Seed longevity is controlled by metacaspases
Nature Communications, vol. 15, pp. 6748
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.
Authors 19
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University of Crete · Sun Yat-sen University · Swedish University of Agricultural Sciences · Foundation for Research and Technology Hellas
Affiliation as printed
Department of Biology, University of Crete, 71500, Heraklion, Greece
Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden
Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, 71500, Heraklion, Greece
State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, 510275, Guangzhou, China
State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat–Sen University, 510275, Guangzhou, China
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University of Crete · Foundation for Research and Technology Hellas
Affiliation as printed
Department of Biology, University of Crete, 71500, Heraklion, Greece
Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, 71500, Heraklion, Greece
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University of Potsdam · HMU Health and Medical University
Affiliation as printed
Department of Medicine, Health and Medical University, 14471, Potsdam, Germany
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Affiliation as printed
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
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Swedish University of Agricultural Sciences
Affiliation as printed
Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden
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Swedish University of Agricultural Sciences
Affiliation as printed
Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden
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Swedish University of Agricultural Sciences · Ghent University · VIB-UGent Center for Plant Systems Biology
Affiliation as printed
Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052, Ghent, Belgium
VIB-Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium
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Consejo Superior de Investigaciones Científicas · Instituto de Bioquímica Vegetal y Fotosíntesis · Universidad de Sevilla
Affiliation as printed
Departamento de Bioquımica Vegetal y Biologıa Molecular, Facultad de Biologıa, Universidad de Sevilla, 41012, Sevilla, Spain
Instituto de Bioquımica Vegetal y Fotosıntesis, Consejo Superior de Investigaciones Cientıficas (CSIC)–Universidad de Sevilla, 41092, Sevilla, Spain
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Ghent University · VIB-UGent Center for Plant Systems Biology
Affiliation as printed
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052, Ghent, Belgium
VIB-Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium
VIB–Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium
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Affiliation as printed
University of Bonn, Institute of Molecular Physiology and Biotechnology of Plants (IMBIO), Karlrobert Kreiten Straße 13, 53115, Bonn, Germany
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AgroParisTech · Université Paris-Saclay · Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · Institut Jean-Pierre Bourgin
Affiliation as printed
Université Paris–Saclay, INRAE, AgroParisTech, Institut Jean–Pierre Bourgin (IJPB), 78000, Versailles, France
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Ghent University · VIB-UGent Center for Medical Biotechnology
Affiliation as printed
Department of Biomolecular Medicine, Ghent University, Technologiepark-Zwijnaarde 75, B9052, Ghent, Belgium
VIB Center for Medical Biotechnology, Technologiepark-Zwijnaarde 75, B9052, Ghent, Belgium
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Consejo Superior de Investigaciones Científicas · Instituto de Bioquímica Vegetal y Fotosíntesis · Universidad de Sevilla
Affiliation as printed
Instituto de Bioquımica Vegetal y Fotosıntesis, Consejo Superior de Investigaciones Cientıficas (CSIC)–Universidad de Sevilla, 41092, Sevilla, Spain
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Affiliation as printed
Institute of Biology Leiden, Leiden University, 2333 BE, Leiden, The Netherlands
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Ghent University · VIB-UGent Center for Plant Systems Biology
Affiliation as printed
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052, Ghent, Belgium
VIB-Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium
VIB–Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium
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Ghent University · VIB-UGent Center for Plant Systems Biology
Affiliation as printed
Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052, Ghent, Belgium
VIB-Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium
VIB–Ugent Center for Plant Systems Biology, Technologiepark 71, 9052, Ghent, Belgium
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University of East Anglia · Sainsbury Laboratory
Affiliation as printed
The Sainsbury Laboratory, University of East Anglia, Colney Lane, NR47UH, Norwich, UK
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Swedish University of Agricultural Sciences
Affiliation as printed
Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007, Uppsala, Sweden
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Panagiotis N. Moschou corresponding
University of Crete · Swedish University of Agricultural Sciences · FORTH Institute of Molecular Biology and Biotechnology · Foundation for Research and Technology Hellas
Affiliation as printed
Department of Biology, University of Crete, 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
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
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