Seed longevity is controlled by metacaspases

Liu, Chen, Hatzianestis, Ioannis H., Pfirrmann, Thorsten, Reza, Salim H., Minina, Elena A., Moazzami, Ali, Stael, Simon, Gutierrez–Beltran, Emilio, Pitsili, Eugenia, Dörmann, Peter, D’Andrea, Sabine, Gevaert, Kris, Romero–Campero, Francisco, Ding, Pingtao, Nowack, Moritz K., Van Breusegem, Frank, Jones, Jonathan D. G., Bozhkov, Peter V. and Moschou, Panagiotis N. (2024) Seed longevity is controlled by metacaspases. Nature Communications, 15 (1). ISSN 2041-1723

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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.

Item Type:	Article
Additional Information:	Data availability statement: All data, code, and materials used in the analysis are available and were deposited in public repositories. Gene sequence information of MCAs is provided in Supplementary Data 1 and 12. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifiers PXD048890 and PXD049287. The processed data are available online at https://zenodo.org/records/12684164. The raw RNAseq data of this article have been deposited to the BioStudies database with the dataset accession number S-BSST1310. Source data are provided with this paper. Funding information: This work received funding from the Knut and Alice Wallenberg Foundation 2018.0026 (PVB, PNM); EPIC–XS, Horizon 2020 programme of the European Union project number 823839 (KG, PNM); European Research Council (ERC) Starting Grant ‘R–ELEVATION’ 101039824 (P Ding); European Research Council (ERC) Consolidator Grant PLANTEX, 101126019, 10.3030/101126019 (PNM); Future Leader Fellowship from the Biotechnology and Biological Sciences Research Council (BBSRC) BB/R012172/1 (P Ding); European Union and Greek national funds through the Operational Program Competitiveness, Entrepreneurship, and Innovation, Τ2ΕΔΚ–00597 under the call RESEARCH–CREATE–INNOVATE “BIOME” (PNM); European Union Horizon 2020 Marie Curie–RISE Grant PANTHEON 872969 (PNM); Hellenic Foundation of Research and Innovation Grant–Theodoros Papazoglou–Always Strive for Excellence NESTOR 1426 (PNM); Hellenic Foundation of Research and Innovation Fellowship 5947 (IHH); The Swedish Research Council (VR) 2019–04250 (PVB, PNM); Carl Trygger Foundation (CTS) 22:2025 (PVB); European Union Marie Skłodowska–Curie Action IF project 656011 (PNM); DESTINY (BOF–UGent) (SS, FVB). Views and opinions expressed are those of the author(s) only and do not necessarily reflect those of the European Union or the European Research Council Executive Agency. Neither the European Union nor the granting authority can be held responsible for them. Open access funding provided by Swedish University of Agricultural Sciences.
Uncontrolled Keywords:	chemistry(all),biochemistry, genetics and molecular biology(all),physics and astronomy(all) ,/dk/atira/pure/subjectarea/asjc/1600
Faculty \ School:	Faculty of Science > School of Biological Sciences
UEA Research Groups:	Faculty of Science > Research Groups > Plant Sciences
Related URLs:	http://www.scopus.com/inward/record.url?...
Depositing User:	LivePure Connector
Date Deposited:	23 Oct 2024 10:30
Last Modified:	25 Oct 2024 15:30
URI:	https://ueaeprints.uea.ac.uk/id/eprint/97138
DOI:	10.1038/s41467-024-50848-2

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