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; Verchot, Jeanmarie; Wang, Aiming

doi:10.1371/journal.pgen.1005164

Title: The UPR Branch IRE1-bZIP60 in Plants Plays an Essential Role in Viral Infection and Is Complementary to the Only UPR Pathway in Yeast

Journal Article · Wed Apr 15 00:00:00 EDT 2015 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1005164· OSTI ID:1904889

Zhang, Lingrui ^[1]; Chen, Hui ^[2]; Brandizzi, Federica ^[3]; Verchot, Jeanmarie ^[4]; Wang, Aiming ^[2]

Agriculture and Agri-Food Canada, London, ON (Canada). Southern Crop Protection and Food Research
Agriculture and Agri-Food Canada, London, ON (Canada). Southern Crop Protection and Food Research
Michigan State University, East Lansing, MI (United States).
Oklahoma State University, Stillwater, OK (United States)

The unfolded protein response (UPR) signaling network encompasses two pathways in plants, one mediated by inositol-requiring protein-1 (IRE1)-bZIP60 mRNA and the other by site-1/site-2 proteases (S1P/S2P)-bZIP17/bZIP28. As the major sensor of UPR in eukaryotes, IRE1, in response to endoplasmic reticulum (ER) stress, catalyzes the unconventional splicing of HAC1 in yeast, bZIP60 in plants and XBP1 in metazoans. Recent studies suggest that IRE1p and HAC1 mRNA, the only UPR pathway found in yeast, evolves as a cognate system responsible for the robust UPR induction. However, the functional connectivity of IRE1 and its splicing target in multicellular eukaryotes as well as the degree of conservation of IRE1 downstream signaling effectors across eukaryotes remains to be established. Here, we report that IRE1 and its substrate bZIP60 function as a strictly cognate enzymesubstrate pair to control viral pathogenesis in plants. Moreover, we show that the S1P/ S2P-bZIP17/bZIP28 pathway, the other known branch of UPR in plants, does not play a detectable role in virus infection, demonstrating the distinct function of the IRE1-bZIP60 pathway in plants. Furthermore, we provide evidence that bZIP60 and HAC1, products of the enzyme-substrate duet, rather than IRE1, are functionally replaceable to cope with ER stress in yeast. Taken together, we conclude that the downstream signaling of the IRE1- mediated splicing is evolutionarily conserved in yeast and plants, and that the IRE1-bZIP60 UPR pathway not only confers overlapping functions with the other UPR branch in fundamental biology but also may exert a unique role in certain biological processes such as virus-plant interactions.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Natural Sciences and Engineering Research Council of Canada (NSERC); National Institutes of Health (NIH); US Department of Agriculture (USDA)

Grant/Contract Number:: SC0014664; R01 GM101038; 2014-67014-21715

OSTI ID:: 1904889

Journal Information:: PLoS Genetics, Vol. 11, Issue 4; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (70)

Endoplasmic Reticulum (ER) Stress Response and Its Physiological Roles in Plants Deng, Yan; Srivastava, Renu; Howell, Stephen International Journal of Molecular Sciences, Vol. 14, Issue 4 https://doi.org/10.3390/ijms14048188	journal	April 2013
Identification of an Arabidopsis transmembrane bZIP transcription factor involved in the endoplasmic reticulum stress response Tajima, Hiromi; Iwata, Yuji; Iwano, Megumi Biochemical and Biophysical Research Communications, Vol. 374, Issue 2 https://doi.org/10.1016/j.bbrc.2008.07.021	journal	September 2008
Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana Lu, Dong-Ping; Christopher, David A. Molecular Genetics and Genomics, Vol. 280, Issue 3 https://doi.org/10.1007/s00438-008-0356-z	journal	June 2008
Identification of stress-tolerance-related transcription-factor genes via mini-scale Full-length cDNA Over-eXpressor (FOX) gene hunting system Fujita, Miki; Mizukado, Saho; Fujita, Yasunari Biochemical and Biophysical Research Communications, Vol. 364, Issue 2 https://doi.org/10.1016/j.bbrc.2007.09.124	journal	December 2007
Structure of the Dual Enzyme Ire1 Reveals the Basis for Catalysis and Regulation in Nonconventional RNA Splicing Lee, Kenneth P. K.; Dey, Madhusudan; Neculai, Dante Cell, Vol. 132, Issue 1 https://doi.org/10.1016/j.cell.2007.10.057	journal	January 2008
IRE1: ER stress sensor and cell fate executor Chen, Yani; Brandizzi, Federica Trends in Cell Biology, Vol. 23, Issue 11 https://doi.org/10.1016/j.tcb.2013.06.005	journal	November 2013
The 8ab protein of SARS-CoV is a luminal ER membrane-associated protein and induces the activation of ATF6 Sung, Shu-Chiun; Chao, Che-Yi; Jeng, King-Song Virology, Vol. 387, Issue 2 https://doi.org/10.1016/j.virol.2009.02.021	journal	May 2009
Analysis of potato virus X replicase and TGBp3 subcellular locations Bamunusinghe, Devinka; Hemenway, Cynthia L.; Nelson, Richard. S. Virology, Vol. 393, Issue 2 https://doi.org/10.1016/j.virol.2009.08.002	journal	October 2009
Functional and Genomic Analyses Reveal an Essential Coordination between the Unfolded Protein Response and ER-Associated Degradation Travers, Kevin J.; Patil, Christopher K.; Wodicka, Lisa Cell, Vol. 101, Issue 3 https://doi.org/10.1016/s0092-8674(00)80835-1	journal	April 2000
Block of HAC1 mRNA Translation by Long-Range Base Pairing Is Released by Cytoplasmic Splicing upon Induction of the Unfolded Protein Response Rüegsegger, Ursula; Leber, Jess H.; Walter, Peter Cell, Vol. 107, Issue 1 https://doi.org/10.1016/s0092-8674(01)00505-0	journal	October 2001
Characterization of two homologs of Ire1p, a kinase/endoribonuclease in yeast, in Arabidopsis thaliana Noh, S. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1575, Issue 1-3 https://doi.org/10.1016/s0167-4781(02)00237-3	journal	May 2002
Paneth cells as a site of origin for intestinal inflammation Adolph, Timon E.; Tomczak, Michal F.; Niederreiter, Lukas Nature, Vol. 503, Issue 7475 https://doi.org/10.1038/nature12599	journal	October 2013
The unfolded protein response: controlling cell fate decisions under ER stress and beyond Hetz, Claudio Nature Reviews Molecular Cell Biology, Vol. 13, Issue 2 https://doi.org/10.1038/nrm3270	journal	January 2012
The biological meaning of the UPR Hetz, Claudio Nature Reviews Molecular Cell Biology, Vol. 14, Issue 7 https://doi.org/10.1038/nrm3606	journal	June 2013
An elegant UPR discovery Taylor, Rebecca C. Nature Reviews Molecular Cell Biology, Vol. 19, Issue 9 https://doi.org/10.1038/s41580-018-0043-9	journal	July 2018
Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor Nagashima, Yukihiro; Mishiba, Kei-ichiro; Suzuki, Eiji Scientific Reports, Vol. 1, Issue 1 https://doi.org/10.1038/srep00029	journal	July 2011
Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants Whitham, Steven A.; Quan, Sheng; Chang, Hur-Song The Plant Journal, Vol. 33, Issue 2 https://doi.org/10.1046/j.1365-313x.2003.01625.x	journal	January 2003
mRNA splicing-mediated C-terminal replacement of transcription factor Hac1p is required for efficient activation of the unfolded protein response Mori, Kazutoshi; Ogawa, Naoki; Kawahara, Tetsushi Proceedings of the National Academy of Sciences, Vol. 97, Issue 9 https://doi.org/10.1073/pnas.050010197	journal	April 2000
A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana Gao, H.; Brandizzi, F.; Benning, C. Proceedings of the National Academy of Sciences, Vol. 105, Issue 42 https://doi.org/10.1073/pnas.0808463105	journal	October 2008
In vitro assembly of the Tomato bushy stunt virus replicase requires the host Heat shock protein 70 Pogany, Judit; Stork, Jozsef; Li, Zhenghe Proceedings of the National Academy of Sciences, Vol. 105, Issue 50 https://doi.org/10.1073/pnas.0810851105	journal	December 2008
BiP-mediated polar nuclei fusion is essential for the regulation of endosperm nuclei proliferation in Arabidopsis thaliana Maruyama, D.; Endo, T.; Nishikawa, S. -i. Proceedings of the National Academy of Sciences, Vol. 107, Issue 4 https://doi.org/10.1073/pnas.0905795107	journal	January 2010
Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering Li, H.; Korennykh, A. V.; Behrman, S. L. Proceedings of the National Academy of Sciences, Vol. 107, Issue 37 https://doi.org/10.1073/pnas.1010580107	journal	August 2010
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
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
Influenza A Viral Replication Is Blocked by Inhibition of the Inositol-requiring Enzyme 1 (IRE1) Stress Pathway Hassan, Ihab H.; Zhang, Michael S.; Powers, Linda S. Journal of Biological Chemistry, Vol. 287, Issue 7 https://doi.org/10.1074/jbc.m111.284695	journal	February 2012
Hepatitis C Virus Suppresses the IRE1-XBP1 Pathway of the Unfolded Protein Response Tardif, Keith D.; Mori, Kazutoshi; Kaufman, Randal J. Journal of Biological Chemistry, Vol. 279, Issue 17 https://doi.org/10.1074/jbc.m312144200	journal	April 2004
pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response Yoshida, Hiderou; Oku, Masaya; Suzuki, Mie The Journal of Cell Biology, Vol. 172, Issue 4 https://doi.org/10.1083/jcb.200508145	journal	February 2006
SCF^Cdc4-mediated Degradation of the Hac1p Transcription Factor Regulates the Unfolded Protein Response inSaccharomyces cerevisiae Pal, Bhupinder; Chan, Nickie C.; Helfenbaum, Leon Molecular Biology of the Cell, Vol. 18, Issue 2 https://doi.org/10.1091/mbc.e06-04-0304	journal	February 2007
NucPred Predicting nuclear localization of proteins Brameier, M.; Krings, A.; MacCallum, R. M. Bioinformatics, Vol. 23, Issue 9 https://doi.org/10.1093/bioinformatics/btm066	journal	March 2007
Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway Gonzalez, T. N. The EMBO Journal, Vol. 18, Issue 11 https://doi.org/10.1093/emboj/18.11.3119	journal	June 1999
Mfold web server for nucleic acid folding and hybridization prediction Zuker, M. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg595	journal	July 2003
Identification of a consensus element recognized and cleaved by IRE1α Oikawa, Daisuke; Tokuda, Mio; Hosoda, Akira Nucleic Acids Research, Vol. 38, Issue 18 https://doi.org/10.1093/nar/gkq452	journal	May 2010
Spatial Analysis of Arabidopsis thaliana Gene Expression in Response to Turnip mosaic virus Infection Yang, Chunling; Guo, Rong; Jie, Fei Molecular Plant-Microbe Interactions®, Vol. 20, Issue 4 https://doi.org/10.1094/mpmi-20-4-0358	journal	April 2007
Transcriptional Changes and Oxidative Stress Associated with the Synergistic Interaction Between Potato virus X and Potato virus Y and Their Relationship with Symptom Expression García-Marcos, Alberto; Pacheco, Remedios; Martiáñez, Justo Molecular Plant-Microbe Interactions®, Vol. 22, Issue 11 https://doi.org/10.1094/mpmi-22-11-1431	journal	November 2009
Molecular Characterization of Two Arabidopsis Ire1 Homologs, Endoplasmic Reticulum-Located Transmembrane Protein Kinases Koizumi, Nozomu; Martinez, Immaculada M.; Kimata, Yukio Plant Physiology, Vol. 127, Issue 3 https://doi.org/10.1104/pp.010636	journal	November 2001
Virus Induction of Heat Shock Protein 70 Reflects a General Response to Protein Accumulation in the Plant Cytosol Aparicio, Frederic; Thomas, Carole L.; Lederer, Carsten Plant Physiology, Vol. 138, Issue 1 https://doi.org/10.1104/pp.104.058958	journal	May 2005
Separation of Arabidopsis Pollen Tetrads Is Regulated by QUARTET1 , a Pectin Methylesterase Gene Francis, Kirk E.; Lam, Sandy Y.; Copenhaver, Gregory P. Plant Physiology, Vol. 142, Issue 3 https://doi.org/10.1104/pp.106.085274	journal	September 2006
The Unfolded Protein Response Is Triggered by a Plant Viral Movement Protein Ye, Changming; Dickman, Martin B.; Whitham, Steven A. Plant Physiology, Vol. 156, Issue 2 https://doi.org/10.1104/pp.111.174110	journal	April 2011
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
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
The Cytosolic Protein Response as a Subcomponent of the Wider Heat Shock Response in Arabidopsis Sugio, Akiko; Dreos, René; Aparicio, Frederic The Plant Cell, Vol. 21, Issue 2 https://doi.org/10.1105/tpc.108.062596	journal	February 2009
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
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
TGBp3 triggers the unfolded protein response and SKP1-dependent programmed cell death Ye, Chang-Ming; Chen, Shaorong; Payton, Mark Molecular Plant Pathology, Vol. 14, Issue 3 https://doi.org/10.1111/mpp.12000	journal	March 2013
Proapoptotic BAX and BAK Modulate the Unfolded Protein Response by a Direct Interaction with IRE1 Hetz, C. Science, Vol. 312, Issue 5773 https://doi.org/10.1126/science.1123480	journal	April 2006
IRE1 Signaling Affects Cell Fate During the Unfolded Protein Response Lin, J. H.; Li, H.; Yasumura, D. Science, Vol. 318, Issue 5852 https://doi.org/10.1126/science.1146361	journal	November 2007
Unfolded Proteins Are Ire1-Activating Ligands That Directly Induce the Unfolded Protein Response Gardner, B. M.; Walter, P. Science, Vol. 333, Issue 6051 https://doi.org/10.1126/science.1209126	journal	August 2011
IRE1α Cleaves Select microRNAs During ER Stress to Derepress Translation of Proapoptotic Caspase-2 Upton, John-Paul; Wang, Likun; Han, Dan Science, Vol. 338, Issue 6108 https://doi.org/10.1126/science.1226191	journal	November 2012
Coupling of Stress in the ER to Activation of JNK Protein Kinases by Transmembrane Protein Kinase IRE1 Urano, F. Science, Vol. 287, Issue 5453 https://doi.org/10.1126/science.287.5453.664	journal	January 2000
Effects of Inactivation and Constitutive Expression of the Unfolded- Protein Response Pathway on Protein Production in the Yeast Saccharomyces cerevisiae Valkonen, M.; Penttila, M.; Saloheimo, M. Applied and Environmental Microbiology, Vol. 69, Issue 4 https://doi.org/10.1128/aem.69.4.2065-2072.2003	journal	April 2003
Coronavirus Infection Modulates the Unfolded Protein Response and Mediates Sustained Translational Repression Bechill, John; Chen, Zhongbin; Brewer, Joseph W. Journal of Virology, Vol. 82, Issue 9 https://doi.org/10.1128/jvi.00017-08	journal	May 2008
Flux of the paramyxovirus hemagglutinin-neuraminidase glycoprotein through the endoplasmic reticulum activates transcription of the GRP78-BiP gene Watowich, S. S.; Morimoto, R. I.; Lamb, R. A. Journal of Virology, Vol. 65, Issue 7 https://doi.org/10.1128/jvi.65.7.3590-3597.1991	journal	July 1991
African Swine Fever Virus Inhibits Induction of the Stress-Induced Proapoptotic Transcription Factor CHOP/GADD153 Netherton, Christopher L.; Parsley, James C.; Wileman, Thomas Journal of Virology, Vol. 78, Issue 19 https://doi.org/10.1128/jvi.78.19.10825-10828.2004	journal	October 2004
Proteomics Analysis of the Tombusvirus Replicase: Hsp70 Molecular Chaperone Is Associated with the Replicase and Enhances Viral RNA Replication Serva, Saulius; Nagy, Peter D. Journal of Virology, Vol. 80, Issue 5 https://doi.org/10.1128/jvi.80.5.2162-2169.2006	journal	March 2006
Classification of Human B-ZIP Proteins Based on Dimerization Properties Vinson, Charles; Myakishev, Max; Acharya, Asha Molecular and Cellular Biology, Vol. 22, Issue 18 https://doi.org/10.1128/mcb.22.18.6321-6335.2002	journal	September 2002
Endoplasmic Reticulum Stress Responses in Plants Howell, Stephen H. Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120053	journal	April 2013
The Unfolded Protein Response: Integrating Stress Signals Through the Stress Sensor IRE1α Hetz, Claudio; Martinon, Fabio; Rodriguez, Diego Physiological Reviews, Vol. 91, Issue 4 https://doi.org/10.1152/physrev.00001.2011	journal	October 2011
Inhibition of Akt Potentiates 2-DG–Induced Apoptosis via Downregulation of UPR in Acute Lymphoblastic Leukemia DeSalvo, Joanna; Kuznetsov, Jeffim N.; Du, Jianfeng Molecular Cancer Research, Vol. 10, Issue 7 https://doi.org/10.1158/1541-7786.mcr-12-0125	journal	July 2012
Unconventional splicing of XBP1 mRNA occurs in the cytoplasm during the mammalian unfolded protein response Uemura, Aya; Oku, Masaya; Mori, Kazutoshi Journal of Cell Science, Vol. 122, Issue 16 https://doi.org/10.1242/jcs.040584	journal	August 2009
BiP Binding to the ER-Stress Sensor Ire1 Tunes the Homeostatic Behavior of the Unfolded Protein Response Pincus, David; Chevalier, Michael W.; Aragón, Tomás PLoS Biology, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pbio.1000415	journal	July 2010
Genetic Interactions Due to Constitutive and Inducible Gene Regulation Mediated by the Unfolded Protein Response in C. elegans Shen, Xiaohua; Ellis, Ronald E.; Sakaki, Kenjiro PLoS Genetics, Vol. 1, Issue 3 https://doi.org/10.1371/journal.pgen.0010037	journal	September 2005
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
Alteration of the bZIP60/IRE1 Pathway Affects Plant Response to ER Stress in Arabidopsis thaliana Humbert, Sabrina; Zhong, Sihui; Deng, Yan PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0039023	journal	June 2012
Formation of Complexes at Plasmodesmata for Potyvirus Intercellular Movement Is Mediated by the Viral Protein P3N-PIPO Wei, Taiyun; Zhang, Changwei; Hong, Jian PLoS Pathogens, Vol. 6, Issue 6 https://doi.org/10.1371/journal.ppat.1000962	journal	June 2010
A new paradigm: innate immune sensing of viruses via the unfolded protein response Smith, Judith A. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00222	journal	May 2014
Virus-induced ER stress and the unfolded protein response Zhang, Lingrui; Wang, Aiming Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00293	journal	January 2012
When supply does not meet demand-ER stress and plant programmed cell death Williams, Brett; Verchot, Jeanmarie; Dickman, Martin B. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00211	journal	June 2014
The unfolded protein response in fission yeast modulates stability of select mRNAs to maintain protein homeostasis Kimmig, Philipp; Diaz, Marcy; Zheng, Jiashun eLife, Vol. 1 https://doi.org/10.7554/elife.00048	journal	October 2012
New twists in the unfolded protein response Cross, Benedict C. S.; Ron, David eLife, Vol. 1 https://doi.org/10.7554/elife.00243	journal	October 2012
Redox signaling via the molecular chaperone BiP protects cells against endoplasmic reticulum-derived oxidative stress Wang, Jie; Pareja, Kristeen A.; Kaiser, Chris A. eLife, Vol. 3 https://doi.org/10.7554/elife.03496	journal	July 2014

Cited By (15)

External and internal triggers of cell death in yeast Falcone, Claudio; Mazzoni, Cristina Cellular and Molecular Life Sciences, Vol. 73, Issue 11-12 https://doi.org/10.1007/s00018-016-2197-y	journal	April 2016
Divergence and Conservation of the Major UPR Branch IRE1-bZIP Signaling Pathway across Eukaryotes Zhang, Lingrui; Zhang, Changwei; Wang, Aiming Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep27362	journal	June 2016
Recruitment of Arabidopsis RNA Helicase AtRH9 to the Viral Replication Complex by Viral Replicase to Promote Turnip Mosaic Virus Replication Li, Yinzi; Xiong, Ruyi; Bernards, Mark Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep30297	journal	July 2016
The multifunctional protein CI of potyviruses plays interlinked and distinct roles in viral genome replication and intercellular movement Deng, Ping; Wu, Zujian; Wang, Aiming Virology Journal, Vol. 12, Issue 1 https://doi.org/10.1186/s12985-015-0369-2	journal	September 2015
Recessive Resistance to Plant Viruses: Potential Resistance Genes Beyond Translation Initiation Factors Hashimoto, Masayoshi; Neriya, Yutaro; Yamaji, Yasuyuki Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01695	journal	October 2016
An improved high-throughput screening assay for tunicamycin sensitivity in Arabidopsis seedlings McCormack, Maggie E.; Liu, Xiaoyu; Jordan, Melissa R. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00663	journal	August 2015
The Unfolded Protein Response Supports Plant Development and Defense as well as Responses to Abiotic Stress Bao, Yan; Howell, Stephen H. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00344	journal	March 2017
Hop/Sti1 – A Two-Faced Cochaperone Involved in Pattern Recognition Receptor Maturation and Viral Infection Lamm, Christian E.; Kraner, Max. E.; Hofmann, Jörg Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01754	journal	October 2017
Activation of the Transducers of Unfolded Protein Response in Plants Nawkar, Ganesh M.; Lee, Eun Seon; Shelake, Rahul M. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00214	journal	February 2018
Exploring the Diversity of Mechanisms Associated With Plant Tolerance to Virus Infection Paudel, Dinesh Babu; Sanfaçon, Hélène Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01575	journal	November 2018
Endoplasmic Reticulum Plays a Critical Role in Integrating Signals Generated by Both Biotic and Abiotic Stress in Plants Park, Chang-Jin; Park, Jeong Mee Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00399	journal	April 2019
ER-Phagy and ER Stress Response (ERSR) in Plants Zeng, Yonglun; Li, Baiying; Zhang, Wenxin Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01192	journal	September 2019
Endoplasmic Reticulum Stress Signaling in Plant Immunity—At the Crossroad of Life and Death Kørner, Camilla; Du, Xinran; Vollmer, Marie International Journal of Molecular Sciences, Vol. 16, Issue 11 https://doi.org/10.3390/ijms161125964	journal	November 2015
The Multifaceted Roles of Plant Hormone Salicylic Acid in Endoplasmic Reticulum Stress and Unfolded Protein Response Poór, Péter; Czékus, Zalán; Tari, Irma International Journal of Molecular Sciences, Vol. 20, Issue 23 https://doi.org/10.3390/ijms20235842	journal	November 2019
Susceptibility Genes to Plant Viruses Garcia-Ruiz, Hernan Viruses, Vol. 10, Issue 9 https://doi.org/10.3390/v10090484	journal	September 2018

Similar Records

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:1904889

Ruberti, Cristina; Lai, YaShiuan; Brandizzi, Federica

Genome-scale approaches for discovering novel nonconventional splicing substrates of the Ire1 nuclease

Journal Article · Wed Dec 22 00:00:00 EST 2004 · GenomeBiology.com · OSTI ID:1904889

Niwa, Maho; Patil, Christopher K.; DeRisi, Joe; +1 more

Flavonol Activation Defines an Unanticipated Ligand-Binding Site in the Kinase-RNase Domain of IRE1

Journal Article · Wed Aug 18 00:00:00 EDT 2010 · Mol. Cell · OSTI ID:1904889

Wiseman, R Luke; Zhang, Yuhong; Lee, Kenneth P.K.; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
yeast
RNA splicing
Arabidopsis thaliana
leaves
phenotypes
basic leucine zipper domains
messenger RNA
fluorescence resonance energy transfer

Title: The UPR Branch IRE1-bZIP60 in Plants Plays an Essential Role in Viral Infection and Is Complementary to the Only UPR Pathway in Yeast

Citation Formats

References (70)

Cited By (15)

Similar Records

Related Subjects