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Dynamics of ER stress-induced gene regulation in plants

Nature Reviews Genetics (2024)Cite this article

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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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Fig. 1: The ER stress response in plants versus metazoans.
Fig. 2: Historical timeline of plant UPR research.
Fig. 3: Transcriptional coregulation of bZIP28 and bZIP60 in response to various stress conditions.
Fig. 4: Experimental designs for analysing responses to ER stress in Arabidopsis.
Fig. 5: A schematic model for gene regulation in plant UPR.

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Acknowledgements

The authors’ work is supported by the National Institutes of Health (R35GM136637) with contributing support from the Great Lakes Bioenergy Research Center, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research (DE-SC0018409), Chemical Sciences, Geoscience and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U.S. Department of Energy (DE-FG02-91ER20021), and MSU AgBioResearch (MICL02598).

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Authors and Affiliations

  1. MSU-DOE Plant Research Lab, Michigan State University, East Lansing, MI, USA

    Dae Kwan Ko & Federica Brandizzi

  2. Department of Plant Biology, Michigan State University, East Lansing, MI, USA

    Dae Kwan Ko & Federica Brandizzi

  3. Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, USA

    Dae Kwan Ko & Federica Brandizzi

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  1. Dae Kwan Ko
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D.K.K. wrote the initial draft of the article. Both authors researched the literature, substantially discussed the content, and reviewed and/or edited the manuscript before submission.

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Glossary

Abscisic acid

A plant hormone that regulates numerous biological pathways, including growth, development and responses to environmental stress.

Chaperone

A group of functionally related proteins that facilitate and regulate polypeptide folding within cells, including the highly conserved heat shock protein 70 (HSP70), which is present in all cellular compartments.

Chromatin immunoprecipitation followed by sequencing

(ChIP–seq). The most popular in vivo technique to identify DNA sequences bound by a transcription factor of interest at genome scale.

DNA microarray

A technology utilizing over 20,000 DNA probes attached to a surface, which are hybridized with cDNA (reverse-transcribed from mRNA using reverse transcriptase), enabling simultaneous measurement of expression levels of numerous genes.

Endoplasmic reticulum

(ER). A cellular organelle composed of a membranous tubule network involved in the synthesis of protein and lipids and the export of secreted proteins.

ER-associated protein degradation

A cellular pathway that eliminates misfolded proteins in the ER via ubiquitination followed by degradation by a protein-degradation complex known as the proteasome.

ER-phagy

A mechanism that degrades portions of the ER in response to an excessive accumulation of misfolded proteins.

Foldase

A particular set of molecular chaperones that facilitate the non-covalent folding of proteins in an ATP-dependent manner.

Golgi apparatus

A cellular organelle where proteins and lipids are modified, packaged and transported to target destinations.

Nuclear localization signal

An amino acid sequence that serves as a ‘tag’ for directing a protein into the nucleus through nuclear transport.

Plasmodesmata

Small channels that connect plant cells to each other, providing living tubes between cells.

Salicylic acid

A plant hormone that is crucial for triggering plant defence against both biotic and abiotic stresses, using morphological, physiological and biochemical mechanisms.

Tunicamycin

A mixture of four homologous nucleoside antibiotics that inhibits N-linked glycosylation in the ER, thus disrupting protein folding and maturation.

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Ko, D.K., Brandizzi, F. Dynamics of ER stress-induced gene regulation in plants. Nat Rev Genet (2024). https://doi.org/10.1038/s41576-024-00710-4

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