NADPH oxidase activity is required for ER stress survival in plants
Abstract
In all eukaryotes, the unfolded protein response (UPR) relieves endoplasmic reticulum (ER) stress, which is a potentially lethal condition caused by the accumulation of misfolded proteins in the ER. In mammalian and yeast cells, reactive oxygen species (ROS) generated during ER stress attenuate the UPR, negatively impacting cell survival. In plants, the relationship between the UPR and ROS is less clear. Although ROS develop during ER stress, the sources of ROS linked to ER stress responses and the physiological impact of ROS generation on the survival from proteotoxic stress are yet unknown. Here we show that in Arabidopsis thaliana the respiratory burst oxidase homologs, RBOHD and RBOHF, contribute to the production of ROS during ER stress. We also demonstrate that during ER stress RBOHD and RBOHF are necessary to properly mount the adaptive UPR and overcome temporary and chronic ER stress situations. Furthermore, these results ascribe a cytoprotective role to RBOH-generated ROS in the defense from proteotoxic stress in an essential organelle, and support a plant-specific feature of the UPR management among eukaryotes.
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Aeronautics and Space Administration (NASA); National Institute of General Medical Sciences; National Institutes of Health Training Program
- OSTI Identifier:
- 1671332
- Alternate Identifier(s):
- OSTI ID: 1478544
- Grant/Contract Number:
- FG02-91ER20021; NNX12AN71G; R01‐GM101038
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The Plant Journal
- Additional Journal Information:
- Journal Volume: 96; Journal Issue: 6; Journal ID: ISSN 0960-7412
- Publisher:
- Society for Experimental Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Unfolded protein response; ER stress; Arabidopsis thaliana; reactive oxygen species; RBOHD; RBOHF
Citation Formats
Angelos, Evan, and Brandizzi, Federica. NADPH oxidase activity is required for ER stress survival in plants. United States: N. p., 2018.
Web. doi:10.1111/tpj.14091.
Angelos, Evan, & Brandizzi, Federica. NADPH oxidase activity is required for ER stress survival in plants. United States. https://doi.org/10.1111/tpj.14091
Angelos, Evan, and Brandizzi, Federica. Sat .
"NADPH oxidase activity is required for ER stress survival in plants". United States. https://doi.org/10.1111/tpj.14091. https://www.osti.gov/servlets/purl/1671332.
@article{osti_1671332,
title = {NADPH oxidase activity is required for ER stress survival in plants},
author = {Angelos, Evan and Brandizzi, Federica},
abstractNote = {In all eukaryotes, the unfolded protein response (UPR) relieves endoplasmic reticulum (ER) stress, which is a potentially lethal condition caused by the accumulation of misfolded proteins in the ER. In mammalian and yeast cells, reactive oxygen species (ROS) generated during ER stress attenuate the UPR, negatively impacting cell survival. In plants, the relationship between the UPR and ROS is less clear. Although ROS develop during ER stress, the sources of ROS linked to ER stress responses and the physiological impact of ROS generation on the survival from proteotoxic stress are yet unknown. Here we show that in Arabidopsis thaliana the respiratory burst oxidase homologs, RBOHD and RBOHF, contribute to the production of ROS during ER stress. We also demonstrate that during ER stress RBOHD and RBOHF are necessary to properly mount the adaptive UPR and overcome temporary and chronic ER stress situations. Furthermore, these results ascribe a cytoprotective role to RBOH-generated ROS in the defense from proteotoxic stress in an essential organelle, and support a plant-specific feature of the UPR management among eukaryotes.},
doi = {10.1111/tpj.14091},
journal = {The Plant Journal},
number = 6,
volume = 96,
place = {United States},
year = {Sat Sep 15 00:00:00 EDT 2018},
month = {Sat Sep 15 00:00:00 EDT 2018}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 26 works
Citation information provided by
Web of Science
Web of Science
Figures / Tables:
Figure 1: NADPH oxidase dependent O2- is generated during ER Stress partially through RBOHD and RBOHF activity In situ detection and semi-quantification of superoxide in root tissues by staining with nitro-tetrazolium blue (NBT) A. WT or rbohd rbohf seedlings treated with 1.0 μg/ml Tm, 1.0 μg/ml TM + 2.5more »
All figures and tables
(6 total)
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Control of Plant Development by Reactive Oxygen Species: Figure 1.
journal, June 2006
- Gapper, Catherine; Dolan, Liam
- Plant Physiology, Vol. 141, Issue 2
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
Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling: Salt stress elicits ER stress response
journal, July 2007
- Liu, Jian-Xiang; Srivastava, Renu; Che, Ping
- The Plant Journal, Vol. 51, Issue 5
ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death
journal, April 2013
- Han, Jaeseok; Back, Sung Hoon; Hur, Junguk
- Nature Cell Biology, Vol. 15, Issue 5
Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase
journal, January 1999
- Harding, Heather P.; Zhang, Yuhong; Ron, David
- Nature, Vol. 397, Issue 6716
Interactions between Light and the Circadian Clock in the Regulation of CAT2 Expression in Arabidopsis
journal, March 1994
- Zhong, H. H.; Young, J. C.; Pease, E. A.
- Plant Physiology, Vol. 104, Issue 3
Stressed to death – mechanisms of ER stress-induced cell death
journal, January 2014
- Sovolyova, Natalia; Healy, Sandra; Samali, Afshin
- Biological Chemistry, Vol. 395, Issue 1
Salicylic acid-independent role of NPR1 is required for protection from proteotoxic stress in the plant endoplasmic reticulum
journal, May 2018
- Lai, Ya-Shiuan; Renna, Luciana; Yarema, John
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 22
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
Ero1 and redox homeostasis in the endoplasmic reticulum
journal, April 2008
- Sevier, Carolyn S.; Kaiser, Chris A.
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1783, Issue 4
Regulated Translation Initiation Controls Stress-Induced Gene Expression in Mammalian Cells
journal, November 2000
- Harding, Heather P.; Novoa, Isabel; Zhang, Yuhong
- Molecular Cell, Vol. 6, Issue 5
Phenotypic Analysis of Arabidopsis Mutants: Electrolyte Leakage after Freezing Stress
journal, January 2010
- Lee, B. -h.; Zhu, J. -K.
- Cold Spring Harbor Protocols, Vol. 2010, Issue 1
Specific Aquaporins Facilitate the Diffusion of Hydrogen Peroxide across Membranes
journal, November 2006
- Bienert, Gerd P.; Møller, Anders L. B.; Kristiansen, Kim A.
- Journal of Biological Chemistry, Vol. 282, Issue 2
Reactive Oxygen Species Activation of Plant Ca 2+ Channels. A Signaling Mechanism in Polar Growth, Hormone Transduction, Stress Signaling, and Hypothetically Mechanotransduction: Figure 1.
journal, June 2004
- Mori, Izumi C.; Schroeder, Julian I.
- Plant Physiology, Vol. 135, Issue 2
BINDING PROTEIN Is a Master Regulator of the Endoplasmic Reticulum Stress Sensor/Transducer bZIP28 in Arabidopsis
journal, April 2013
- Srivastava, Renu; Deng, Yan; Shah, Shweta
- The Plant Cell, Vol. 25, Issue 4
A Putative Arabidopsis Nucleoporin, AtNUP160, Is Critical for RNA Export and Required for Plant Tolerance to Cold Stress
journal, October 2006
- Dong, C. -H.; Hu, X.; Tang, W.
- Molecular and Cellular Biology, Vol. 26, Issue 24
Respiratory burst oxidases: the engines of ROS signaling
journal, December 2011
- Suzuki, Nobuhiro; Miller, Gad; Morales, Jorge
- Current Opinion in Plant Biology, Vol. 14, Issue 6
Genome-wide Association Study Reveals that the Aquaporin NIP1;1 Contributes to Variation in Hydrogen Peroxide Sensitivity in Arabidopsis thaliana
journal, August 2017
- Sadhukhan, Ayan; Kobayashi, Yuriko; Nakano, Yuki
- Molecular Plant, Vol. 10, Issue 8
AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis
journal, October 2011
- Chen, Yani; Brandizzi, Federica
- The Plant Journal, Vol. 69, Issue 2
ZINC FINGER OF ARABIDOPSIS THALIANA12 (ZAT12) Interacts with FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR (FIT) Linking Iron Deficiency and Oxidative Stress Responses
journal, November 2015
- Le, Cham Thi Tuyet; Brumbarova, Tzvetina; Ivanov, Rumen
- Plant Physiology, Vol. 170, Issue 1
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
Nrf2 Is a Direct PERK Substrate and Effector of PERK-Dependent Cell Survival
journal, September 2003
- Cullinan, S. B.; Zhang, D.; Hannink, M.
- Molecular and Cellular Biology, Vol. 23, Issue 20
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
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
NAD(P)H Oxidase Nox-4 Mediates 7-Ketocholesterol-Induced Endoplasmic Reticulum Stress and Apoptosis in Human Aortic Smooth Muscle Cells
journal, November 2004
- Pedruzzi, E.; Guichard, C.; Ollivier, V.
- Molecular and Cellular Biology, Vol. 24, Issue 24
An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants
journal, March 2005
- Iwata, Y.; Koizumi, N.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 14
Heterotrimeric G Proteins Serve as a Converging Point in Plant Defense Signaling Activated by Multiple Receptor-Like Kinases
journal, February 2013
- Liu, Jinman; Ding, Pingtao; Sun, Tongjun
- Plant Physiology, Vol. 161, Issue 4
Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response
journal, December 2001
- Torres, M. A.; Dangl, J. L.; Jones, J. D. G.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 1
Functional Interplay Between Arabidopsis NADPH Oxidases and Heterotrimeric G Protein
journal, June 2013
- Torres, Miguel Angel; Morales, Jorge; Sánchez-Rodríguez, Clara
- Molecular Plant-Microbe Interactions, Vol. 26, Issue 6
NADPH oxidase links endoplasmic reticulum stress, oxidative stress, and PKR activation to induce apoptosis
journal, December 2010
- Li, Gang; Scull, Christopher; Ozcan, Lale
- The Journal of Experimental Medicine, Vol. 207, Issue 13
Translation Attenuation through eIF2α Phosphorylation Prevents Oxidative Stress and Maintains the Differentiated State in β Cells
journal, July 2009
- Back, Sung Hoon; Scheuner, Donalyn; Han, Jaeseok
- Cell Metabolism, Vol. 10, Issue 1
IRE1/bZIP60-Mediated Unfolded Protein Response Plays Distinct Roles in Plant Immunity and Abiotic Stress Responses
journal, February 2012
- Moreno, Adrian A.; Mukhtar, M. Shahid; Blanco, Francisca
- PLoS ONE, Vol. 7, Issue 2
Ca2+ homeostasis and endoplasmic reticulum (ER) stress: An integrated view of calcium signaling
journal, April 2015
- Krebs, Joachim; Agellon, Luis B.; Michalak, Marek
- Biochemical and Biophysical Research Communications, Vol. 460, Issue 1
Cytosolic calcium, hydrogen peroxide and related gene expression and protein modulation in Arabidopsis thaliana cell cultures respond immediately to altered gravitation: parabolic flight data
journal, July 2013
- Hausmann, N.; Fengler, S.; Hennig, A.
- Plant Biology, Vol. 16
Cysteine Sulfenylation Directs IRE-1 to Activate the SKN-1/Nrf2 Antioxidant Response
journal, August 2016
- Hourihan, John M.; Moronetti Mazzeo, Lorenza E.; Fernández-Cárdenas, L. Paulette
- Molecular Cell, Vol. 63, Issue 4
Amplex UltraRed enhances the sensitivity of fluorimetric pyruvate detection
journal, August 2010
- Zhu, Aiping; Romero, Roberto; Petty, Howard R.
- Analytical Biochemistry, Vol. 403, Issue 1-2
Superoxide-responsive gene expression in Arabidopsis thaliana and Zea mays
journal, August 2017
- Xu, Junhuan; Tran, Thu; Padilla Marcia, Carmen S.
- Plant Physiology and Biochemistry, Vol. 117
Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD
journal, February 2016
- Liu, Yukun; He, Chengzhong
- Plant Cell Reports, Vol. 35, Issue 5
The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity
journal, January 2016
- Morales, Jorge; Kadota, Yasuhiro; Zipfel, Cyril
- Journal of Experimental Botany, Vol. 67, Issue 6
Reactive oxygen species generation and signaling in plants
journal, December 2012
- Tripathy, Baishnab Charan; Oelmüller, Ralf
- Plant Signaling & Behavior, Vol. 7, Issue 12
Pathogen-induced, NADPH oxidase–derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana
journal, September 2005
- Torres, Miguel Angel; Jones, Jonathan D. G.; Dangl, Jeffery L.
- Nature Genetics, Vol. 37, Issue 10
Oxidative protein folding in eukaryotes: Figure 1.: mechanisms and consequences
journal, February 2004
- Tu, Benjamin P.; Weissman, Jonathan S.
- The Journal of Cell Biology, Vol. 164, Issue 3
Oxidative Homeostasis Regulates the Response to Reductive Endoplasmic Reticulum Stress through Translation Control
journal, July 2016
- Maity, Shuvadeep; Rajkumar, Asher; Matai, Latika
- Cell Reports, Vol. 16, Issue 3
Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases
journal, April 2007
- Dunand, Christophe; Crèvecoeur, Michèle; Penel, Claude
- New Phytologist, Vol. 174, Issue 2
CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum
journal, December 2004
- Marciniak, S. J.
- Genes & Development, Vol. 18, Issue 24
ECA1 complements yeast mutants defective in Ca2+ pumps and encodes an endoplasmic reticulum-type Ca2+-ATPase in Arabidopsis thaliana
journal, August 1997
- Liang, F.; Cunningham, K. W.; Harper, J. F.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 16
The Roles of Mitochondrial Reactive Oxygen Species in Cellular Signaling and Stress Response in Plants
journal, March 2016
- Huang, Shaobai; Van Aken, Olivier; Schwarzländer, Markus
- Plant Physiology, Vol. 171, Issue 3
Endoplasmic reticulum stress triggers ROS signalling, changes the redox state, and regulates the antioxidant defence of Arabidopsis thaliana
journal, February 2014
- Ozgur, Rengin; Turkan, Ismail; Uzilday, Baris
- Journal of Experimental Botany, Vol. 65, Issue 5
Synergistic Activation of the Arabidopsis NADPH Oxidase AtrbohD by Ca 2+ and Phosphorylation
journal, January 2008
- Ogasawara, Yoko; Kaya, Hidetaka; Hiraoka, Goro
- Journal of Biological Chemistry, Vol. 283, Issue 14
Maintaining the factory: the roles of the unfolded protein response in cellular homeostasis in plants
journal, March 2017
- Angelos, Evan; Ruberti, Cristina; Kim, Sang-Jin
- The Plant Journal, Vol. 90, Issue 4
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, December 2017
- Ruberti, Cristina; Lai, YaShiuan; Brandizzi, Federica
- The Plant Journal, Vol. 93, Issue 1
The effects of induced production of reactive oxygen species in organelles on endoplasmic reticulum stress and on the unfolded protein response in arabidopsis
journal, June 2015
- Ozgur, Rengin; Uzilday, Baris; Sekmen, A. Hediye
- Annals of Botany, Vol. 116, Issue 4
Identification and functional study of the endoplasmic reticulum stress sensor IRE 1 in Chlamydomonas reinhardtii
journal, March 2018
- Yamaoka, Yasuyo; Choi, Bae Young; Kim, Hanul
- The Plant Journal, Vol. 94, Issue 1
ER Stress Regulation of ATF6 Localization by Dissociation of BiP/GRP78 Binding and Unmasking of Golgi Localization Signals
journal, July 2002
- Shen, Jingshi; Chen, Xi; Hendershot, Linda
- Developmental Cell, Vol. 3, Issue 1
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
Signal integration in the endoplasmic reticulum unfolded protein response
journal, July 2007
- Ron, David; Walter, Peter
- Nature Reviews Molecular Cell Biology, Vol. 8, Issue 7
NADPH oxidase links endoplasmic reticulum stress, oxidative stress, and PKR activation to induce apoptosis
journal, December 2010
- Li, Gang; Scull, Christopher; Ozcan, Lale
- The Journal of Cell Biology, Vol. 191, Issue 6
Why are literature data for H2O2 contents so variable? A discussion of potential difficulties in the quantitative assay of leaf extracts
journal, February 2008
- Queval, G.; Hager, J.; Gakiere, B.
- Journal of Experimental Botany, Vol. 59, Issue 2
Quantification of hydrogen peroxide in plant tissues using Amplex Red
journal, October 2016
- Chakraborty, Sourav; Hill, Amy L.; Shirsekar, Gautam
- Methods, Vol. 109
Increase in catalase-3 activity as a response to use of alternative catabolic substrates during sucrose starvation
journal, April 2010
- Contento, Anthony L.; Bassham, Diane C.
- Plant Physiology and Biochemistry, Vol. 48, Issue 4
An Endoplasmic Reticulum Stress Response in Arabidopsis Is Mediated by Proteolytic Processing and Nuclear Relocation of a Membrane-Associated Transcription Factor, bZIP28
journal, December 2007
- Liu, Jian-Xiang; Srivastava, Renu; Che, Ping
- The Plant Cell, Vol. 19, Issue 12
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
Protein folding in the cell
journal, January 1992
- Gething, Mary-Jane; Sambrook, Joseph
- Nature, Vol. 355, Issue 6355
Endoplasmic Reticulum Stress and Oxidative Stress: A Vicious Cycle or a Double-Edged Sword?
journal, December 2007
- Malhotra, Jyoti D.; Kaufman, Randal J.
- Antioxidants & Redox Signaling, Vol. 9, Issue 12
Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response
text, January 2002
- Miguel, Torres,; Jeffery, Dangl,; Jonathan, Jones,
- The University of North Carolina at Chapel Hill University Libraries
The Plant NADPH Oxidase RBOHD Mediates Rapid Systemic Signaling in Response to Diverse Stimuli
journal, August 2009
- Miller, G.; Schlauch, K.; Tam, R.
- Science Signaling, Vol. 2, Issue 84
The Roles of ROS and ABA in Systemic Acquired Acclimation
journal, January 2015
- Mittler, Ron; Blumwald, Eduardo
- The Plant Cell, Vol. 27, Issue 1
The acute transcriptional responses to dietary methionine restriction are triggered by inhibition of ternary complex formation and linked to Erk1/2, mTOR, and ATF4
journal, February 2021
- Stone, Kirsten P.; Ghosh, Sujoy; Kovalik, Jean Paul
- Scientific Reports, Vol. 11, Issue 1
Interplay between the unfolded protein response and reactive oxygen species: a dynamic duo
journal, February 2018
- Ozgur, Rengin; Uzilday, Baris; Iwata, Yuji
- Journal of Experimental Botany, Vol. 69, Issue 14
ERO1: A protein disulfide oxidase and H2O2 producer
journal, June 2015
- Zito, Ester
- Free Radical Biology and Medicine, Vol. 83
Works referencing / citing this record:
Genomics analysis of genes encoding respiratory burst oxidase homologs (RBOHs) in jatropha and the comparison with castor bean
journal, January 2019
- Zhao, Yongguo; Zou, Zhi
- PeerJ, Vol. 7
Communications Between the Endoplasmic Reticulum and Other Organelles During Abiotic Stress Response in Plants
journal, June 2019
- Liu, Linchuan; Li, Jianming
- Frontiers in Plant Science, Vol. 10
Maize Sep15 ‐like functions in endoplasmic reticulum and reactive oxygen species homeostasis to promote salt and osmotic stress resistance
journal, January 2019
- Zhu, Jiantang; Wang, Guangling; Li, Cuiling
- Plant, Cell & Environment, Vol. 42, Issue 5
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
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
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
Communications Between the Endoplasmic Reticulum and Other Organelles During Abiotic Stress Response in Plants
journal, June 2019
- Liu, Linchuan; Li, Jianming
- Frontiers in Plant Science, Vol. 10
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
Figures / Tables found in this record:
Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.