Systemic signaling contributes to the unfolded protein response of the plant endoplasmic reticulum

Lai, Ya-Shiuan; Stefano, Giovanni; Zemelis-Durfee, Starla; Ruberti, Cristina; Gibbons, Lizzie; Brandizzi, Federica

doi:10.1038/s41467-018-06289-9

Title: Systemic signaling contributes to the unfolded protein response of the plant endoplasmic reticulum

Journal Article · Tue Sep 25 00:00:00 EDT 2018 · Nature Communications

DOI:https://doi.org/10.1038/s41467-018-06289-9· OSTI ID:1619789

Lai, Ya-Shiuan; Stefano, Giovanni; Zemelis-Durfee, Starla; Ruberti, Cristina; Gibbons, Lizzie; Brandizzi, Federica

Abstract The unfolded protein response (UPR) of the endoplasmic reticulum constitutes a conserved and essential cytoprotective pathway designed to survive biotic and abiotic stresses that alter the proteostasis of the endoplasmic reticulum. The UPR is typically considered cell-autonomous and it is yet unclear whether it can also act systemically through non-cell autonomous signaling. We have addressed this question using a genetic approach coupled with micro-grafting and a suite of molecular reporters in the model plant species Arabidopsis thaliana . We show that the UPR has a non-cell autonomous component, and we demonstrate that this is partially mediated by the intercellular movement of the UPR transcription factor bZIP60 facilitating systemic UPR signaling. Therefore, in multicellular eukaryotes such as plants, non-cell autonomous UPR signaling relies on the systemic movement of at least a UPR transcriptional modulator.

View Journal Article

Cite

Export

Save

Research Organization:: Univ. of Wisconsin, Madison, WI (United States); Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: FC02-07ER64494; FG02-91ER20021

OSTI ID:: 1619789

Alternate ID(s):: OSTI ID: 1511712

Journal Information:: Nature Communications, Journal Name: Nature Communications Vol. 9 Journal Issue: 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

Citation Metrics:

Cited by: 16 works

Citation information provided by
Web of Science

References (49)

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
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
Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants Song, Ze-Ting; Sun, Le; Lu, Sun-Jie Proceedings of the National Academy of Sciences, Vol. 112, Issue 9 https://doi.org/10.1073/pnas.1419703112	journal	February 2015
Identification of a root-specific glycosyltransferase from Arabidopsis and characterization of its promoter Vijaybhaskar, Virupapuram; Subbiah, Veeraputhiran; Kaur, Jagreet Journal of Biosciences, Vol. 33, Issue 2 https://doi.org/10.1007/s12038-008-0036-5	journal	June 2008
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 Proceedings of the National Academy of Sciences, Vol. 115, Issue 22 https://doi.org/10.1073/pnas.1802254115	journal	May 2018
A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns Brady, S. M.; Orlando, D. A.; Lee, J. -Y. Science, Vol. 318, Issue 5851 https://doi.org/10.1126/science.1146265	journal	November 2007
Dual targeting of a virus movement protein to ER and plasma membrane subdomains is essential for plasmodesmata localization Ishikawa, Kazuya; Hashimoto, Masayoshi; Yusa, Akira PLOS Pathogens, Vol. 13, Issue 6 https://doi.org/10.1371/journal.ppat.1006463	journal	June 2017
XBP-1 Is a Cell-Nonautonomous Regulator of Stress Resistance and Longevity Taylor, Rebecca C.; Dillin, Andrew Cell, Vol. 153, Issue 7 https://doi.org/10.1016/j.cell.2013.05.042	journal	June 2013
A Feedback Regulatory Loop between G3P and Lipid Transfer Proteins DIR1 and AZI1 Mediates Azelaic-Acid-Induced Systemic Immunity Yu, Keshun; Soares, Juliana Moreira; Mandal, Mihir Kumar Cell Reports, Vol. 3, Issue 4 https://doi.org/10.1016/j.celrep.2013.03.030	journal	April 2013
Plasmodesmata Localizing Proteins Regulate Transport and Signaling during Systemic Acquired Immunity in Plants Lim, Gah-Hyun; Shine, M. B.; de Lorenzo, Laura Cell Host & Microbe, Vol. 19, Issue 4 https://doi.org/10.1016/j.chom.2016.03.006	journal	April 2016
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
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
Callose Biosynthesis Regulates Symplastic Trafficking during Root Development Vatén, Anne; Dettmer, Jan; Wu, Shuang Developmental Cell, Vol. 21, Issue 6 https://doi.org/10.1016/j.devcel.2011.10.006	journal	December 2011
Long distance transport and movement of RNA through the phloem Kehr, J.; Buhtz, A. Journal of Experimental Botany, Vol. 59, Issue 1 https://doi.org/10.1093/jxb/erm176	journal	December 2007
Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling Tabata, R.; Sumida, K.; Yoshii, T. Science, Vol. 346, Issue 6207 https://doi.org/10.1126/science.1257800	journal	October 2014
Xbp1s in Pomc Neurons Connects ER Stress with Energy Balance and Glucose Homeostasis Williams, Kevin W.; Liu, Tiemin; Kong, Xingxing Cell Metabolism, Vol. 20, Issue 3 https://doi.org/10.1016/j.cmet.2014.06.002	journal	September 2014
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
Two Pseudomonas syringae Type III Effectors Inhibit RIN4-Regulated Basal Defense in Arabidopsis Kim, Min Gab; da Cunha, Luis; McFall, Aidan J. Cell, Vol. 121, Issue 5 https://doi.org/10.1016/j.cell.2005.03.025	journal	June 2005
Intercellular movement of the putative transcription factor SHR in root patterning Nakajima, Keiji; Sena, Giovanni; Nawy, Tal Nature, Vol. 413, Issue 6853 https://doi.org/10.1038/35095061	journal	September 2001
The Dynamic of the Splicing of bZIP60 and the Proteins Encoded by the Spliced and Unspliced mRNAs Reveals Some Unique Features during the Activation of UPR in Arabidopsis thaliana Parra-Rojas, Juan; Moreno, Adrian A.; Mitina, Irina PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0122936	journal	April 2015
Mobile FT mRNA contributes to the systemic florigen signalling in floral induction Li, Chunyang; Gu, Mei; Shi, Nongnong Scientific Reports, Vol. 1, Issue 1 https://doi.org/10.1038/srep00073	journal	August 2011
Mechanisms Regulating SHORT-ROOT Intercellular Movement Gallagher, Kimberly L.; Paquette, Alice J.; Nakajima, Keiji Current Biology, Vol. 14, Issue 20 https://doi.org/10.1016/j.cub.2004.09.081	journal	October 2004
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
An efficient flat-surface collar-free grafting method for Arabidopsis thaliana seedlings Marsch-Martínez, Nayelli; Franken, John; Gonzalez-Aguilera, Karla L. Plant Methods, Vol. 9, Issue 1 https://doi.org/10.1186/1746-4811-9-14	journal	January 2013
Identification of SHRUBBY, a SHORT-ROOT and SCARECROW interacting protein that controls root growth and radial patterning Koizumi, K.; Gallagher, K. L. Development, Vol. 140, Issue 6 https://doi.org/10.1242/dev.090761	journal	February 2013
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
A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling Gilroy, Simon; Suzuki, Nobuhiro; Miller, Gad Trends in Plant Science, Vol. 19, Issue 10 https://doi.org/10.1016/j.tplants.2014.06.013	journal	October 2014
An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants Zuo, Jianru; Niu, Qi-Wen; Chua, Nam-Hai The Plant Journal, Vol. 24, Issue 2 https://doi.org/10.1046/j.1365-313x.2000.00868.x	journal	October 2000
SHORT-ROOT and SCARECROW Regulate Leaf Growth in Arabidopsis by Stimulating S-Phase Progression of the Cell Cycle Dhondt, Stijn; Coppens, Frederik; De Winter, Freya Plant Physiology, Vol. 154, Issue 3 https://doi.org/10.1104/pp.110.158857	journal	August 2010
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 Ruberti, Cristina; Lai, YaShiuan; Brandizzi, Federica The Plant Journal, Vol. 93, Issue 1 https://doi.org/10.1111/tpj.13768	journal	December 2017
Lights at the end of the tunnel: new views of plasmodesmal structure and function Xu, Xianfeng Morgan; Jackson, David Current Opinion in Plant Biology, Vol. 13, Issue 6 https://doi.org/10.1016/j.pbi.2010.09.003	journal	December 2010
Symplastic signaling instructs cell division, cell expansion, and cell polarity in the ground tissue of Arabidopsis thaliana roots Wu, Shuang; O’Lexy, Ruthsabel; Xu, Meizhi Proceedings of the National Academy of Sciences, Vol. 113, Issue 41 https://doi.org/10.1073/pnas.1610358113	journal	September 2016
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
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
Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants Sparkes, Imogen A.; Runions, John; Kearns, Anne Nature Protocols, Vol. 1, Issue 4 https://doi.org/10.1038/nprot.2006.286	journal	November 2006
The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling Helariutta, Yrjo; Fukaki, Hidehiro; Wysocka-Diller, Joanna Cell, Vol. 101, Issue 5 https://doi.org/10.1016/S0092-8674(00)80865-X	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
Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments Deeken, Rosalia; Ache, Peter; Kajahn, Inga The Plant Journal, Vol. 55, Issue 5 https://doi.org/10.1111/j.1365-313X.2008.03555.x	journal	September 2008
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
Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly Haseloff, J.; Siemering, K. R.; Prasher, D. C. Proceedings of the National Academy of Sciences, Vol. 94, Issue 6 https://doi.org/10.1073/pnas.94.6.2122	journal	March 1997
Systemic Acquired Resistance: Turning Local Infection into Global Defense Fu, Zheng Qing; Dong, Xinnian Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105606	journal	April 2013
Transport of Proteins and Nucleic Acids Through Plasmodesmata Ghoshroy, Soumitra; Lartey, Robert; Sheng, Jinsong Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.arplant.48.1.27	journal	June 1997
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
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
Non-Targeted and Targeted Protein Movement through Plasmodesmata in Leaves in Different Developmental and Physiological States Crawford, Katrina M.; Zambryski, Patricia C. Plant Physiology, Vol. 125, Issue 4 https://doi.org/10.1104/pp.125.4.1802	journal	April 2001
ER stress signaling requires RHD3, a functionally conserved ER-shaping GTPase Lai, Ya-Shiuan; Stefano, Giovanni; Brandizzi, Federica Journal of Cell Science, Vol. 127, Issue 15 https://doi.org/10.1242/jcs.147447	journal	May 2014
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

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:1619789

Ruberti, Cristina; Lai, YaShiuan; Brandizzi, Federica

Advanced genomics identifies growth effectors for proteotoxic ER stress recovery in Arabidopsis thaliana

Journal Article · Tue Jan 11 00:00:00 EST 2022 · Communications Biology · OSTI ID:1619789

Ko, Dae Kwan; Brandizzi, Federica

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:1619789

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

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Systemic signaling contributes to the unfolded protein response of the plant endoplasmic reticulum

Citation Formats

References (49)

Similar Records

Related Subjects