*Result*: Transcriptome analysis coupled with virus induced gene silencing delineates the unfolded protein response of tomato.
Title:
Transcriptome analysis coupled with virus induced gene silencing delineates the unfolded protein response of tomato.
Authors:
Rana A; BRIC-National Agri-Food and Biomanufacturing Institute, Mohali, Punjab, India.; Regional Centre for Biotechnology, Faridabad, India., Kaur N; BRIC-National Agri-Food and Biomanufacturing Institute, Mohali, Punjab, India.; University of New Brunswick, Frederickton, Canada., Pandey AK; BRIC-National Agri-Food and Biomanufacturing Institute, Mohali, Punjab, India., Kandoth PK; BRIC-National Agri-Food and Biomanufacturing Institute, Mohali, Punjab, India. pramod@cukerala.ac.in.; Central University of Kerala, Kasaragod, Periye, Kerala, India. pramod@cukerala.ac.in.
Source:
Molecular genetics and genomics : MGG [Mol Genet Genomics] 2026 Mar 10; Vol. 301 (1). Date of Electronic Publication: 2026 Mar 10.
Publication Type:
Journal Article
Language:
English
Journal Info:
Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 101093320 Publication Model: Electronic Cited Medium: Internet ISSN: 1617-4623 (Electronic) Linking ISSN: 16174623 NLM ISO Abbreviation: Mol Genet Genomics Subsets: MEDLINE
Imprint Name(s):
Original Publication: Berlin : Springer-Verlag, c2001-
MeSH Terms:
Solanum lycopersicum*/genetics , Solanum lycopersicum*/virology , Solanum lycopersicum*/metabolism , Unfolded Protein Response*/genetics , Transcriptome*/genetics, Endoplasmic Reticulum Stress/genetics ; Endoplasmic Reticulum Stress/drug effects ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Gene Expression Profiling/methods ; Basic-Leucine Zipper Transcription Factors/genetics ; Tunicamycin/pharmacology ; Gene Expression Regulation, Plant ; Gene Silencing
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Czékus Z, Csíkos O, Ördög A, Tari I, Poór P (2020) Effects of Jasmonic Acid in ER Stress and Unfolded Protein Response in Tomato Plants. Biomolecules 10:1031. (PMID: 32664460740731210.3390/biom10071031)
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Daudi A, O’brien JA (2012) Detection of hydrogen peroxide by DAB staining in Arabidopsis leaves. Bio Protoc 2:e263. (PMID: 27390754493290210.21769/BioProtoc.263)
Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, Howell SH (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci U S A 108:7247–7252. (PMID: 21482766308411910.1073/pnas.1102117108)
Deng Y, Srivastava R, Howell SH (2013a) Endoplasmic reticulum (ER) stress response and its physiological roles in plants. Int J Mol Sci 14:8188–8212. (PMID: 23591838364573810.3390/ijms14048188)
Deng Y, Srivastava R, Howell SH (2013b) Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis. Proc Natl Acad Sci U S A 110:19633–19638. (PMID: 24145452384509910.1073/pnas.1314749110)
Faria JAQA, Reis PAB, Reis MTB, Rosado GL, Pinheiro GL, Mendes GC, Fontes EPB (2011) The NAC domain-containing protein, GmNAC6, is a downstream component of the ER stress- and osmotic stress-induced NRP-mediated cell-death signaling pathway. BMC Plant Biol 11:129. (PMID: 21943253319303410.1186/1471-2229-11-129)
Geng X, Zang X, Li H, Liu Z, Zhao A, Liu J, Peng H, Yao Y, Hu Z, Ni Z, Sun Q, Xin M (2018) Unconventional splicing of wheat TabZIP60 confers heat tolerance in transgenic Arabidopsis. Plant Sci 274:252–260. (PMID: 3008061110.1016/j.plantsci.2018.05.029)
Han K, Zhao Y, Sun Y, Li Y (2023) NACs, generalist in plant life. Plant Biotech J 21:2433–2457. (PMID: 10.1111/pbi.14161)
Hayashi S, Wakasa Y, Takaiwa F (2012) Functional integration between defence and IRE1-mediated ER stress response in rice. Sci Rep 2:670. (PMID: 22993695344591410.1038/srep00670)
Henriquez-Valencia C, Moreno AA, Sandoval-Ibañez O, Mitina I, Blanco-Herrera F, Cifuentes-Esquivel N, Orellana A (2015) BZIP17 and bZIP60 Regulate the Expression of BiP3 and Other Salt Stress Responsive Genes in an UPR-Independent Manner in Arabidopsis thaliana. J Cell Biochem 116:1638–1645. (PMID: 2570466910.1002/jcb.25121)
Herath V, Gayral M, Miller RK, Verchot J (2020) BIP and the unfolded protein response are important for potyvirus and potexvirus infection. Plant Signal Behav 15:1807723. (PMID: 32799639759808210.1080/15592324.2020.1807723)
Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol 64:477–499. (PMID: 2333079410.1146/annurev-arplant-050312-120053)
Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci U S A 102:5280–5285. (PMID: 1578187355597810.1073/pnas.0408941102)
Iwata, Y.; Koizumi, N. (2012) Plant transducers of the endoplasmicreticulum unfolded protein response. Trends Plant Sci. 17, 720–727.
Kandoth PK, Ranf S, Pancholi SS, Jayanty S, Walla MD, Miller W, Howe GA, Lincoln DE, Stratmann JW, Ryan CA (2007) Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects. Proc Natl Acad Sci U S A 104:12205–12210. (PMID: 17623784192453410.1073/pnas.0700344104)
Kaur N, Kandoth PK (2021) Tomato bZIP60 mRNA undergoes splicing in endoplasmic reticulum stress and in response to environmental stresses. Plant Physiol Biochem 160:397–403. (PMID: 3355675510.1016/j.plaphy.2021.01.033)
Kimata Y, Oikawa D, Shimizu Y, Ishiwata-Kimata Y, Kohno K (2004) A role for BiP as an adjustor for the endoplasmic reticulum stress-sensing protein Ire1. J Cell Biol 167:445–456. (PMID: 15520230217250110.1083/jcb.200405153)
Ko DK, Brandizzi F (2024) Dynamics of ER stress-induced gene regulation in plants. Nat Rev Genet 25:513–525. (PMID: 384997691118672510.1038/s41576-024-00710-4)
Koizumi N, Martinez IM, Kimata Y, Kohno K, Sano H, Chrispeels MJ (2001) Molecular Characterization of Two Arabidopsis Ire1 Transmembrane Protein Kinases 1. Plant Physiol 127:949–962. (PMID: 1170617712926610.1104/pp.010636)
Liu JX, Howell SH (2010a) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22:2930–2942. (PMID: 20876830296555110.1105/tpc.110.078154)
Liu JX, Howell SH (2010b) bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell 22:782–796. (PMID: 20207753286147510.1105/tpc.109.072173)
Liu JX, Srivastava R, Che P, Howell SH (2007a) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909. (PMID: 17662035215617210.1111/j.1365-313X.2007.03195.x)
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Grant Information:
Department of Biotechnology, Ministry of Science and Technology, India Department of Biotechnology, Ministry of Science and Technology, India
Contributed Indexing:
Keywords: ER stress; IRE1; NAC-TF; Tomato; UPR; VIGS; bZIP60
Substance Nomenclature:
0 (Plant Proteins)
0 (Basic-Leucine Zipper Transcription Factors)
11089-65-9 (Tunicamycin)
0 (Basic-Leucine Zipper Transcription Factors)
11089-65-9 (Tunicamycin)
Entry Date(s):
Date Created: 20260310 Date Completed: 20260311 Latest Revision: 20260310
Update Code:
20260311
DOI:
10.1007/s00438-026-02400-8
PMID:
41805988
Database:
MEDLINE
*Further Information*
*The molecular details of endoplasmic reticulum (ER) stress and the unfolded protein response (UPR) and their functional significance in combating environmental stress in crop species remain inadequately elucidated. Tomato (Solanum lycopersicum) is an important crop, sensitive to temperature, and serves as a model crop plant for studying these pathways. To establish a tomato UPR transcriptome profile, we performed RNA sequencing (RNA-seq) analysis of tomato seedlings under tunicamycin (Tm)-induced ER stress. The 339 differentially expressed genes encompassed traditional ER stress markers, ER-associated degradation elements, transcription factors, and novel candidate genes. Our functional analysis of key UPR genes, viz., SlIRE1A, SlIRE1B, SlbZIP60, and SlbZIP28, using Virus-Induced Gene Silencing (VIGS) revealed differential requirements for SlIRE1A and SlIRE1B in the Tm-induced upregulation of downstream genes. Additionally, we found that the expression of most of the downstream genes we analyzed was equally dependent on both the IRE1 and bZIP28 pathways. The expression analysis of several of these genes under environmental stress conditions indicated that their expression patterns did not align with those observed during ER stress. Furthermore, our analysis of VIGS plants subjected to heat stress revealed that the regulation of reactive oxygen species (ROS) levels in tomato depends on the IRE1-bZIP60 pathway. Overall, this study provides a comprehensive analysis of UPR pathways in tomato and offers essential molecular insights for developing resilient tomato cultivars that can withstand adverse environmental conditions.
(© 2026. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)*
*Declarations. Conflict of interest: The authors have no competing interests to declare that are relevant to the content of this article.*