ATG8 delipidation is not universally critical for autophagy in plants

Abstract Intracellular recycling via autophagy is governed by post-translational modifications of the autophagy-related (ATG) proteins. One notable example is ATG4-dependent delipidation of ATG8, a process that plays critical but distinct roles in autophagosome formation in yeast and mammals. Here,...

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Main Authors: Yong Zou, Jonas A. Ohlsson, Sanjana Holla, Igor Sabljić, Jia Xuan Leong, Florentine Ballhaus, Melanie Krebs, Karin Schumacher, Panagiotis N. Moschou, Simon Stael, Suayib Üstün, Yasin Dagdas, Peter V. Bozhkov, Elena A. Minina
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55754-1
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author Yong Zou
Jonas A. Ohlsson
Sanjana Holla
Igor Sabljić
Jia Xuan Leong
Florentine Ballhaus
Melanie Krebs
Karin Schumacher
Panagiotis N. Moschou
Simon Stael
Suayib Üstün
Yasin Dagdas
Peter V. Bozhkov
Elena A. Minina
author_facet Yong Zou
Jonas A. Ohlsson
Sanjana Holla
Igor Sabljić
Jia Xuan Leong
Florentine Ballhaus
Melanie Krebs
Karin Schumacher
Panagiotis N. Moschou
Simon Stael
Suayib Üstün
Yasin Dagdas
Peter V. Bozhkov
Elena A. Minina
author_sort Yong Zou
collection DOAJ
description Abstract Intracellular recycling via autophagy is governed by post-translational modifications of the autophagy-related (ATG) proteins. One notable example is ATG4-dependent delipidation of ATG8, a process that plays critical but distinct roles in autophagosome formation in yeast and mammals. Here, we aim to elucidate the specific contribution of this process to autophagosome formation in species representative of evolutionarily distant green plant lineages: unicellular green alga Chlamydomonas reinhardtii, with a relatively simple set of ATG genes, and a vascular plant Arabidopsis thaliana, harboring expanded ATG gene families. Remarkably, the more complex autophagy machinery of Arabidopsis renders ATG8 delipidation entirely dispensable for the maturation of autophagosomes, autophagic flux, and related stress tolerance; whereas autophagy in Chlamydomonas strictly depends on the ATG4-mediated delipidation of ATG8. Importantly, we also demonstrate the distinct impact of different Arabidopsis ATG8 orthologs on autophagosome formation, especially prevalent under nitrogen depletion, providing new insight into potential drivers behind the expansion of the ATG8 family in higher plants. Our findings underscore the evolutionary diversification of the molecular mechanism governing the maturation of autophagosomes in eukaryotic lineages and highlight how this conserved pathway is tailored to diverse organisms.
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spelling doaj-art-8b7bf3c12c3743e28a86aabea904a5192025-01-12T12:30:28ZengNature PortfolioNature Communications2041-17232025-01-0116111910.1038/s41467-024-55754-1ATG8 delipidation is not universally critical for autophagy in plantsYong Zou0Jonas A. Ohlsson1Sanjana Holla2Igor Sabljić3Jia Xuan Leong4Florentine Ballhaus5Melanie Krebs6Karin Schumacher7Panagiotis N. Moschou8Simon Stael9Suayib Üstün10Yasin Dagdas11Peter V. Bozhkov12Elena A. Minina13Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant BiologyDepartment of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant BiologyDepartment of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant BiologyDepartment of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant BiologyDepartment of Algal Development and Evolution, Max Planck Institute for Biology TübingenDepartment of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant BiologyCentre for Organismal Studies (COS), Heidelberg UniversityCentre for Organismal Studies (COS), Heidelberg UniversityDepartment of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant BiologyDepartment of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant BiologyFaculty of Biology and Biotechnology, Ruhr-University BochumGregor Mendel Institute of Molecular Plant Biology, Austrian Academy of SciencesDepartment of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant BiologyDepartment of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant BiologyAbstract Intracellular recycling via autophagy is governed by post-translational modifications of the autophagy-related (ATG) proteins. One notable example is ATG4-dependent delipidation of ATG8, a process that plays critical but distinct roles in autophagosome formation in yeast and mammals. Here, we aim to elucidate the specific contribution of this process to autophagosome formation in species representative of evolutionarily distant green plant lineages: unicellular green alga Chlamydomonas reinhardtii, with a relatively simple set of ATG genes, and a vascular plant Arabidopsis thaliana, harboring expanded ATG gene families. Remarkably, the more complex autophagy machinery of Arabidopsis renders ATG8 delipidation entirely dispensable for the maturation of autophagosomes, autophagic flux, and related stress tolerance; whereas autophagy in Chlamydomonas strictly depends on the ATG4-mediated delipidation of ATG8. Importantly, we also demonstrate the distinct impact of different Arabidopsis ATG8 orthologs on autophagosome formation, especially prevalent under nitrogen depletion, providing new insight into potential drivers behind the expansion of the ATG8 family in higher plants. Our findings underscore the evolutionary diversification of the molecular mechanism governing the maturation of autophagosomes in eukaryotic lineages and highlight how this conserved pathway is tailored to diverse organisms.https://doi.org/10.1038/s41467-024-55754-1
spellingShingle Yong Zou
Jonas A. Ohlsson
Sanjana Holla
Igor Sabljić
Jia Xuan Leong
Florentine Ballhaus
Melanie Krebs
Karin Schumacher
Panagiotis N. Moschou
Simon Stael
Suayib Üstün
Yasin Dagdas
Peter V. Bozhkov
Elena A. Minina
ATG8 delipidation is not universally critical for autophagy in plants
Nature Communications
title ATG8 delipidation is not universally critical for autophagy in plants
title_full ATG8 delipidation is not universally critical for autophagy in plants
title_fullStr ATG8 delipidation is not universally critical for autophagy in plants
title_full_unstemmed ATG8 delipidation is not universally critical for autophagy in plants
title_short ATG8 delipidation is not universally critical for autophagy in plants
title_sort atg8 delipidation is not universally critical for autophagy in plants
url https://doi.org/10.1038/s41467-024-55754-1
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