Dynamics of ER Stress-induced Gene Regulation in Plants

Overview

Journal Nat Rev Genet

Specialty Genetics

Date 2024 Mar 19

PMID 38499769

Authors

Dae Kwan Ko

Federica Brandizzi

Affiliations

Soon will be listed here.

Abstract

Endoplasmic reticulum (ER) stress is a potentially lethal condition that is induced by the abnormal accumulation of unfolded or misfolded secretory proteins in the ER. In eukaryotes, ER stress is managed by the unfolded protein response (UPR) through a tightly regulated, yet highly dynamic, reprogramming of gene transcription. Although the core principles of the UPR are similar across eukaryotes, unique features of the plant UPR reflect the adaptability of plants to their ever-changing environments and the need to balance the demands of growth and development with the response to environmental stressors. The past decades have seen notable progress in understanding the mechanisms underlying ER stress sensing and signalling transduction pathways, implicating the UPR in the effects of physiological and induced ER stress on plant growth and crop yield. Facilitated by sequencing technologies and advances in genetic and genomic resources, recent efforts have driven the discovery of transcriptional regulators and elucidated the mechanisms that mediate the dynamic and precise gene regulation in response to ER stress at the systems level.

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References

Oberkofler V, Pratx L, Baurle I . Epigenetic regulation of abiotic stress memory: maintaining the good things while they last. Curr Opin Plant Biol. 2021; 61:102007. PMC: 8250047. DOI: 10.1016/j.pbi.2021.102007. View

Bao Y, Bassham D, Howell S . A Functional Unfolded Protein Response Is Required for Normal Vegetative Development. Plant Physiol. 2019; 179(4):1834-1843. PMC: 6446744. DOI: 10.1104/pp.18.01261. View

. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000; 408(6814):796-815. DOI: 10.1038/35048692. View

Sun L, Yang Z, Song Z, Wang M, Sun L, Lu S . The plant-specific transcription factor gene NAC103 is induced by bZIP60 through a new cis-regulatory element to modulate the unfolded protein response in Arabidopsis. Plant J. 2013; 76(2):274-86. DOI: 10.1111/tpj.12287. View

Liu J, Howell S . 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. 2010; 22(3):782-96. PMC: 2861475. DOI: 10.1105/tpc.109.072173. View

Lee Y, Ko K, Lee H, Lee E, Han K, Yoo J . CRISPR/Cas9-Mediated Gene Editing Reduces Growth Inhibition in Chinese Cabbage () under ER Stress. Int J Mol Sci. 2023; 24(17). PMC: 10487758. DOI: 10.3390/ijms241713105. View

Robles L, Wampole J, Christians M, Larsen P . Arabidopsis enhanced ethylene response 4 encodes an EIN3-interacting TFIID transcription factor required for proper ethylene response, including ERF1 induction. J Exp Bot. 2007; 58(10):2627-39. DOI: 10.1093/jxb/erm080. View

Ko D, Brandizzi F . Advanced genomics identifies growth effectors for proteotoxic ER stress recovery in Arabidopsis thaliana. Commun Biol. 2022; 5(1):16. PMC: 8752741. DOI: 10.1038/s42003-021-02964-8. View

Crosti P, Malerba M, Bianchetti R . Tunicamycin and Brefeldin A induce in plant cells a programmed cell death showing apoptotic features. Protoplasma. 2001; 216(1-2):31-8. DOI: 10.1007/BF02680128. View

10.

Eulgem T . Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci. 2005; 10(2):71-8. DOI: 10.1016/j.tplants.2004.12.006. View

11.

Zhang S, Yang H, Ding L, Song Z, Ma H, Chang F . Tissue-Specific Transcriptomics Reveals an Important Role of the Unfolded Protein Response in Maintaining Fertility upon Heat Stress in Arabidopsis. Plant Cell. 2017; 29(5):1007-1023. PMC: 5466030. DOI: 10.1105/tpc.16.00916. View

12.

Yamada K, Lim J, Dale J, Chen H, Shinn P, Palm C . Empirical analysis of transcriptional activity in the Arabidopsis genome. Science. 2003; 302(5646):842-6. DOI: 10.1126/science.1088305. View

13.

Kim J, Sakamoto Y, Takahashi F, Shibata M, Urano K, Matsunaga S . TBP-ASSOCIATED FACTOR 12 ortholog NOBIRO6 controls root elongation with unfolded protein response cofactor activity. Proc Natl Acad Sci U S A. 2022; 119(6). PMC: 8833210. DOI: 10.1073/pnas.2120219119. View

14.

Martinez I, Chrispeels M . Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell. 2003; 15(2):561-76. PMC: 141221. DOI: 10.1105/tpc.007609. View

15.

Howell S . Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol. 2013; 64:477-99. DOI: 10.1146/annurev-arplant-050312-120053. View

16.

Moreno A, Mukhtar M, Blanco F, Boatwright J, Moreno I, Jordan M . IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLoS One. 2012; 7(2):e31944. PMC: 3281089. DOI: 10.1371/journal.pone.0031944. View

17.

Liu J, Srivastava R, Howell S . Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress in Arabidopsis. Plant Cell Environ. 2008; 31(12):1735-43. DOI: 10.1111/j.1365-3040.2008.01873.x. View

18.

Srivastava R, Li Z, Russo G, Tang J, Bi R, Muppirala U . Response to Persistent ER Stress in Plants: A Multiphasic Process That Transitions Cells from Prosurvival Activities to Cell Death. Plant Cell. 2018; 30(6):1220-1242. PMC: 6048783. DOI: 10.1105/tpc.18.00153. View

19.

Liu J, Srivastava R, Che P, Howell S . An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell. 2007; 19(12):4111-9. PMC: 2217655. DOI: 10.1105/tpc.106.050021. View

20.

Skubacz A, Daszkowska-Golec A, Szarejko I . The Role and Regulation of ABI5 (ABA-Insensitive 5) in Plant Development, Abiotic Stress Responses and Phytohormone Crosstalk. Front Plant Sci. 2016; 7:1884. PMC: 5159420. DOI: 10.3389/fpls.2016.01884. View