Seed longevity is controlled by metacaspases.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
08 Aug 2024
Historique:
received: 19 04 2023
accepted: 23 07 2024
medline: 9 8 2024
pubmed: 9 8 2024
entrez: 8 8 2024
Statut: epublish

Résumé

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.

Identifiants

pubmed: 39117606
doi: 10.1038/s41467-024-50848-2
pii: 10.1038/s41467-024-50848-2
doi:

Substances chimiques

Arabidopsis Proteins 0
Valosin Containing Protein EC 3.6.4.6

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

6748

Subventions

Organisme : Knut och Alice Wallenbergs Stiftelse (Knut and Alice Wallenberg Foundation)
ID : 2018.0026
Organisme : Knut och Alice Wallenbergs Stiftelse (Knut and Alice Wallenberg Foundation)
ID : 2018.0026
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 101039824
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 101126019
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/R012172/1
Organisme : EC | Horizon 2020 Framework Programme (EU Framework Programme for Research and Innovation H2020)
ID : 872969
Organisme : Vetenskapsrådet (Swedish Research Council)
ID : 2019-04250
Organisme : Vetenskapsrådet (Swedish Research Council)
ID : 2019-04250
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 Marie Skłodowska-Curie Actions (H2020 Excellent Science - Marie Skłodowska-Curie Actions)
ID : 656011
Organisme : Carl Tryggers Stiftelse för Vetenskaplig Forskning (Carl Trygger Foundation)
ID : 22:2025

Informations de copyright

© 2024. The Author(s).

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Auteurs

Chen Liu (C)

State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, 510275, Guangzhou, China.
Department of Biology, University of Crete, 71500, Heraklion, Greece.
Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, 71500, Heraklion, Greece.
Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden.

Ioannis H Hatzianestis (IH)

Department of Biology, University of Crete, 71500, Heraklion, Greece.
Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, 71500, Heraklion, Greece.

Thorsten Pfirrmann (T)

Department of Medicine, Health and Medical University, 14471, Potsdam, Germany.

Salim H Reza (SH)

Plant Ecology and Evolution, Department of Ecology and Genetics, Evolutionary Biology Centre and the Linnean Centre for Plant Biology in Uppsala, Uppsala University, 75236, Uppsala, Sweden.

Elena A Minina (EA)

Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden.

Ali Moazzami (A)

Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden.

Simon Stael (S)

Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden.
VIB-Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium.
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052, Ghent, Belgium.

Emilio Gutierrez-Beltran (E)

Instituto de Bioquımica Vegetal y Fotosıntesis, Consejo Superior de Investigaciones Cientıficas (CSIC)-Universidad de Sevilla, 41092, Sevilla, Spain.
Departamento de Bioquımica Vegetal y Biologıa Molecular, Facultad de Biologıa, Universidad de Sevilla, 41012, Sevilla, Spain.

Eugenia Pitsili (E)

VIB-Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium.
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052, Ghent, Belgium.

Peter Dörmann (P)

University of Bonn, Institute of Molecular Physiology and Biotechnology of Plants (IMBIO), Karlrobert Kreiten Straße 13, 53115, Bonn, Germany.

Sabine D'Andrea (S)

Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France.

Kris Gevaert (K)

VIB Center for Medical Biotechnology, Technologiepark-Zwijnaarde 75, B9052, Ghent, Belgium.
Department of Biomolecular Medicine, Ghent University, Technologiepark-Zwijnaarde 75, B9052, Ghent, Belgium.

Francisco Romero-Campero (F)

Instituto de Bioquımica Vegetal y Fotosıntesis, Consejo Superior de Investigaciones Cientıficas (CSIC)-Universidad de Sevilla, 41092, Sevilla, Spain.

Pingtao Ding (P)

Institute of Biology Leiden, Leiden University, 2333 BE, Leiden, The Netherlands.

Moritz K Nowack (MK)

VIB-Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium.
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052, Ghent, Belgium.

Frank Van Breusegem (F)

VIB-Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium.
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052, Ghent, Belgium.

Jonathan D G Jones (JDG)

The Sainsbury Laboratory, University of East Anglia, Colney Lane, NR47UH, Norwich, UK.

Peter V Bozhkov (PV)

Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden.

Panagiotis N Moschou (PN)

Department of Biology, University of Crete, 71500, Heraklion, Greece. Panagiotis.moschou@uoc.gr.
Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, 71500, Heraklion, Greece. Panagiotis.moschou@uoc.gr.
Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden. Panagiotis.moschou@uoc.gr.

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