Plant autophagosomes mature into amphisomes prior to their delivery to the central vacuole
Zhao J, Bui MT, Ma J, Künzl F, Picchianti L, De La Concepcion JC, Chen Y, Petsangouraki S, Mohseni A, García-Leon M, Gomez MS, Giannini C, Gwennogan D, Kobylinska R, Clavel M, Schellmann S, Jaillais Y, Friml J, Kang B-H, Dagdas Y. 2022. Plant autophagosomes mature into amphisomes prior to their delivery to the central vacuole. Journal of Cell Biology. 221(12), e202203139.
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Author
Zhao, Jierui;
Bui, Mai Thu;
Ma, Juncai;
Künzl, Fabian;
Picchianti, Lorenzo;
De La Concepcion, Juan Carlos;
Chen, Yixuan;
Petsangouraki, Sofia;
Mohseni, Azadeh;
García-Leon, Marta;
Gomez, Marta Salas;
Giannini, CaterinaISTA
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All
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Abstract
Autophagosomes are double-membraned vesicles that traffic harmful or unwanted cellular macromolecules to the vacuole for recycling. Although autophagosome biogenesis has been extensively studied, autophagosome maturation, i.e., delivery and fusion with the vacuole, remains largely unknown in plants. Here, we have identified an autophagy adaptor, CFS1, that directly interacts with the autophagosome marker ATG8 and localizes on both membranes of the autophagosome. Autophagosomes form normally in Arabidopsis thaliana cfs1 mutants, but their delivery to the vacuole is disrupted. CFS1’s function is evolutionarily conserved in plants, as it also localizes to the autophagosomes and plays a role in autophagic flux in the liverwort Marchantia polymorpha. CFS1 regulates autophagic flux by bridging autophagosomes with the multivesicular body-localized ESCRT-I component VPS23A, leading to the formation of amphisomes. Similar to CFS1-ATG8 interaction, disrupting the CFS1-VPS23A interaction blocks autophagic flux and renders plants sensitive to nitrogen starvation. Altogether, our results reveal a conserved vacuolar sorting hub that regulates autophagic flux in plants.
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Publishing Year
Date Published
2022-12-01
Journal Title
Journal of Cell Biology
Acknowledgement
We thank Suayip Ustün, Karin Schumacher, Erika Isono, Gerd Juergens, Takashi Ueda, Daniel Hofius, and Liwen Jiang for sharing published materials.
We acknowledge funding from Austrian Academy of Sciences, Austrian Science Fund (FWF, P 32355, P 34944), Austrian Science Fund (FWF-SFB F79), Vienna Science and Technology
Fund (WWTF, LS17-047) to Y. Dagdas; Austrian Academy of Sciences DOC Fellowship to J. Zhao, Marie Curie VIP2 Fellowship to J.C. De La Concepcion and M. Clavel; Hong Kong Research Grant Council (GRF14121019, 14113921, AoE/M-05/12, C4002-17G) to B.-H. Kang. We thank Vienna Biocenter Core Facilities (VBCF) Protein Chemistry, Biooptics, Plant Sciences, Molecular Biology, and Protein Technologies. We thank J. Matthew Watson
and members of the Dagdas lab for the critical reading and editing of the manuscript.
Volume
221
Issue
12
Article Number
e202203139
ISSN
eISSN
IST-REx-ID
Cite this
Zhao J, Bui MT, Ma J, et al. Plant autophagosomes mature into amphisomes prior to their delivery to the central vacuole. Journal of Cell Biology. 2022;221(12). doi:10.1083/jcb.202203139
Zhao, J., Bui, M. T., Ma, J., Künzl, F., Picchianti, L., De La Concepcion, J. C., … Dagdas, Y. (2022). Plant autophagosomes mature into amphisomes prior to their delivery to the central vacuole. Journal of Cell Biology. Rockefeller University Press. https://doi.org/10.1083/jcb.202203139
Zhao, Jierui, Mai Thu Bui, Juncai Ma, Fabian Künzl, Lorenzo Picchianti, Juan Carlos De La Concepcion, Yixuan Chen, et al. “Plant Autophagosomes Mature into Amphisomes Prior to Their Delivery to the Central Vacuole.” Journal of Cell Biology. Rockefeller University Press, 2022. https://doi.org/10.1083/jcb.202203139.
J. Zhao et al., “Plant autophagosomes mature into amphisomes prior to their delivery to the central vacuole,” Journal of Cell Biology, vol. 221, no. 12. Rockefeller University Press, 2022.
Zhao J, Bui MT, Ma J, Künzl F, Picchianti L, De La Concepcion JC, Chen Y, Petsangouraki S, Mohseni A, García-Leon M, Gomez MS, Giannini C, Gwennogan D, Kobylinska R, Clavel M, Schellmann S, Jaillais Y, Friml J, Kang B-H, Dagdas Y. 2022. Plant autophagosomes mature into amphisomes prior to their delivery to the central vacuole. Journal of Cell Biology. 221(12), e202203139.
Zhao, Jierui, et al. “Plant Autophagosomes Mature into Amphisomes Prior to Their Delivery to the Central Vacuole.” Journal of Cell Biology, vol. 221, no. 12, e202203139, Rockefeller University Press, 2022, doi:10.1083/jcb.202203139.
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