In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling
Abstract
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,more »
- Authors:
-
- Michigan State Univ., East Lansing, MI (United States)
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Institutes of Health (NHI)
- OSTI Identifier:
- 1596268
- Grant/Contract Number:
- FG02-91ER20021; FC02-07ER64494; GM101038
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Planta
- Additional Journal Information:
- Journal Volume: 246; Journal Issue: 1; Journal ID: ISSN 0032-0935
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Kim, Sang-Jin, Zemelis-Durfee, Starla, Wilkerson, Curtis, and Brandizzi, Federica. In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling. United States: N. p., 2017.
Web. doi:10.1007/s00425-017-2687-7.
Kim, Sang-Jin, Zemelis-Durfee, Starla, Wilkerson, Curtis, & Brandizzi, Federica. In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling. United States. https://doi.org/10.1007/s00425-017-2687-7
Kim, Sang-Jin, Zemelis-Durfee, Starla, Wilkerson, Curtis, and Brandizzi, Federica. Fri .
"In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling". United States. https://doi.org/10.1007/s00425-017-2687-7. https://www.osti.gov/servlets/purl/1596268.
@article{osti_1596268,
title = {In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling},
author = {Kim, Sang-Jin and Zemelis-Durfee, Starla and Wilkerson, Curtis and Brandizzi, Federica},
abstractNote = {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.},
doi = {10.1007/s00425-017-2687-7},
journal = {Planta},
number = 1,
volume = 246,
place = {United States},
year = {Fri Mar 31 00:00:00 EDT 2017},
month = {Fri Mar 31 00:00:00 EDT 2017}
}
Web of Science
Works referenced in this record:
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops
journal, January 2013
- Bita, Craita E.; Gerats, Tom
- Frontiers in Plant Science, Vol. 4
Cellulose Synthase-Like CslF Genes Mediate the Synthesis of Cell Wall (1,3;1,4)- -D-Glucans
journal, March 2006
- Burton, R. A.
- Science, Vol. 311, Issue 5769
Tissue-specific regulation of BiP genes: a cis-acting regulatory domain is required for BiP promoter activity in plant meristems
journal, January 2002
- Buzeli, Reginaldo A. A.; Cascardo, Júlio C. M.; Rodrigues, Leonardo A. Z.
- Plant Molecular Biology, Vol. 50, Issue 4/5, p. 757-771
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
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
Endoplasmic Reticulum (ER) Stress Response and Its Physiological Roles in Plants
journal, April 2013
- Deng, Yan; Srivastava, Renu; Howell, Stephen
- International Journal of Molecular Sciences, Vol. 14, Issue 4
Unfolded protein response in pollen development and heat stress tolerance
journal, March 2016
- Fragkostefanakis, Sotirios; Mesihovic, Anida; Hu, Yangjie
- Plant Reproduction, Vol. 29, Issue 1-2
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
Brachypodium distachyon grain: characterization of endosperm cell walls
journal, November 2010
- Guillon, F.; Bouchet, B.; Jamme, F.
- Journal of Experimental Botany, Vol. 62, Issue 3
A comparative view of grain development in Brachypodium distachyon
journal, July 2012
- Hands, Philip; Drea, Sinéad
- Journal of Cereal Science, Vol. 56, Issue 1
Perk Is Essential for Translational Regulation and Cell Survival during the Unfolded Protein Response
journal, May 2000
- Harding, Heather P.; Zhang, Yuhong; Bertolotti, Anne
- Molecular Cell, Vol. 5, Issue 5
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
journal, December 2011
- Hayashi, Shimpei; Wakasa, Yuhya; Takahashi, Hideyuki
- The Plant Journal, Vol. 69, Issue 6
Identification of a cis -element that mediates multiple pathways of the endoplasmic reticulum stress response in rice
journal, March 2013
- Hayashi, Shimpei; Takahashi, Hideyuki; Wakasa, Yuhya
- The Plant Journal, Vol. 74, Issue 2
bZIP17 and bZIP60 Regulate the Expression of BiP3 and Other Salt Stress Responsive Genes in an UPR-Independent Manner in Arabidopsis thaliana : bZIP17
journal, June 2015
- Henriquez-Valencia, Carlos; Moreno, Adrian A.; Sandoval-Ibañez, Omar
- Journal of Cellular Biochemistry, Vol. 116, Issue 8
Arabidopsis bZIP60 Is a Proteolysis-Activated Transcription Factor Involved in the Endoplasmic Reticulum Stress Response
journal, November 2008
- Iwata, Yuji; Fedoroff, Nina V.; Koizumi, Nozomu
- The Plant Cell, Vol. 20, Issue 11
The cytoplasmic localization of the catalytic site of CSLF6 supports a channeling model for the biosynthesis of mixed-linkage glucan
journal, February 2015
- Kim, Sang-Jin; Zemelis, Starla; Keegstra, Kenneth
- The Plant Journal, Vol. 81, Issue 4
ER stress signaling requires RHD3, a functionally conserved ER-shaping GTPase
journal, May 2014
- Lai, Ya-Shiuan; Stefano, Giovanni; Brandizzi, Federica
- Journal of Cell Science, Vol. 127, Issue 15
Brachypodium distachyon grain: identification and subcellular localization of storage proteins
journal, April 2010
- Larré, C.; Penninck, S.; Bouchet, B.
- Journal of Experimental Botany, Vol. 61, Issue 6
Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering
journal, August 2010
- Li, H.; Korennykh, A. V.; Behrman, S. L.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 37
ZmbZIP60 mRNA is spliced in maize in response to ER stress
journal, March 2012
- Li, Yanjie; Humbert, Sabrina; Howell, Stephen H.
- BMC Research Notes, Vol. 5, Issue 1
IRE1 Signaling Affects Cell Fate During the Unfolded Protein Response
journal, November 2007
- Lin, J. H.; Li, H.; Yasumura, D.
- Science, Vol. 318, Issue 5852
bZIP28 and NF-Y Transcription Factors Are Activated by ER Stress and Assemble into a Transcriptional Complex to Regulate Stress Response Genes in Arabidopsis
journal, March 2010
- Liu, Jian-Xiang; Howell, Stephen H.
- The Plant Cell, Vol. 22, Issue 3
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
Conservation of IRE1-Regulated bZIP74 mRNA Unconventional Splicing in Rice (Oryza sativa L.) Involved in ER Stress Responses
journal, March 2012
- Lu, Sun-Jie; Yang, Zheng-Ting; Sun, Ling
- Molecular Plant, Vol. 5, Issue 2
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
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
Endosperm development in Brachypodium distachyon
journal, November 2010
- Opanowicz, Magdalena; Hands, Philip; Betts, Donna
- Journal of Experimental Botany, Vol. 62, Issue 2
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
journal, April 2015
- Parra-Rojas, Juan; Moreno, Adrian A.; Mitina, Irina
- PLOS ONE, Vol. 10, Issue 4
Molecular mechanisms of the plant heat stress response
journal, March 2013
- Qu, Ai-Li; Ding, Yan-Fei; Jiang, Qiong
- Biochemical and Biophysical Research Communications, Vol. 432, Issue 2
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
The Secreted Plant N-Glycoproteome and Associated Secretory Pathways
journal, January 2012
- Ruiz-May, Eliel; Kim, Sang-Jin; Brandizzi, Federica
- Frontiers in Plant Science, Vol. 3
Discordance of UPR signaling by ATF6 and Ire1p-XBP1 with levels of target transcripts
journal, April 2004
- Shang, Jie; Lehrman, Mark A.
- Biochemical and Biophysical Research Communications, Vol. 317, Issue 2
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
Cereal seed storage proteins: structures, properties and role in grain utilization
journal, April 2002
- Shewry, Peter R.; Halford, Nigel G.
- Journal of Experimental Botany, Vol. 53, Issue 370
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011
- Sievers, Fabian; Wilm, Andreas; Dineen, David
- Molecular Systems Biology, Vol. 7, Issue 1
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
Loss of Cellulose Synthase - Like F6 Function Affects Mixed-Linkage Glucan Deposition, Cell Wall Mechanical Properties, and Defense Responses in Vegetative Tissues of Rice
journal, March 2012
- Vega-Sánchez, Miguel E.; Verhertbruggen, Yves; Christensen, Ulla
- Plant Physiology, Vol. 159, Issue 1
The Unfolded Protein Response: From Stress Pathway to Homeostatic Regulation
journal, November 2011
- Walter, P.; Ron, D.
- Science, Vol. 334, Issue 6059
Determining the Subcellular Location of Synthesis and Assembly of the Cell Wall Polysaccharide (1,3; 1,4)-β-d-Glucan in Grasses
journal, March 2015
- Wilson, Sarah M.; Ho, Yin Ying; Lampugnani, Edwin R.
- The Plant Cell, Vol. 27, Issue 3
Differential Contributions of ATF6 and XBP1 to the Activation of Endoplasmic Reticulum Stress-Responsive cis-Acting Elements ERSE, UPRE and ERSE-II
journal, September 2004
- Yamamoto, K.
- Journal of Biochemistry, Vol. 136, Issue 3
Cotranslational Targeting of XBP1 Protein to the Membrane Promotes Cytoplasmic Splicing of Its Own mRNA
journal, April 2009
- Yanagitani, Kota; Imagawa, Yusuke; Iwawaki, Takao
- Molecular Cell, Vol. 34, Issue 2
ER Stress Induces Cleavage of Membrane-Bound ATF6 by the Same Proteases that Process SREBPs
journal, December 2000
- Ye, Jin; Rawson, Robert B.; Komuro, Ryutaro
- Molecular Cell, Vol. 6, Issue 6
Isolation and characterization of plant cell walls and cell wall components
book, January 1986
- York, William S.; Darvill, Alan G.; McNeil, Michael
- Methods in Enzymology
XBP1 mRNA Is Induced by ATF6 and Spliced by IRE1 in Response to ER Stress to Produce a Highly Active Transcription Factor
journal, December 2001
- Yoshida, Hiderou; Matsui, Toshie; Yamamoto, Akira
- Cell, Vol. 107, Issue 7
Molecular Characterization and Expression Profiling of the Protein Disulfide Isomerase Gene Family in Brachypodium distachyon L
journal, April 2014
- Zhu, Chong; Luo, Nana; He, Miao
- PLoS ONE, Vol. 9, Issue 4
Mfold web server for nucleic acid folding and hybridization prediction
journal, July 2003
- Zuker, M.
- Nucleic Acids Research, Vol. 31, Issue 13
Works referencing / citing this record:
In the grass species Brachypodium distachyon , the production of mixed‐linkage (1,3;1,4)‐β‐glucan ( MLG ) occurs in the Golgi apparatus
journal, February 2018
- Kim, Sang‐Jin; Zemelis‐Durfee, Starla; Jensen, Jacob Krüger
- The Plant Journal, Vol. 93, Issue 6