In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling

Kim, Sang-Jin; Zemelis-Durfee, Starla; Wilkerson, Curtis; Brandizzi, Federica

doi:10.1007/s00425-017-2687-7

Title: In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling

Journal Article · Fri Mar 31 00:00:00 EDT 2017 · Planta

DOI:https://doi.org/10.1007/s00425-017-2687-7· OSTI ID:1596268

Kim, Sang-Jin ^[1]; Zemelis-Durfee, Starla ^[1]; Wilkerson, Curtis ^[1];

^[1]

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

A conserved UPR machinery is necessary for Brachypodium ER stress resistance and grain filling. Human and livestock diets depend on the accumulation of cereal storage proteins and carbohydrates, including mixed-linkage glucan (MLG), in the endosperm during seed development. Storage proteins and proteins responsible for the production of carbohydrates are synthesized in the endoplasmic reticulum (ER). Unfavorable conditions during growth that hamper the ER biosynthetic capacity, such as heat, can cause a potentially lethal condition known as ER stress, which activates the unfolded protein response (UPR), a signaling response designed to mitigate ER stress. The UPR relies primarily on a conserved ER-associated kinase and ribonuclease, IRE1, which splices the mRNA of a transcription factor (TF), such as bZIP60 in plants, to produce an active TF that controls the expression of ER resident chaperones. Here, we investigated activation of the UPR in Brachypodium, as a model to study the UPR in seeds of a monocotyledon species, as well as the consequences of heat stress on MLG deposition in seeds. We identified a Brachypodium bZIP60 orthologue and determined a positive correlation between bZIP60 splicing and ER stress induced by chemicals and heat. Each stress condition led to transcriptional modulation of several BiP genes, supporting the existence of condition-specific BiP regulation. Finally, we found that the UPR is elevated at the early stage of seed development and that MLG production is negatively affected by heat stress via modulation of MLG synthase accumulation. We present that successful accomplishment of seed filling is strongly correlated with the ability of the plant to sustain ER stress via the UPR.

View Accepted Manuscript (DOE)

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 (NHI)

Grant/Contract Number:: FG02-91ER20021; FC02-07ER64494; GM101038

OSTI ID:: 1596268

Journal Information:: Planta, Vol. 246, Issue 1; ISSN 0032-0935

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 6 works

Citation information provided by
Web of Science

References (48)

Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops Bita, Craita E.; Gerats, Tom Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00273	journal	January 2013
Plant Productivity and Environment Boyer, J. S. Science, Vol. 218, Issue 4571 https://doi.org/10.1126/science.218.4571.443	journal	October 1982
Cellulose Synthase-Like CslF Genes Mediate the Synthesis of Cell Wall (1,3;1,4)- -D-Glucans Burton, R. A. Science, Vol. 311, Issue 5769 https://doi.org/10.1126/science.1122975	journal	March 2006
Tissue-specific regulation of BiP genes: a cis-acting regulatory domain is required for BiP promoter activity in plant meristems Buzeli, Reginaldo A. A.; Cascardo, Júlio C. M.; Rodrigues, Leonardo A. Z. Plant Molecular Biology, Vol. 50, Issue 4/5, p. 757-771 https://doi.org/10.1023/A:1019994721545	journal	January 2002
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
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
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
Unfolded protein response in pollen development and heat stress tolerance Fragkostefanakis, Sotirios; Mesihovic, Anida; Hu, Yangjie Plant Reproduction, Vol. 29, Issue 1-2 https://doi.org/10.1007/s00497-016-0276-8	journal	March 2016
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
Brachypodium distachyon grain: characterization of endosperm cell walls Guillon, F.; Bouchet, B.; Jamme, F. Journal of Experimental Botany, Vol. 62, Issue 3 https://doi.org/10.1093/jxb/erq332	journal	November 2010
A comparative view of grain development in Brachypodium distachyon Hands, Philip; Drea, Sinéad Journal of Cereal Science, Vol. 56, Issue 1 https://doi.org/10.1016/j.jcs.2011.12.010	journal	July 2012
Perk Is Essential for Translational Regulation and Cell Survival during the Unfolded Protein Response Harding, Heather P.; Zhang, Yuhong; Bertolotti, Anne Molecular Cell, Vol. 5, Issue 5 https://doi.org/10.1016/S1097-2765(00)80330-5	journal	May 2000
Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the endoplasmic reticulum stress response of rice: ER stress response in rice Hayashi, Shimpei; Wakasa, Yuhya; Takahashi, Hideyuki The Plant Journal, Vol. 69, Issue 6 https://doi.org/10.1111/j.1365-313X.2011.04844.x	journal	December 2011
Identification of a cis -element that mediates multiple pathways of the endoplasmic reticulum stress response in rice Hayashi, Shimpei; Takahashi, Hideyuki; Wakasa, Yuhya The Plant Journal, Vol. 74, Issue 2 https://doi.org/10.1111/tpj.12117	journal	March 2013
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
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 cytoplasmic localization of the catalytic site of CSLF6 supports a channeling model for the biosynthesis of mixed-linkage glucan Kim, Sang-Jin; Zemelis, Starla; Keegstra, Kenneth The Plant Journal, Vol. 81, Issue 4 https://doi.org/10.1111/tpj.12748	journal	February 2015
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
Brachypodium distachyon grain: identification and subcellular localization of storage proteins Larré, C.; Penninck, S.; Bouchet, B. Journal of Experimental Botany, Vol. 61, Issue 6 https://doi.org/10.1093/jxb/erq050	journal	April 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
ZmbZIP60 mRNA is spliced in maize in response to ER stress Li, Yanjie; Humbert, Sabrina; Howell, Stephen H. BMC Research Notes, Vol. 5, Issue 1 https://doi.org/10.1186/1756-0500-5-144	journal	March 2012
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
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
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
Conservation of IRE1-Regulated bZIP74 mRNA Unconventional Splicing in Rice (Oryza sativa L.) Involved in ER Stress Responses Lu, Sun-Jie; Yang, Zheng-Ting; Sun, Ling Molecular Plant, Vol. 5, Issue 2 https://doi.org/10.1093/mp/ssr115	journal	March 2012
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
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
Endosperm development in Brachypodium distachyon Opanowicz, Magdalena; Hands, Philip; Betts, Donna Journal of Experimental Botany, Vol. 62, Issue 2 https://doi.org/10.1093/jxb/erq309	journal	November 2010
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
Molecular mechanisms of the plant heat stress response Qu, Ai-Li; Ding, Yan-Fei; Jiang, Qiong Biochemical and Biophysical Research Communications, Vol. 432, Issue 2 https://doi.org/10.1016/j.bbrc.2013.01.104	journal	March 2013
Unfolded protein response in plants: one master, many questions Ruberti, Cristina; Kim, Sang-Jin; Stefano, Giovanni Current Opinion in Plant Biology, Vol. 27 https://doi.org/10.1016/j.pbi.2015.05.016	journal	October 2015
The Secreted Plant N-Glycoproteome and Associated Secretory Pathways Ruiz-May, Eliel; Kim, Sang-Jin; Brandizzi, Federica Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00117	journal	January 2012
Discordance of UPR signaling by ATF6 and Ire1p-XBP1 with levels of target transcripts Shang, Jie; Lehrman, Mark A. Biochemical and Biophysical Research Communications, Vol. 317, Issue 2 https://doi.org/10.1016/j.bbrc.2004.03.058	journal	April 2004
ER Stress Regulation of ATF6 Localization by Dissociation of BiP/GRP78 Binding and Unmasking of Golgi Localization Signals Shen, Jingshi; Chen, Xi; Hendershot, Linda Developmental Cell, Vol. 3, Issue 1 https://doi.org/10.1016/S1534-5807(02)00203-4	journal	July 2002
Cereal seed storage proteins: structures, properties and role in grain utilization Shewry, Peter R.; Halford, Nigel G. Journal of Experimental Botany, Vol. 53, Issue 370 https://doi.org/10.1093/jexbot/53.370.947	journal	April 2002
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
BINDING PROTEIN Is a Master Regulator of the Endoplasmic Reticulum Stress Sensor/Transducer bZIP28 in Arabidopsis Srivastava, Renu; Deng, Yan; Shah, Shweta The Plant Cell, Vol. 25, Issue 4 https://doi.org/10.1105/tpc.113.110684	journal	April 2013
Loss of Cellulose Synthase - Like F6 Function Affects Mixed-Linkage Glucan Deposition, Cell Wall Mechanical Properties, and Defense Responses in Vegetative Tissues of Rice Vega-Sánchez, Miguel E.; Verhertbruggen, Yves; Christensen, Ulla Plant Physiology, Vol. 159, Issue 1 https://doi.org/10.1104/pp.112.195495	journal	March 2012
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
Determining the Subcellular Location of Synthesis and Assembly of the Cell Wall Polysaccharide (1,3; 1,4)-β-d-Glucan in Grasses Wilson, Sarah M.; Ho, Yin Ying; Lampugnani, Edwin R. The Plant Cell, Vol. 27, Issue 3 https://doi.org/10.1105/tpc.114.135970	journal	March 2015
Differential Contributions of ATF6 and XBP1 to the Activation of Endoplasmic Reticulum Stress-Responsive cis-Acting Elements ERSE, UPRE and ERSE-II Yamamoto, K. Journal of Biochemistry, Vol. 136, Issue 3 https://doi.org/10.1093/jb/mvh122	journal	September 2004
Cotranslational Targeting of XBP1 Protein to the Membrane Promotes Cytoplasmic Splicing of Its Own mRNA Yanagitani, Kota; Imagawa, Yusuke; Iwawaki, Takao Molecular Cell, Vol. 34, Issue 2 https://doi.org/10.1016/j.molcel.2009.02.033	journal	April 2009
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
Isolation and characterization of plant cell walls and cell wall components York, William S.; Darvill, Alan G.; McNeil, Michael Methods in Enzymology https://doi.org/10.1016/0076-6879(86)18062-1	book	January 1986
XBP1 mRNA Is Induced by ATF6 and Spliced by IRE1 in Response to ER Stress to Produce a Highly Active Transcription Factor Yoshida, Hiderou; Matsui, Toshie; Yamamoto, Akira Cell, Vol. 107, Issue 7 https://doi.org/10.1016/S0092-8674(01)00611-0	journal	December 2001
Molecular Characterization and Expression Profiling of the Protein Disulfide Isomerase Gene Family in Brachypodium distachyon L Zhu, Chong; Luo, Nana; He, Miao PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0094704	journal	April 2014
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

Cited By (1)

In the grass species Brachypodium distachyon , the production of mixed‐linkage (1,3;1,4)‐β‐glucan ( MLG ) occurs in the Golgi apparatus Kim, Sang‐Jin; Zemelis‐Durfee, Starla; Jensen, Jacob Krüger The Plant Journal, Vol. 93, Issue 6 https://doi.org/10.1111/tpj.13830	journal	February 2018

Similar Records

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 · OSTI ID:1596268

Lai, Ya-Shiuan; Renna, Luciana; Yarema, John; +3 more

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:1596268

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

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:1596268

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

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling

Citation Formats

References (48)

Cited By (1)

Similar Records

Related Subjects