ATG8ylation of vacuolar membrane protects plants against cell wall damage

Jose Julian; Peng Gao; Alessia Del Chiaro; Juan Carlos De La Concepcion; Laia Armengot; Marc Somssich; Heloise Duverge; Marion Clavel; Nenad Grujic; Roksolana Kobylinska; Ingo Polivka; Maarten Besten; Tonni Grube Andersen; Christian Dank; Barbara Korbei; Andreas Bachmair; Nuria S. Coll; Elena A. Minina; Joris Sprakel; Yasin Dagdas

doi:10.1038/s41477-025-01907-z

ATG8ylation of vacuolar membrane protects plants against cell wall damage

Jose Julian^*, Peng Gao, Alessia Del Chiaro, Juan Carlos De La Concepcion, Laia Armengot, Marc Somssich, Heloise Duverge, Marion Clavel, Nenad Grujic, Roksolana Kobylinska, Ingo Polivka, Maarten Besten, Tonni Grube Andersen, Christian Dank, Barbara Korbei, Andreas Bachmair, Nuria S. Coll, Elena A. Minina, Joris Sprakel, Yasin Dagdas^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Vacuoles are essential for cellular metabolism and growth and the maintenance of internal turgor pressure. They sequester lytic enzymes, ions and secondary metabolites that, if leaked into the cytosol, could lead to cell death. Despite their pivotal roles, quality control pathways that safeguard vacuolar integrity have remained elusive in plants. Here we describe a conserved vacuolar quality control pathway that is activated upon cell wall damage in a turgor-pressure-dependent manner. Cell wall perturbations induce a distinct modification—ATG8ylation—on the vacuolar membrane (tonoplast) that is regulated by the V-ATPase and ATG8 conjugation machinery. Genetic disruption of tonoplast ATG8ylation impairs vacuolar integrity, leading to cell death. Together, our findings reveal a homeostatic pathway that preserves vacuolar integrity upon cell wall damage.

Original language	English
Article number	327
Pages (from-to)	321-339
Number of pages	35
Journal	Nature Plants
Volume	11
Issue number	2
Early online date	7 Feb 2025
DOIs	https://doi.org/10.1038/s41477-025-01907-z
Publication status	Published - 2025

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Julian, J., Gao, P., Del Chiaro, A., Carlos De La Concepcion, J., Armengot, L., Somssich, M., Duverge, H., Clavel, M., Grujic, N., Kobylinska, R., Polivka, I., Besten, M., Andersen, T. G., Dank, C., Korbei, B., Bachmair, A., Coll, N. S., Minina, E. A., Sprakel, J., & Dagdas, Y. (2025). ATG8ylation of vacuolar membrane protects plants against cell wall damage. Nature Plants, 11(2), 321-339. Article 327. https://doi.org/10.1038/s41477-025-01907-z

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title = "ATG8ylation of vacuolar membrane protects plants against cell wall damage",

abstract = "Vacuoles are essential for cellular metabolism and growth and the maintenance of internal turgor pressure. They sequester lytic enzymes, ions and secondary metabolites that, if leaked into the cytosol, could lead to cell death. Despite their pivotal roles, quality control pathways that safeguard vacuolar integrity have remained elusive in plants. Here we describe a conserved vacuolar quality control pathway that is activated upon cell wall damage in a turgor-pressure-dependent manner. Cell wall perturbations induce a distinct modification—ATG8ylation—on the vacuolar membrane (tonoplast) that is regulated by the V-ATPase and ATG8 conjugation machinery. Genetic disruption of tonoplast ATG8ylation impairs vacuolar integrity, leading to cell death. Together, our findings reveal a homeostatic pathway that preserves vacuolar integrity upon cell wall damage.",

author = "Jose Julian and Peng Gao and {Del Chiaro}, Alessia and {Carlos De La Concepcion}, Juan and Laia Armengot and Marc Somssich and Heloise Duverge and Marion Clavel and Nenad Grujic and Roksolana Kobylinska and Ingo Polivka and Maarten Besten and Andersen, {Tonni Grube} and Christian Dank and Barbara Korbei and Andreas Bachmair and Coll, {Nuria S.} and Minina, {Elena A.} and Joris Sprakel and Yasin Dagdas",

year = "2025",

doi = "10.1038/s41477-025-01907-z",

language = "English",

volume = "11",

pages = "321--339",

journal = "Nature Plants",

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Julian, J, Gao, P, Del Chiaro, A, Carlos De La Concepcion, J, Armengot, L, Somssich, M, Duverge, H, Clavel, M, Grujic, N, Kobylinska, R, Polivka, I, Besten, M, Andersen, TG, Dank, C, Korbei, B, Bachmair, A, Coll, NS, Minina, EA, Sprakel, J & Dagdas, Y 2025, 'ATG8ylation of vacuolar membrane protects plants against cell wall damage', Nature Plants, vol. 11, no. 2, 327, pp. 321-339. https://doi.org/10.1038/s41477-025-01907-z

TY - JOUR

T1 - ATG8ylation of vacuolar membrane protects plants against cell wall damage

AU - Julian, Jose

AU - Gao, Peng

AU - Del Chiaro, Alessia

AU - Carlos De La Concepcion, Juan

AU - Armengot, Laia

AU - Somssich, Marc

AU - Duverge, Heloise

AU - Clavel, Marion

AU - Grujic, Nenad

AU - Kobylinska, Roksolana

AU - Polivka, Ingo

AU - Besten, Maarten

AU - Andersen, Tonni Grube

AU - Dank, Christian

AU - Korbei, Barbara

AU - Bachmair, Andreas

AU - Coll, Nuria S.

AU - Minina, Elena A.

AU - Sprakel, Joris

AU - Dagdas, Yasin

PY - 2025

Y1 - 2025

N2 - Vacuoles are essential for cellular metabolism and growth and the maintenance of internal turgor pressure. They sequester lytic enzymes, ions and secondary metabolites that, if leaked into the cytosol, could lead to cell death. Despite their pivotal roles, quality control pathways that safeguard vacuolar integrity have remained elusive in plants. Here we describe a conserved vacuolar quality control pathway that is activated upon cell wall damage in a turgor-pressure-dependent manner. Cell wall perturbations induce a distinct modification—ATG8ylation—on the vacuolar membrane (tonoplast) that is regulated by the V-ATPase and ATG8 conjugation machinery. Genetic disruption of tonoplast ATG8ylation impairs vacuolar integrity, leading to cell death. Together, our findings reveal a homeostatic pathway that preserves vacuolar integrity upon cell wall damage.

AB - Vacuoles are essential for cellular metabolism and growth and the maintenance of internal turgor pressure. They sequester lytic enzymes, ions and secondary metabolites that, if leaked into the cytosol, could lead to cell death. Despite their pivotal roles, quality control pathways that safeguard vacuolar integrity have remained elusive in plants. Here we describe a conserved vacuolar quality control pathway that is activated upon cell wall damage in a turgor-pressure-dependent manner. Cell wall perturbations induce a distinct modification—ATG8ylation—on the vacuolar membrane (tonoplast) that is regulated by the V-ATPase and ATG8 conjugation machinery. Genetic disruption of tonoplast ATG8ylation impairs vacuolar integrity, leading to cell death. Together, our findings reveal a homeostatic pathway that preserves vacuolar integrity upon cell wall damage.

U2 - 10.1038/s41477-025-01907-z

DO - 10.1038/s41477-025-01907-z

M3 - Article

AN - SCOPUS:85218048219

SN - 2055-026X

VL - 11

SP - 321

EP - 339

JO - Nature Plants

JF - Nature Plants

IS - 2

M1 - 327

ER -

ATG8ylation of vacuolar membrane protects plants against cell wall damage

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