An IRE1-proteasome system signalling cohort controls cell fate determination in unresolved proteotoxic stress of the plant endoplasmic reticulum

Ko, Dae Kwan; Kim, Joo Yong; Thibault, Ethan A.; Brandizzi, Federica

doi:10.1038/s41477-023-01480-3

An IRE1-proteasome system signalling cohort controls cell fate determination in unresolved proteotoxic stress of the plant endoplasmic reticulum

Journal Article · Thu Aug 10 00:00:00 EDT 2023 · Nature Plants (Online)

DOI:https://doi.org/10.1038/s41477-023-01480-3· OSTI ID:2202447

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

Excessive accumulation of misfolded proteins in the endoplasmic reticulum (ER) causes ER stress, which is an underlying cause of major crop losses and devastating human conditions. Here, ER proteostasis surveillance is mediated by the conserved master regulator of the unfolded protein response (UPR), Inositol Requiring Enzyme 1 (IRE1), which determines cell fate by controlling pro-life and pro-death outcomes through as yet largely unknown mechanisms. Here we report that Arabidopsis IRE1 determines cell fate in ER stress by balancing the ubiquitin–proteasome system (UPS) and UPR through the plant-unique E3 ligase, PHOSPHATASE TYPE 2CA (PP2CA)-INTERACTING RING FINGER PROTEIN 1 (PIR1). Indeed, PIR1 loss leads to suppression of pro-death UPS and the lethal phenotype of an IRE1 loss-of-function mutant in unresolved ER stress in addition to activating pro-survival UPR. Specifically, in ER stress, PIR1 loss stabilizes ABI5, a basic leucine zipper (bZIP) transcription factor, that directly activates expression of the critical UPR regulator gene, bZIP60, triggering transcriptional cascades enhancing pro-survival UPR. Collectively, our results identify new cell fate effectors in plant ER stress by showing that IRE1’s coordination of cell death and survival hinges on PIR1, a key pro-death component of the UPS, which controls ABI5, a pro-survival transcriptional activator of bZIP60.

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Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Michigan State University, East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: FG02-91ER20021; SC0018409

OSTI ID:: 2202447

Journal Information:: Nature Plants (Online), Journal Name: Nature Plants (Online) Journal Issue: 8 Vol. 9; ISSN 2055-0278

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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An IRE1-proteasome system signalling cohort controls cell fate determination in unresolved proteotoxic stress of the plant endoplasmic reticulum

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