Relevance of the Unfolded Protein Response to Spaceflight-Induced Transcriptional Reprogramming in Arabidopsis

Angelos, Evan; Ko, Dae Kwan; Zemelis-Durfee, Starla; Brandizzi, Federica

doi:10.1089/ast.2020.2313

Relevance of the Unfolded Protein Response to Spaceflight-Induced Transcriptional Reprogramming in Arabidopsis

Journal Article · Mon Dec 14 23:00:00 EST 2020 · Astrobiology

DOI:https://doi.org/10.1089/ast.2020.2313· OSTI ID:1764378

Angelos, Evan ^[1]; Ko, Dae Kwan ^[2]; Zemelis-Durfee, Starla ^[2]; Brandizzi, Federica ^[2]

Michigan State Univ., East Lansing, MI (United States); MSU-DOE Plant Research Laboratory
Michigan State Univ., East Lansing, MI (United States)

Plants are primary producers of food and oxygen on Earth and will likewise be indispensable to the establishment of large-scale sustainable ecosystems and human survival in space. To contribute to the understanding of how plants respond to spaceflight stress, we examined the significance of the unfolded protein response (UPR), a conserved signaling cascade that responds to a number of unfavorable environmental stresses, in the model plant Arabidopsis thaliana. To do so, we performed a large-scale comparative transcriptome profiling in wild type and various UPR-defective mutants during the SpaceX-CRS12 mission to the International Space Station. We established that orbital culture substantially alters the expression of hundreds of stress-related genes compared with ground control conditions. Although expression of those genes varied in the UPR mutants on the ground, it was largely similar across the genotypes in the spaceflight condition. Furthermore, our results have yielded new information on how plants respond to growth in orbit and support the hypothesis that spaceflight induces the activation of signaling pathways that compensate for the loss of UPR regulators in the control of downstream transcriptional regulatory networks.

View Accepted Manuscript (DOE)

Research Organization:: Great Lakes Bioenergy Research Center; GLBRC; Michigan State University

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0018409; FC02-07ER64494; FG02-91ER20021

OSTI ID:: 1764378

Journal Information:: Astrobiology, Journal Name: Astrobiology Journal Issue: 3 Vol. 21; ISSN 1531-1074

Publisher:: Mary Ann Liebert, Inc.Copyright Statement

Country of Publication:: United States

Language:: English

References (52)

Variation in the transcriptome of different ecotypes of Arabidopsis thaliana reveals signatures of oxidative stress in plant responses to spaceflight Choi, Won-Gyu; Barker, Richard J.; Kim, Su-Hwa American Journal of Botany, Vol. 106, Issue 1 https://doi.org/10.1002/ajb2.1223	journal	January 2019
AtIRE1C, an unconventional isoform of the UPR master regulator AtIRE1, is functionally associated with AtIRE1B in Arabidopsis gametogenesis Pu, Yunting; Ruberti, Cristina; Angelos, Evan R. Plant Direct, Vol. 3, Issue 11 https://doi.org/10.1002/pld3.187	journal	November 2019
Morphometric analyses of petioles of seedlings grown in a spaceflight experiment Johnson, Christina M.; Subramanian, Aswati; Edelmann, Richard E. Journal of Plant Research, Vol. 128, Issue 6 https://doi.org/10.1007/s10265-015-0749-0	journal	September 2015
Plants in space Ferl, Robert; Wheeler, Raymond; Levine, Howard G. Current Opinion in Plant Biology, Vol. 5, Issue 3 https://doi.org/10.1016/S1369-5266(02)00254-6	journal	June 2002
The UPR Activator ATF6 Responds to Proteotoxic and Lipotoxic Stress by Distinct Mechanisms Tam, Arvin B.; Roberts, Lindsay S.; Chandra, Vivek Developmental Cell, Vol. 46, Issue 3 https://doi.org/10.1016/j.devcel.2018.04.023	journal	August 2018
Growth in spaceflight hardware results in alterations to the transcriptome and proteome Basu, Proma; Kruse, Colin P. S.; Luesse, Darron R. Life Sciences in Space Research, Vol. 15 https://doi.org/10.1016/j.lssr.2017.09.001	journal	November 2017
Activation of the Unfolded Protein Response by Lipid Bilayer Stress Halbleib, Kristina; Pesek, Kristina; Covino, Roberto Molecular Cell, Vol. 67, Issue 4 https://doi.org/10.1016/j.molcel.2017.06.012	journal	August 2017
Amino Acid Catabolism in Plants Hildebrandt, Tatjana M.; Nunes Nesi, Adriano; Araújo, Wagner L. Molecular Plant, Vol. 8, Issue 11 https://doi.org/10.1016/j.molp.2015.09.005	journal	November 2015
The Pre-rRNA Processing Complex in Arabidopsis Includes Two WD40-Domain-Containing Proteins Encoded by Glucose-Inducible Genes and Plant-Specific Proteins Ishida, Tetsuya; Maekawa, Shugo; Yanagisawa, Shuichi Molecular Plant, Vol. 9, Issue 2 https://doi.org/10.1016/j.molp.2015.11.003	journal	February 2016
Functional Diversification of ER Stress Responses in Arabidopsis Pastor-Cantizano, Noelia; Ko, Dae Kwan; Angelos, Evan Trends in Biochemical Sciences, Vol. 45, Issue 2 https://doi.org/10.1016/j.tibs.2019.10.008	journal	February 2020
X-ray Radiation Induces Deprotonation of the Bilin Chromophore in Crystalline D. radiodurans Phytochrome Li, Feifei; Burgie, E. Sethe; Yu, Tao Journal of the American Chemical Society, Vol. 137, Issue 8 https://doi.org/10.1021/ja510923m	journal	February 2015
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Trapnell, Cole; Williams, Brian A.; Pertea, Geo Nature Biotechnology, Vol. 28, Issue 5 https://doi.org/10.1038/nbt.1621	journal	May 2010
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Signal integration in the endoplasmic reticulum unfolded protein response Ron, David; Walter, Peter Nature Reviews Molecular Cell Biology, Vol. 8, Issue 7 https://doi.org/10.1038/nrm2199	journal	July 2007
Integrated TORC1 and PKA signaling control the temporal activation of glucose-induced gene expression in yeast Kunkel, Joseph; Luo, Xiangxia; Capaldi, Andrew P. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11540-y	journal	August 2019
Protocol Update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0) Mi, Huaiyu; Muruganujan, Anushya; Huang, Xiaosong Nature Protocols, Vol. 14, Issue 3 https://doi.org/10.1038/s41596-019-0128-8	journal	February 2019
Evaluation of two main RNA-seq approaches for gene quantification in clinical RNA sequencing: polyA+ selection versus rRNA depletion Zhao, Shanrong; Zhang, Ying; Gamini, Ramya Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-23226-4	journal	March 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
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
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
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
Photoreceptor effects on plant biomass, resource allocation, and metabolic state Yang, Deyue; Seaton, Daniel D.; Krahmer, Johanna Proceedings of the National Academy of Sciences, Vol. 113, Issue 27 https://doi.org/10.1073/pnas.1601309113	journal	June 2016
Spaceflight Transcriptomes: Unique Responses to a Novel Environment Paul, Anna-Lisa; Zupanska, Agata K.; Ostrow, Dejerianne T. Astrobiology, Vol. 12, Issue 1 https://doi.org/10.1089/ast.2011.0696	journal	January 2012
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
GeneLab: Omics database for spaceflight experiments Ray, Shayoni; Gebre, Samrawit; Fogle, Homer Bioinformatics, Vol. 35, Issue 10 https://doi.org/10.1093/bioinformatics/bty884	journal	October 2018
PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools Mi, Huaiyu; Muruganujan, Anushya; Ebert, Dustin Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1038	journal	November 2018
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
ER-Anchored Transcription Factors bZIP17 and bZIP28 Regulate Root Elongation Kim, June-Sik; Yamaguchi-Shinozaki, Kazuko; Shinozaki, Kazuo Plant Physiology, Vol. 176, Issue 3 https://doi.org/10.1104/pp.17.01414	journal	January 2018
Phytochrome-mediated Germination Responses in γ-Irradiated Lettuce Seeds Hsiao, A. I.; Vidaver, William Plant Physiology, Vol. 54, Issue 1 https://doi.org/10.1104/pp.54.1.72	journal	July 1974
Tissue-Specific Transcriptomics Reveals an Important Role of the Unfolded Protein Response in Maintaining Fertility upon Heat Stress in Arabidopsis Zhang, Shuang-Shuang; Yang, Hongxing; Ding, Lan The Plant Cell, Vol. 29, Issue 5 https://doi.org/10.1105/tpc.16.00916	journal	April 2017
Sucrose control of phytochrome A signaling in Arabidopsis. Dijkwel, P. P.; Huijser, C.; Weisbeek, P. J. The Plant Cell, Vol. 9, Issue 4 https://doi.org/10.1105/tpc.9.4.583	journal	April 1997
Sugar-inducible expression of the nucleolin-1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development: Sugar-inducible expression of nucleolin gene Kojima, Hisae; Suzuki, Takamasa; Kato, Takenori The Plant Journal, Vol. 49, Issue 6 https://doi.org/10.1111/j.1365-313X.2006.03016.x	journal	February 2007
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
Shade avoidance Franklin, Keara A. New Phytologist, Vol. 179, Issue 4 https://doi.org/10.1111/j.1469-8137.2008.02507.x	journal	August 2008
The role of amino acid metabolism during abiotic stress release Batista‐Silva, Willian; Heinemann, Björn; Rugen, Nils Plant, Cell & Environment, Vol. 42, Issue 5 https://doi.org/10.1111/pce.13518	journal	January 2019
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
Endoplasmic reticulum‐mediated unfolded protein response is an integral part of singlet oxygen signalling in plants Beaugelin, Inès; Chevalier, Anne; D'Alessandro, Stefano The Plant Journal, Vol. 102, Issue 6 https://doi.org/10.1111/tpj.14700	journal	February 2020
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
mTOR-Dependent Regulation of Ribosomal Gene Transcription Requires S6K1 and Is Mediated by Phosphorylation of the Carboxy-Terminal Activation Domain of the Nucleolar Transcription Factor UBF† Hannan, Katherine M.; Brandenburger, Yves; Jenkins, Anna Molecular and Cellular Biology, Vol. 23, Issue 23 https://doi.org/10.1128/MCB.23.23.8862-8877.2003	journal	December 2003
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Kim, Daehwan; Pertea, Geo; Trapnell, Cole Genome Biology, Vol. 14, Issue 4 https://doi.org/10.1186/gb-2013-14-4-r36	journal	January 2013
Epigenomics in an extraterrestrial environment: organ-specific alteration of DNA methylation and gene expression elicited by spaceflight in Arabidopsis thaliana Zhou, Mingqi; Sng, Natasha J.; LeFrois, Collin E. BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5554-z	journal	March 2019
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
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 PLOS Genetics, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pgen.1005164	journal	April 2015
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
Genetic dissection of the Arabidopsis spaceflight transcriptome: Are some responses dispensable for the physiological adaptation of plants to spaceflight? Paul, Anna-Lisa; Sng, Natasha J.; Zupanska, Agata K. PLOS ONE, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pone.0180186	journal	June 2017
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
Unfolded protein-independent IRE1 activation contributes to multifaceted developmental processes in Arabidopsis Mishiba, Kei-ichiro; Iwata, Yuji; Mochizuki, Tomofumi Life Science Alliance, Vol. 2, Issue 5 https://doi.org/10.26508/lsa.201900459	journal	October 2019
Fundamental Plant Biology Enabled by The Space Shuttle Paul, Anna-Lisa; Wheeler, Ray M.; Levine, Howard G. American Journal of Botany, Vol. 100, Issue 1 https://doi.org/10.3732/ajb.1200338	journal	January 2013
Transcriptional response of Arabidopsis seedlings during spaceflight reveals peroxidase and cell wall remodeling genes associated with root hair development Kwon, Taegun; Sparks, J. Alan; Nakashima, Jin American Journal of Botany, Vol. 102, Issue 1 https://doi.org/10.3732/ajb.1400458	journal	January 2015
Comparative transcriptomics indicate changes in cell wall organization and stress response in seedlings during spaceflight Johnson, Christina M.; Subramanian, Aswati; Pattathil, Sivakumar American Journal of Botany, Vol. 104, Issue 8 https://doi.org/10.3732/ajb.1700079	journal	August 2017
Impact of the UPR on the virulence of the plant fungal pathogen A. brassicicola Guillemette, Thomas; Calmes, Benoit; Simoneau, Philippe Virulence, Vol. 5, Issue 2 https://doi.org/10.4161/viru.26772	journal	October 2013

Similar Records

The Arabidopsis endoplasmic reticulum associated degradation pathways are involved in the regulation of heat stress response

Journal Article · Sat May 27 00:00:00 EDT 2017 · Biochemical and Biophysical Research Communications · OSTI ID:22697033

Transcriptional competition shapes proteotoxic ER stress resolution

Journal Article · Mon May 16 00:00:00 EDT 2022 · Nature Plants (Online) · OSTI ID:1876165

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Arabidopsis
microgravity
spaceflight
unfolded protein response

Relevance of the Unfolded Protein Response to Spaceflight-Induced Transcriptional Reprogramming in Arabidopsis

Citation Formats

References (52)

Similar Records

Related Subjects