journal, October 2015

  • Castro, Pedro Humberto; Verde, Nuno; Lourenço, Tiago
  • Plant and Cell Physiology, Vol. 56, Issue 12
  • DOI: 10.1093/pcp/pcv149

AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis
journal, October 2011


IRE1: ER stress sensor and cell fate executor
journal, November 2013


Signal peptide peptidase functions in ERAD to cleave the unfolded protein response regulator XBP 1u
journal, September 2014

  • Chen, Chia‐yi; Malchus, Nicole S.; Hehn, Beate
  • The EMBO Journal, Vol. 33, Issue 21
  • DOI: 10.15252/embj.201488208

Inter-regulation of the unfolded protein response and auxin signaling
journal, December 2013

  • Chen, Yani; Aung, Kyaw; Rolčík, Jakub
  • The Plant Journal, Vol. 77, Issue 1
  • DOI: 10.1111/tpj.12373

Roles of Salicylic Acid, Jasmonic Acid, and Ethylene in cpr -Induced Resistance in Arabidopsis
journal, November 2000

  • Clarke, Joseph D.; Volko, Sigrid M.; Ledford, Heidi
  • The Plant Cell, Vol. 12, Issue 11
  • DOI: 10.1105/tpc.12.11.2175

Secretory Pathway Research: The More Experimental Systems the Better
journal, April 2012

  • Denecke, Jurgen; Aniento, Fernando; Frigerio, Lorenzo
  • The Plant Cell, Vol. 24, Issue 4
  • DOI: 10.1105/tpc.112.096362

Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis
journal, April 2011

  • Deng, Y.; Humbert, S.; Liu, J. -X.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 17
  • DOI: 10.1073/pnas.1102117108

Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis
journal, October 2013

  • Deng, Y.; Srivastava, R.; Howell, S. H.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 48
  • DOI: 10.1073/pnas.1314749110

ELM 2016—data update and new functionality of the eukaryotic linear motif resource
journal, November 2015

  • Dinkel, Holger; Van Roey, Kim; Michael, Sushama
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1291

Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells
journal, March 2010

  • Fonseca, Sonya G.; Ishigaki, Shinsuke; Oslowski, Christine M.
  • Journal of Clinical Investigation, Vol. 120, Issue 3
  • DOI: 10.1172/JCI39678

A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana
journal, October 2008

  • Gao, H.; Brandizzi, F.; Benning, C.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 42
  • DOI: 10.1073/pnas.0808463105

Global analysis of protein expression in yeast
journal, October 2003

  • Ghaemmaghami, Sina; Huh, Won-Ki; Bower, Kiowa
  • Nature, Vol. 425, Issue 6959
  • DOI: 10.1038/nature02046

Development of PCR-based SNP markers for rice blast resistance genes at the Piz locus
journal, January 2004


bZIP17 and bZIP60 Regulate the Expression of BiP3 and Other Salt Stress Responsive Genes in an UPR-Independent Manner in Arabidopsis thaliana : bZIP17
journal, June 2015

  • Henriquez-Valencia, Carlos; Moreno, Adrian A.; Sandoval-Ibañez, Omar
  • Journal of Cellular Biochemistry, Vol. 116, Issue 8
  • DOI: 10.1002/jcb.25121

The unfolded protein response: controlling cell fate decisions under ER stress and beyond
journal, January 2012

  • Hetz, Claudio
  • Nature Reviews Molecular Cell Biology, Vol. 13, Issue 2
  • DOI: 10.1038/nrm3270

Endoplasmic Reticulum Stress Responses in Plants
journal, April 2013


Growth–Defense Tradeoffs in Plants: A Balancing Act to Optimize Fitness
journal, August 2014

  • Huot, Bethany; Yao, Jian; Montgomery, Beronda L.
  • Molecular Plant, Vol. 7, Issue 8
  • DOI: 10.1093/mp/ssu049

Function of IRE1 alpha in the placenta is essential for placental development and embryonic viability
journal, September 2009

  • Iwawaki, T.; Akai, R.; Yamanaka, S.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 39
  • DOI: 10.1073/pnas.0903775106

Arabidopsis COMPASS-Like Complexes Mediate Histone H3 Lysine-4 Trimethylation to Control Floral Transition and Plant Development
journal, March 2011


Early leaf senescence is associated with an altered cellular redox balance in Arabidopsis cpr5 / old1 mutants
journal, September 2008


CPR5 is involved in cell proliferation and cell death control and encodes a novel transmembrane protein
journal, November 2001


BAX Inhibitor-1 Is a Negative Regulator of the ER Stress Sensor IRE1α
journal, March 2009


Managing the protein folding demands in the endoplasmic reticulum of plants
journal, March 2016

  • Liu, Jian‐Xiang; Howell, Stephen H.
  • New Phytologist, Vol. 211, Issue 2
  • DOI: 10.1111/nph.13915

Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response
journal, March 2013

  • Mishiba, K. -i.; Nagashima, Y.; Suzuki, E.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 14
  • DOI: 10.1073/pnas.1219047110

Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor
journal, July 2011

  • Nagashima, Yukihiro; Mishiba, Kei-ichiro; Suzuki, Eiji
  • Scientific Reports, Vol. 1, Issue 1
  • DOI: 10.1038/srep00029

Exogenous Salicylic Acid Activates Two Signaling Arms of the Unfolded Protein Response in Arabidopsis
journal, August 2014

  • Nagashima, Yukihiro; Iwata, Yuji; Ashida, Makoto
  • Plant and Cell Physiology, Vol. 55, Issue 10
  • DOI: 10.1093/pcp/pcu108

How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory
journal, April 2016


Feedback Inhibition of the Unfolded Protein Response by GADD34 -Mediated Dephosphorylation of eIF2α
journal, May 2001

  • Novoa, Isabel; Zeng, Huiqing; Harding, Heather P.
  • The Journal of Cell Biology, Vol. 153, Issue 5
  • DOI: 10.1083/jcb.153.5.1011

GeBP/GPL Transcription Factors Regulate a Subset of CPR5 -Dependent Processes
journal, August 2011

  • Perazza, Daniel; Laporte, Frédéric; Balagué, Claudine
  • Plant Physiology, Vol. 157, Issue 3
  • DOI: 10.1104/pp.111.179804

Salicylic acid beyond defence: its role in plant growth and development
journal, February 2011

  • Rivas-San Vicente, M.; Plasencia, J.
  • Journal of Experimental Botany, Vol. 62, Issue 10
  • DOI: 10.1093/jxb/err031

Conserved and plant-unique strategies for overcoming endoplasmic reticulum stress
journal, January 2014


Unfolded protein response in plants: one master, many questions
journal, October 2015

  • Ruberti, Cristina; Kim, Sang-Jin; Stefano, Giovanni
  • Current Opinion in Plant Biology, Vol. 27
  • DOI: 10.1016/j.pbi.2015.05.016

Luminal Domain of ATF6 Alone Is Sufficient for Sensing Endoplasmic Reticulum Stress and Subsequent Transport to the Golgi Apparatus
journal, January 2011

  • Sato, Yoshimi; Nadanaka, Satomi; Okada, Tetsuya
  • Cell Structure and Function, Vol. 36, Issue 1
  • DOI: 10.1247/csf.10010

Organ-specific regulation of growth-defense tradeoffs by plants
journal, February 2016


Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants
journal, February 2015

  • Song, Ze-Ting; Sun, Le; Lu, Sun-Jie
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 9
  • DOI: 10.1073/pnas.1419703112

The Lumen-Facing Domain Is Important for the Biological Function and Organelle-to-Organelle Movement of bZIP28 during ER Stress in Arabidopsis
journal, September 2013

  • Sun, Le; Lu, Sun-Jie; Zhang, Shuang-Shuang
  • Molecular Plant, Vol. 6, Issue 5
  • DOI: 10.1093/mp/sst059

P58 IPK , a Novel Endoplasmic Reticulum Stress-inducible Protein and Potential Negative Regulator of eIF2α Signaling
journal, February 2003

  • van Huizen, Rika; Martindale, Jennifer L.; Gorospe, Myriam
  • Journal of Biological Chemistry, Vol. 278, Issue 18
  • DOI: 10.1074/jbc.M212074200

Plant hormone-mediated regulation of stress responses
journal, April 2016


Endoplasmic reticulum (ER) stress and the unfolded protein response (UPR) in plants
journal, June 2015


A Noncanonical Role for the CKI-RB-E2F Cell-Cycle Signaling Pathway in Plant Effector-Triggered Immunity
journal, December 2014


BAX Inhibitor-1 Modulates Endoplasmic Reticulum Stress-mediated Programmed Cell Death in Arabidopsis
journal, November 2007


Isochorismate synthase is required to synthesize salicylic acid for plant defence
journal, November 2001

  • Wildermuth, Mary C.; Dewdney, Julia; Wu, Gang
  • Nature, Vol. 414, Issue 6863
  • DOI: 10.1038/35107108

The Membrane-Associated Transcription Factor NAC089 Controls ER-Stress-Induced Programmed Cell Death in Plants
journal, March 2014


pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response
journal, February 2006

  • Yoshida, Hiderou; Oku, Masaya; Suzuki, Mie
  • The Journal of Cell Biology, Vol. 172, Issue 4
  • DOI: 10.1083/jcb.200508145

A Genetic Screen Reveals Arabidopsis Stomatal and/or Apoplastic Defenses against Pseudomonas syringae pv. tomato DC3000
journal, October 2011


Works referencing / citing this record:

AtIRE1C, an unconventional isoform of the UPR master regulator AtIRE1, is functionally associated with AtIRE1B in Arabidopsis gametogenesis
journal, November 2019

  • Pu, Yunting; Ruberti, Cristina; Angelos, Evan R.
  • Plant Direct, Vol. 3, Issue 11
  • DOI: 10.1002/pld3.187

Genomic basis of European ash tree resistance to ash dieback fungus
journal, November 2019

  • Stocks, Jonathan J.; Metheringham, Carey L.; Plumb, William J.
  • Nature Ecology & Evolution, Vol. 3, Issue 12
  • DOI: 10.1038/s41559-019-1036-6

Putative alternative translation start site-encoding nucleotides of CPR5 regulate growth and resistance
journal, June 2020

  • Faisal, Muhammad B.; Gechev, Tsanko S.; Mueller-Roeber, Bernd
  • BMC Plant Biology, Vol. 20, Issue 1
  • DOI: 10.1186/s12870-020-02485-2

A high-throughput screening method to identify proteins involved in unfolded protein response of the endoplasmic reticulum in plants
journal, January 2020


Unfolded protein-independent IRE1 activation contributes to multifaceted developmental processes in Arabidopsis
journal, October 2019

  • Mishiba, Kei-ichiro; Iwata, Yuji; Mochizuki, Tomofumi
  • Life Science Alliance, Vol. 2, Issue 5
  • DOI: 10.26508/lsa.201900459

Endoplasmic Reticulum Plays a Critical Role in Integrating Signals Generated by Both Biotic and Abiotic Stress in Plants
journal, April 2019


The Multifaceted Roles of Plant Hormone Salicylic Acid in Endoplasmic Reticulum Stress and Unfolded Protein Response
journal, November 2019

  • Poór, Péter; Czékus, Zalán; Tari, Irma
  • International Journal of Molecular Sciences, Vol. 20, Issue 23
  • DOI: 10.3390/ijms20235842

AtIRE1C, an unconventional isoform of the UPR master regulator AtIRE1, is functionally associated with AtIRE1B in Arabidopsis gametogenesis
journal, November 2019

  • Pu, Yunting; Ruberti, Cristina; Angelos, Evan R.
  • Plant Direct, Vol. 3, Issue 11
  • DOI: 10.1002/pld3.187

Protein Quality Control in Plant Organelles: Current Progress and Future Perspectives
journal, January 2021


NAA50 Is an Enzymatically Active Nα-Acetyltransferase That Is Crucial for Development and Regulation of Stress Responses
journal, May 2020

  • Armbruster, Laura; Linster, Eric; Boyer, Jean-Baptiste
  • Plant Physiology, Vol. 183, Issue 4
  • DOI: 10.1104/pp.20.00222

Endoplasmic Reticulum Plays a Critical Role in Integrating Signals Generated by Both Biotic and Abiotic Stress in Plants
journal, April 2019


The Multifaceted Roles of Plant Hormone Salicylic Acid in Endoplasmic Reticulum Stress and Unfolded Protein Response
journal, November 2019

  • Poór, Péter; Czékus, Zalán; Tari, Irma
  • International Journal of Molecular Sciences, Vol. 20, Issue 23
  • DOI: 10.3390/ijms20235842