Salicylic acid-independent role of NPR1 is required for protection from proteotoxic stress in the plant endoplasmic reticulum

Lai, Ya-Shiuan; Renna, Luciana; Yarema, John; Ruberti, Cristina; He, Sheng Yang; Brandizzi, Federica

doi:10.1073/pnas.1802254115

Title: Salicylic acid-independent role of NPR1 is required for protection from proteotoxic stress in the plant endoplasmic reticulum

Journal Article · Mon May 14 00:00:00 EDT 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1802254115· OSTI ID:1437094

Lai, Ya-Shiuan ^[1]; Renna, Luciana ^[2]; Yarema, John ^[2];

^[2]; He, Sheng Yang ^[3];

^[4]

Michigan State University-US Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Cell and Molecular Biology Program, Michigan State University, East Lansing, MI 48824,
Michigan State University-US Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,
Michigan State University-US Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Plant Biology Department, Michigan State University, East Lansing, MI 48824,, Howard Hughes Medical Institute, Michigan State University, East Lansing, MI 48824
Michigan State University-US Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Plant Biology Department, Michigan State University, East Lansing, MI 48824,

The unfolded protein response (UPR) is an ancient signaling pathway designed to protect cells from the accumulation of unfolded and misfolded proteins in the endoplasmic reticulum (ER). Because misregulation of the UPR is potentially lethal, a stringent surveillance signaling system must be in place to modulate the UPR. The vital signaling arms of the plant UPR have been discovered and rely on the transcriptional activity of the transcription factors bZIP60 and bZIP28 and on the kinase and ribonuclease activity of IRE1, which splices mRNA to activate bZIP60. Both bZIP28 and bZIP60 modulate UPR gene expression to overcome ER stress. In this study, we demonstrate at a genetic level that the transcriptional role of bZIP28 and bZIP60 in ER-stress responses is antagonized by nonexpressor of PR1 genes 1 (NPR1), a critical redox-regulated master regulator of salicylic acid (SA)-dependent responses to pathogens, independently of its role in SA defense. Moreover, we establish that the function of NPR1 in the UPR is concomitant with ER stress-induced reduction of the cytosol and translocation of NPR1 to the nucleus where it interacts with bZIP28 and bZIP60. Our findings indicate a cellular role for NPR1 as well as a model for plant UPR regulation whereby SA-independent ER stress-induced redox activation of NPR1 suppresses the transcriptional role of bZIP28 and bZIP60 in the UPR.

View Journal Article

Cite

Export

Save

Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Institutes of Health (NIH)

Grant/Contract Number:: FG02-91ER20021

OSTI ID:: 1437094

Alternate ID(s):: OSTI ID: 1540290

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: 22; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 46 works

Citation information provided by
Web of Science

References (65)

Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling: Salt stress elicits ER stress response Liu, Jian-Xiang; Srivastava, Renu; Che, Ping The Plant Journal, Vol. 51, Issue 5 https://doi.org/10.1111/j.1365-313X.2007.03195.x	journal	July 2007
Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis Deng, Y.; Srivastava, R.; Howell, S. H. Proceedings of the National Academy of Sciences, Vol. 110, Issue 48 https://doi.org/10.1073/pnas.1314749110	journal	October 2013
BAX Inhibitor-1 Is a Negative Regulator of the ER Stress Sensor IRE1α Lisbona, Fernanda; Rojas-Rivera, Diego; Thielen, Peter Molecular Cell, Vol. 33, Issue 6 https://doi.org/10.1016/j.molcel.2009.02.017	journal	March 2009
Exogenous Salicylic Acid Activates Two Signaling Arms of the Unfolded Protein Response in Arabidopsis Nagashima, Yukihiro; Iwata, Yuji; Ashida, Makoto Plant and Cell Physiology, Vol. 55, Issue 10 https://doi.org/10.1093/pcp/pcu108	journal	August 2014
Arabidopsis Clade I TGA Factors Regulate Apoplastic Defences against the Bacterial Pathogen Pseudomonas syringae through Endoplasmic Reticulum-Based Processes Wang, Lipu; Fobert, Pierre R. PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0077378	journal	September 2013
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
Sec22 and Memb11 Are v-SNAREs of the Anterograde Endoplasmic Reticulum-Golgi Pathway in Tobacco Leaf Epidermal Cells Chatre, Laurent; Brandizzi, Federica; Hocquellet, Agnès Plant Physiology, Vol. 139, Issue 3 https://doi.org/10.1104/pp.105.067447	journal	October 2005
Inter-regulation of the unfolded protein response and auxin signaling Chen, Yani; Aung, Kyaw; Rolčík, Jakub The Plant Journal, Vol. 77, Issue 1 https://doi.org/10.1111/tpj.12373	journal	December 2013
Identification of Novel Components of the Unfolded Protein Response in Arabidopsis Hossain, Md. Amir; Henríquez-Valencia, Carlos; Gómez-Páez, Marcela Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00650	journal	May 2016
The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition Pajerowska-Mukhtar, Karolina M.; Wang, Wei; Tada, Yasuomi Current Biology, Vol. 22, Issue 2 https://doi.org/10.1016/j.cub.2011.12.015	journal	January 2012
AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis Chen, Yani; Brandizzi, Federica The Plant Journal, Vol. 69, Issue 2 https://doi.org/10.1111/j.1365-313X.2011.04788.x	journal	October 2011
Identification and Characterization of Nuclear Pore Complex Components in Arabidopsis thaliana Tamura, Kentaro; Fukao, Yoichiro; Iwamoto, Masaaki The Plant Cell, Vol. 22, Issue 12 https://doi.org/10.1105/tpc.110.079947	journal	December 2010
Arabidopsis bZIP60 Is a Proteolysis-Activated Transcription Factor Involved in the Endoplasmic Reticulum Stress Response Iwata, Yuji; Fedoroff, Nina V.; Koizumi, Nozomu The Plant Cell, Vol. 20, Issue 11 https://doi.org/10.1105/tpc.108.061002	journal	November 2008
Induction of Protein Secretory Pathway Is Required for Systemic Acquired Resistance Wang, D. Science, Vol. 308, Issue 5724 https://doi.org/10.1126/science.1108791	journal	May 2005
Oxidative protein folding and unfolded protein response elicit differing redox regulation in endoplasmic reticulum and cytosol of yeast Delic, Marizela; Rebnegger, Corinna; Wanka, Franziska Free Radical Biology and Medicine, Vol. 52, Issue 9 https://doi.org/10.1016/j.freeradbiomed.2012.02.048	journal	May 2012
Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells Fonseca, Sonya G.; Ishigaki, Shinsuke; Oslowski, Christine M. Journal of Clinical Investigation, Vol. 120, Issue 3 https://doi.org/10.1172/JCI39678	journal	March 2010
ER Stress Induces Cleavage of Membrane-Bound ATF6 by the Same Proteases that Process SREBPs Ye, Jin; Rawson, Robert B.; Komuro, Ryutaro Molecular Cell, Vol. 6, Issue 6 https://doi.org/10.1016/S1097-2765(00)00133-7	journal	December 2000
Modulation of Cellular Disulfide-Bond Formation and the ER Redox Environment by Feedback Regulation of Ero1 Sevier, Carolyn S.; Qu, Hongjing; Heldman, Nimrod Cell, Vol. 129, Issue 2 https://doi.org/10.1016/j.cell.2007.02.039	journal	April 2007
From Pioneers to Team Players: TGA Transcription Factors Provide a Molecular Link Between Different Stress Pathways Gatz, Christiane Molecular Plant-Microbe Interactions, Vol. 26, Issue 2 https://doi.org/10.1094/MPMI-04-12-0078-IA	journal	February 2013
Arabidopsis CaM Binding Protein CBP60g Contributes to MAMP-Induced SA Accumulation and Is Involved in Disease Resistance against Pseudomonas syringae Wang, Lin; Tsuda, Kenichi; Sato, Masanao PLoS Pathogens, Vol. 5, Issue 2 https://doi.org/10.1371/journal.ppat.1000301	journal	February 2009
A monomeric red fluorescent protein Campbell, R. E.; Tour, O.; Palmer, A. E. Proceedings of the National Academy of Sciences, Vol. 99, Issue 12, p. 7877-7882 https://doi.org/10.1073/pnas.082243699	journal	June 2002
An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants Iwata, Y.; Koizumi, N. Proceedings of the National Academy of Sciences, Vol. 102, Issue 14 https://doi.org/10.1073/pnas.0408941102	journal	March 2005
The Arabidopsis bZIP1 Transcription Factor Is Involved in Sugar Signaling, Protein Networking, and DNA Binding Kang, Shin Gene; Price, John; Lin, Pei-Chi Molecular Plant, Vol. 3, Issue 2 https://doi.org/10.1093/mp/ssp115	journal	March 2010
Isochorismate synthase is required to synthesize salicylic acid for plant defence Wildermuth, Mary C.; Dewdney, Julia; Wu, Gang Nature, Vol. 414, Issue 6863 https://doi.org/10.1038/35107108	journal	November 2001
In Vivo Interaction between NPR1 and Transcription Factor TGA2 Leads to Salicylic Acid–Mediated Gene Activation in Arabidopsis Fan, Weihua; Dong, Xinnian The Plant Cell, Vol. 14, Issue 6 https://doi.org/10.1105/tpc.001628	journal	June 2002
A Genetic Screen Reveals Arabidopsis Stomatal and/or Apoplastic Defenses against Pseudomonas syringae pv. tomato DC3000 Zeng, Weiqing; Brutus, Alexandre; Kremer, James M. PLoS Pathogens, Vol. 7, Issue 10 https://doi.org/10.1371/journal.ppat.1002291	journal	October 2011
The eIF2α/ATF4 pathway is essential for stress-induced autophagy gene expression B’chir, Wafa; Maurin, Anne-Catherine; Carraro, Valérie Nucleic Acids Research, Vol. 41, Issue 16 https://doi.org/10.1093/nar/gkt563	journal	June 2013
IRE1/bZIP60-Mediated Unfolded Protein Response Plays Distinct Roles in Plant Immunity and Abiotic Stress Responses Moreno, Adrian A.; Mukhtar, M. Shahid; Blanco, Francisca PLoS ONE, Vol. 7, Issue 2 https://doi.org/10.1371/journal.pone.0031944	journal	February 2012
Endoplasmic Reticulum Export Sites and Golgi Bodies Behave as Single Mobile Secretory Units in Plant Cells daSilva, Luis L. P.; Snapp, Erik L.; Denecke, Jürgen The Plant Cell, Vol. 16, Issue 7 https://doi.org/10.1105/tpc.022673	journal	June 2004
Interaction of NIMIN1 with NPR1 Modulates PR Gene Expression in Arabidopsis Weigel, Ralf R.; Pfitzner, Ursula M.; Gatz, Christiane The Plant Cell, Vol. 17, Issue 4 https://doi.org/10.1105/tpc.104.027441	journal	March 2005
Interaction of the K ⁺ -channel KAT1 with the coat protein complex II coat component Sec24 depends on a di-acidic endoplasmic reticulum export motif Sieben, Christian; Mikosch, Melanie; Brandizzi, Federica The Plant Journal, Vol. 56, Issue 6 https://doi.org/10.1111/j.1365-313X.2008.03658.x	journal	December 2008
The Coactivator Function of Arabidopsis NPR1 Requires the Core of Its BTB/POZ Domain and the Oxidation of C-Terminal Cysteines Rochon, Amanda; Boyle, Patrick; Wignes, Tracy The Plant Cell, Vol. 18, Issue 12 https://doi.org/10.1105/tpc.106.046953	journal	December 2006
Nuclear Localization of NPR1 Is Required for Activation of PR Gene Expression Kinkema, Mark; Fan, Weihua; Dong, Xinnian The Plant Cell, Vol. 12, Issue 12 https://doi.org/10.1105/tpc.12.12.2339	journal	December 2000
A trip to the ER: coping with stress Rutkowski, D. Thomas; Kaufman, Randal J. Trends in Cell Biology, Vol. 14, Issue 1 https://doi.org/10.1016/j.tcb.2003.11.001	journal	January 2004
Investigating Mitochondrial Redox Potential with Redox-sensitive Green Fluorescent Protein Indicators Hanson, George T.; Aggeler, Robert; Oglesbee, Devin Journal of Biological Chemistry, Vol. 279, Issue 13 https://doi.org/10.1074/jbc.M312846200	journal	January 2004
bZIP28 and NF-Y Transcription Factors Are Activated by ER Stress and Assemble into a Transcriptional Complex to Regulate Stress Response Genes in Arabidopsis Liu, Jian-Xiang; Howell, Stephen H. The Plant Cell, Vol. 22, Issue 3 https://doi.org/10.1105/tpc.109.072173	journal	March 2010
Activation of autophagy by unfolded proteins during endoplasmic reticulum stress Yang, Xiaochen; Srivastava, Renu; Howell, Stephen H. The Plant Journal, Vol. 85, Issue 1 https://doi.org/10.1111/tpj.13091	journal	December 2015
Golgi Traffic and Integrity Depend on N-Myristoyl Transferase-1 in Arabidopsis Renna, Luciana; Stefano, Giovanni; Majeran, Wojciech The Plant Cell, Vol. 25, Issue 5 https://doi.org/10.1105/tpc.113.111393	journal	May 2013
The Arabidopsis NPR1/NIM1 Protein Enhances the DNA Binding Activity of a Subgroup of the TGA Family of bZIP Transcription Factors Després, Charles; DeLong, Catherine; Glaze, Sarah The Plant Cell, Vol. 12, Issue 2 https://doi.org/10.1105/tpc.12.2.279	journal	February 2000
Inducers of Plant Systemic Acquired Resistance Regulate NPR1 Function through Redox Changes Mou, Zhonglin; Fan, Weihua; Dong, Xinnian Cell, Vol. 113, Issue 7 https://doi.org/10.1016/S0092-8674(03)00429-X	journal	June 2003
ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 Repress SALICYLIC ACID INDUCTION DEFICIENT2 Expression to Negatively Regulate Plant Innate Immunity in Arabidopsis Chen, Huamin; Xue, Li; Chintamanani, Satya The Plant Cell, Vol. 21, Issue 8 https://doi.org/10.1105/tpc.108.065193	journal	August 2009
The unfolded protein response in nutrient sensing and differentiation Kaufman, Randal J.; Scheuner, Donalyn; Schröder, Martin Nature Reviews Molecular Cell Biology, Vol. 3, Issue 6 https://doi.org/10.1038/nrm829	journal	June 2002
Saturation of the Endoplasmic Reticulum Retention Machinery Reveals Anterograde Bulk Flow Crofts, Andrew J.; Leborgne-Castel, Nathalie; Hillmer, Stefan The Plant Cell, Vol. 11, Issue 11 https://doi.org/10.1105/tpc.11.11.2233	journal	November 1999
The Saccharomyces cerevisiae AMPK, Snf1, Negatively Regulates the Hog1 MAPK Pathway in ER Stress Response Mizuno, Tomoaki; Masuda, Yuto; Irie, Kenji PLOS Genetics, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pgen.1005491	journal	September 2015
MPSR1 is a cytoplasmic PQC E3 ligase for eliminating emergent misfolded proteins in Arabidopsis thaliana Kim, Jong Hum; Cho, Seok Keun; Oh, Tae Rin Proceedings of the National Academy of Sciences, Vol. 114, Issue 46 https://doi.org/10.1073/pnas.1713574114	journal	October 2017
The Lumen-Facing Domain Is Important for the Biological Function and Organelle-to-Organelle Movement of bZIP28 during ER Stress in Arabidopsis Sun, Le; Lu, Sun-Jie; Zhang, Shuang-Shuang Molecular Plant, Vol. 6, Issue 5 https://doi.org/10.1093/mp/sst059	journal	September 2013
A vacuolar carboxypeptidase mutant of Arabidopsis thaliana is degraded by the ERAD pathway independently of its N-glycan Yamamoto, Masaya; Kawanabe, Mitsuyoshi; Hayashi, Yoko Biochemical and Biophysical Research Communications, Vol. 393, Issue 3 https://doi.org/10.1016/j.bbrc.2010.02.001	journal	March 2010
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Clough, Steven J.; Bent, Andrew F. The Plant Journal, Vol. 16, Issue 6, p. 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x	journal	December 1998
ER network homeostasis is critical for plant endosome streaming and endocytosis Stefano, Giovanni; Renna, Luciana; Lai, YaShiuan Cell Discovery, Vol. 1, Issue 1 https://doi.org/10.1038/celldisc.2015.33	journal	November 2015
Non-invasive topology analysis of membrane proteins in the secretory pathway Brach, Thorsten; Soyk, Sebastian; Müller, Christopher The Plant Journal, Vol. 57, Issue 3 https://doi.org/10.1111/j.1365-313X.2008.03704.x	journal	February 2009
Imaging Dynamic Redox Changes in Mammalian Cells with Green Fluorescent Protein Indicators Dooley, Colette T.; Dore, Timothy M.; Hanson, George T. Journal of Biological Chemistry, Vol. 279, Issue 21 https://doi.org/10.1074/jbc.M312847200	journal	February 2004
Tripartite Management of Unfolded Proteins in the Endoplasmic Reticulum Mori, Kazutoshi Cell, Vol. 101, Issue 5 https://doi.org/10.1016/S0092-8674(00)80855-7	journal	May 2000
Endoplasmic Reticulum Protein Quality Control and Its Relationship to Environmental Stress Responses in Plants Liu, Jian-Xiang; Howell, Stephen H. The Plant Cell, Vol. 22, Issue 9 https://doi.org/10.1105/tpc.110.078154	journal	September 2010
An Endoplasmic Reticulum Stress Response in Arabidopsis Is Mediated by Proteolytic Processing and Nuclear Relocation of a Membrane-Associated Transcription Factor, bZIP28 Liu, Jian-Xiang; Srivastava, Renu; Che, Ping The Plant Cell, Vol. 19, Issue 12 https://doi.org/10.1105/tpc.106.050021	journal	December 2007
The Unfolded Protein Response: From Stress Pathway to Homeostatic Regulation Walter, P.; Ron, D. Science, Vol. 334, Issue 6059 https://doi.org/10.1126/science.1209038	journal	November 2011
A Rab1 GTPase Is Required for Transport between the Endoplasmic Reticulum and Golgi Apparatus and for Normal Golgi Movement in Plants Batoko, Henri; Zheng, Huan-Quan; Hawes, Chris The Plant Cell, Vol. 12, Issue 11 https://doi.org/10.1105/tpc.12.11.2201	journal	November 2000
Autophagy: process and function Mizushima, N. Genes & Development, Vol. 21, Issue 22 https://doi.org/10.1101/gad.1599207	journal	November 2007
Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis Deng, Y.; Humbert, S.; Liu, J. -X. Proceedings of the National Academy of Sciences, Vol. 108, Issue 17 https://doi.org/10.1073/pnas.1102117108	journal	April 2011
Jasmonate-Triggered Plant Immunity Campos, Marcelo L.; Kang, Jin-Ho; Howe, Gregg A. Journal of Chemical Ecology, Vol. 40, Issue 7 https://doi.org/10.1007/s10886-014-0468-3	journal	June 2014
The Transmembrane Kinase Ire1p Is a Site-Specific Endonuclease That Initiates mRNA Splicing in the Unfolded Protein Response Sidrauski, Carmela; Walter, Peter Cell, Vol. 90, Issue 6 https://doi.org/10.1016/S0092-8674(00)80369-4	journal	September 1997
Bacteria establish an aqueous living space in plants crucial for virulence Xin, Xiu-Fang; Nomura, Kinya; Aung, Kyaw Nature, Vol. 539, Issue 7630 https://doi.org/10.1038/nature20166	journal	November 2016
bZIP17 and bZIP60 Regulate the Expression of BiP3 and Other Salt Stress Responsive Genes in an UPR-Independent Manner in Arabidopsis thaliana : bZIP17 Henriquez-Valencia, Carlos; Moreno, Adrian A.; Sandoval-Ibañez, Omar Journal of Cellular Biochemistry, Vol. 116, Issue 8 https://doi.org/10.1002/jcb.25121	journal	June 2015
The UPR Branch IRE1-bZIP60 in Plants Plays an Essential Role in Viral Infection and Is Complementary to the Only UPR Pathway in Yeast Zhang, Lingrui; Chen, Hui; Brandizzi, Federica PLOS Genetics, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pgen.1005164	journal	April 2015
ERO1-L, a Human Protein That Favors Disulfide Bond Formation in the Endoplasmic Reticulum Cabibbo, Andrea; Pagani, Massimiliano; Fabbri, Marco Journal of Biological Chemistry, Vol. 275, Issue 7 https://doi.org/10.1074/jbc.275.7.4827	journal	February 2000
Messenger RNA targeting to endoplasmic reticulum stress signalling sites Aragón, Tomás; van Anken, Eelco; Pincus, David Nature, Vol. 457, Issue 7230 https://doi.org/10.1038/nature07641	journal	December 2008

Similar Records

An IRE1-proteasome system signalling cohort controls cell fate determination in unresolved proteotoxic stress of the plant endoplasmic reticulum

Journal Article · Thu Aug 10 00:00:00 EDT 2023 · Nature Plants (Online) · OSTI ID:1437094

Ko, Dae Kwan; Kim, Joo Yong; Thibault, Ethan A.; +1 more

Recovery from temporary endoplasmic reticulum stress in plants relies on the tissue-specific and largely independent roles of bZIP28 and bZIP60, as well as an antagonizing function of BAX-Inhibitor 1 upon the pro-adaptive signaling mediated by bZIP28

Journal Article · Fri Nov 10 00:00:00 EST 2017 · The Plant Journal · OSTI ID:1437094

Ruberti, Cristina; Lai, YaShiuan; Brandizzi, Federica

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

Journal Article · Sun Oct 16 00:00:00 EDT 2016 · The Plant Journal · OSTI ID:1437094

Meng, Zhe; Ruberti, Cristina; Gong, Zhizhong; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
salicylic acid
unfolded protein response
endoplasmic reticulum
NPR1

Title: Salicylic acid-independent role of NPR1 is required for protection from proteotoxic stress in the plant endoplasmic reticulum

Citation Formats

References (65)

Similar Records

Related Subjects