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Seed longevity is controlled by metacaspases

Author

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  • Chen Liu

    (Sun Yat–Sen University
    University of Crete
    Foundation for Research and Technology—Hellas
    Swedish University of Agricultural Sciences and Linnean Center for Plant Biology)

  • Ioannis H. Hatzianestis

    (University of Crete
    Foundation for Research and Technology—Hellas)

  • Thorsten Pfirrmann

    (Health and Medical University)

  • Salim H. Reza

    (Uppsala University)

  • Elena A. Minina

    (Swedish University of Agricultural Sciences and Linnean Center for Plant Biology)

  • Ali Moazzami

    (Swedish University of Agricultural Sciences and Linnean Center for Plant Biology)

  • Simon Stael

    (Swedish University of Agricultural Sciences and Linnean Center for Plant Biology
    Technologiepark 71
    Ghent University)

  • Emilio Gutierrez–Beltran

    (Consejo Superior de Investigaciones Cientıficas (CSIC)–Universidad de Sevilla
    Universidad de Sevilla)

  • Eugenia Pitsili

    (Technologiepark 71
    Ghent University)

  • Peter Dörmann

    (Institute of Molecular Physiology and Biotechnology of Plants (IMBIO))

  • Sabine D’Andrea

    (Institut Jean–Pierre Bourgin (IJPB))

  • Kris Gevaert

    (VIB Center for Medical Biotechnology
    Ghent University)

  • Francisco Romero–Campero

    (Consejo Superior de Investigaciones Cientıficas (CSIC)–Universidad de Sevilla)

  • Pingtao Ding

    (Leiden University)

  • Moritz K. Nowack

    (Technologiepark 71
    Ghent University)

  • Frank Breusegem

    (Technologiepark 71
    Ghent University)

  • Jonathan D. G. Jones

    (University of East Anglia)

  • Peter V. Bozhkov

    (Swedish University of Agricultural Sciences and Linnean Center for Plant Biology)

  • Panagiotis N. Moschou

    (University of Crete
    Foundation for Research and Technology—Hellas
    Swedish University of Agricultural Sciences and Linnean Center for Plant Biology)

Abstract

To survive extreme desiccation, seeds enter a period of quiescence that can last millennia. Seed quiescence involves the accumulation of protective storage proteins and lipids through unknown adjustments in protein homeostasis (proteostasis). Here, we show that mutation of all six type–II metacaspase (MCA–II) proteases in Arabidopsis thaliana disturbs proteostasis in seeds. MCA–II mutant seeds fail to restrict the AAA ATPase CELL DIVISION CYCLE 48 (CDC48) at the endoplasmic reticulum to discard misfolded proteins, compromising seed storability. Endoplasmic reticulum (ER) localization of CDC48 relies on the MCA–IIs-dependent cleavage of PUX10 (ubiquitination regulatory X domain–containing 10), the adaptor protein responsible for titrating CDC48 to lipid droplets. PUX10 cleavage enables the shuttling of CDC48 between lipid droplets and the ER, providing an important regulatory mechanism sustaining spatiotemporal proteolysis, lipid droplet dynamics, and protein homeostasis. In turn, the removal of the PUX10 adaptor in MCA–II mutant seeds partially restores proteostasis, CDC48 localization, and lipid droplet dynamics prolonging seed lifespan. Taken together, we uncover a proteolytic module conferring seed longevity.

Suggested Citation

  • Chen Liu & Ioannis H. Hatzianestis & Thorsten Pfirrmann & Salim H. Reza & Elena A. Minina & Ali Moazzami & Simon Stael & Emilio Gutierrez–Beltran & Eugenia Pitsili & Peter Dörmann & Sabine D’Andrea & , 2024. "Seed longevity is controlled by metacaspases," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50848-2
    DOI: 10.1038/s41467-024-50848-2
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    References listed on IDEAS

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    1. Anup Arumughan & Yvette Roske & Carolin Barth & Laura Lleras Forero & Kenny Bravo-Rodriguez & Alexandra Redel & Simona Kostova & Erik McShane & Robert Opitz & Katja Faelber & Kirstin Rau & Thorsten Mi, 2016. "Quantitative interaction mapping reveals an extended UBX domain in ASPL that disrupts functional p97 hexamers," Nature Communications, Nature, vol. 7(1), pages 1-13, December.
    2. Rubina Tuladhar & Yunku Yeu & John Tyler Piazza & Zhen Tan & Jean Rene Clemenceau & Xiaofeng Wu & Quinn Barrett & Jeremiah Herbert & David H. Mathews & James Kim & Tae Hyun Hwang & Lawrence Lum, 2019. "CRISPR-Cas9-based mutagenesis frequently provokes on-target mRNA misregulation," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    3. Liangguang Lin & Congcong Zhang & Yongwu Chen & Yi Wang & Dinghe Wang & Xiaolei Liu & Muyang Wang & Juan Mao & Jianjun Zhang & Weiman Xing & Linchuan Liu & Jianming Li, 2019. "PAWH1 and PAWH2 are plant-specific components of an Arabidopsis endoplasmic reticulum-associated degradation complex," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    4. Julia Grimmer & Stefan Helm & Dirk Dobritzsch & Gerd Hause & Gerta Shema & René P. Zahedi & Sacha Baginsky, 2020. "Mild proteasomal stress improves photosynthetic performance in Arabidopsis chloroplasts," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
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