Autophagy is a conserved eukaryotic lysosomal degradation pathway that responds to environmental and cellular cues. Autophagy is essential for the meiotic exit and sporulation in budding yeast, but the underlying molecular mechanisms remain unknown. Here, we show that autophagy is maintained during meiosis and stimulated in anaphase I and II. Cells with higher levels of autophagy complete meiosis faster, and genetically enhanced autophagy increases meiotic kinetics and sporulation efficiency. Strikingly, our data reveal that the conserved phosphatase Cdc14 regulates meiosis-specific autophagy. Cdc14 is activated in anaphase I and II, accompanying its subcellular relocation from the nucleolus to the cytoplasm, where it dephosphorylates Atg13 to stimulate Atg1 kinase activity and thus autophagy. Together, our findings reveal a meiosis-tailored mechanism that spatiotemporally controls meiotic autophagy activity to ensure meiosis progression, exit, and sporulation.
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2 May 2022
Article|
March 03 2022
Cdc14 spatiotemporally dephosphorylates Atg13 to activate autophagy during meiotic divisions
Wenzhi Feng
,
Wenzhi Feng
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
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Orlando Argüello-Miranda
,
Orlando Argüello-Miranda
2
Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC
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Suhong Qian
,
Suhong Qian
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
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Fei Wang
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
Correspondence to Fei Wang: Fei.Wang@UTsouthwestern.edu
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Wenzhi Feng
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
Orlando Argüello-Miranda
2
Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC
Suhong Qian
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
Correspondence to Fei Wang: Fei.Wang@UTsouthwestern.edu
Received:
July 26 2021
Revision Received:
January 07 2022
Accepted:
February 03 2022
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding
Funder(s):
National Institutes of Health
- Award Id(s): R01GM133899,K99GM135487
Funder(s):
Welch Foundation
- Award Id(s): I-2019-20190330
Funder(s):
Nancy Cain and Jeffrey A. Marcus Scholar in Medical Research
© 2022 Feng et al.
2022
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2022) 221 (5): e202107151.
Article history
Received:
July 26 2021
Revision Received:
January 07 2022
Accepted:
February 03 2022
Citation
Wenzhi Feng, Orlando Argüello-Miranda, Suhong Qian, Fei Wang; Cdc14 spatiotemporally dephosphorylates Atg13 to activate autophagy during meiotic divisions. J Cell Biol 2 May 2022; 221 (5): e202107151. doi: https://doi.org/10.1083/jcb.202107151
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