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Programmed cell death regulator BAP2 is required for IRE1-mediated unfolded protein response in Arabidopsis

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Listed:
  • Noelia Pastor-Cantizano

    (Michigan State University
    University of Valencia)

  • Evan R. Angelos

    (Michigan State University
    University of California Riverside)

  • Cristina Ruberti

    (Michigan State University
    University of Milan)

  • Tao Jiang

    (Michigan State University
    University of Florida)

  • Xiaoyu Weng

    (University of Texas)

  • Brandon C. Reagan

    (Michigan State University)

  • Taslima Haque

    (University of Texas
    University of Michigan)

  • Thomas E. Juenger

    (University of Texas)

  • Federica Brandizzi

    (Michigan State University
    Michigan State University
    Michigan State University)

Abstract

Environmental and physiological situations can challenge the balance between protein synthesis and folding capacity of the endoplasmic reticulum (ER) and cause ER stress, a potentially lethal condition. The unfolded protein response (UPR) restores ER homeostasis or actuates programmed cell death (PCD) when ER stress is unresolved. The cell fate determination mechanisms of the UPR are not well understood, especially in plants. Here, we integrate genetics and ER stress profiling with natural variation and quantitative trait locus analysis of 350 natural accessions of the model species Arabidopsis thaliana. Our analyses implicate a single nucleotide polymorphism to the loss of function of the general PCD regulator BON-ASSOCIATED PROTEIN2 (BAP2) in UPR outcomes. We establish that ER stress-induced BAP2 expression is antagonistically regulated by the UPR master regulator, inositol-requiring enzyme 1 (IRE1), and that BAP2 controls adaptive UPR amplitude in ER stress and ignites pro-death mechanisms in conditions of UPR insufficiency.

Suggested Citation

  • Noelia Pastor-Cantizano & Evan R. Angelos & Cristina Ruberti & Tao Jiang & Xiaoyu Weng & Brandon C. Reagan & Taslima Haque & Thomas E. Juenger & Federica Brandizzi, 2024. "Programmed cell death regulator BAP2 is required for IRE1-mediated unfolded protein response in Arabidopsis," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50105-6
    DOI: 10.1038/s41467-024-50105-6
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    References listed on IDEAS

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    1. Heather P. Harding & Yuhong Zhang & David Ron, 1999. "Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase," Nature, Nature, vol. 397(6716), pages 271-274, January.
    2. Luciana Renna & Giovanni Stefano & Erin Slabaugh & Clarissa Wormsbaecher & Alan Sulpizio & Krzysztof Zienkiewicz & Federica Brandizzi, 2018. "TGNap1 is required for microtubule-dependent homeostasis of a subpopulation of the plant trans-Golgi network," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    3. Mary C. Wildermuth & Julia Dewdney & Gang Wu & Frederick M. Ausubel, 2001. "Isochorismate synthase is required to synthesize salicylic acid for plant defence," Nature, Nature, vol. 414(6863), pages 562-565, November.
    4. Marcella Calfon & Huiqing Zeng & Fumihiko Urano & Jeffery H. Till & Stevan R. Hubbard & Heather P. Harding & Scott G. Clark & David Ron, 2002. "IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA," Nature, Nature, vol. 415(6867), pages 92-96, January.
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