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The ubiquitin–proteasome system regulates meiotic chromosome organization

Meiotic crossover (CO) recombination is tightly regulated by chromosome architecture to ensure faithful chromosome segregation and to reshuffle alleles between parental chromosomes for genetic diversity of progeny. However, regulation of the meiotic chromosome loop/axis organization is poorly unders...

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Autores principales: Yang, Xiao, Song, Meihui, Wang, Ying, Tan, Taicong, Tian, Zhongyu, Zhai, Binyuan, Yang, Xuan, Tan, Yingjin, Cao, Yanding, Dai, Shaojun, Wang, Shunxin, Zhang, Liangran
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9169913/
https://www.ncbi.nlm.nih.gov/pubmed/35439061
http://dx.doi.org/10.1073/pnas.2106902119
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author Yang, Xiao
Song, Meihui
Wang, Ying
Tan, Taicong
Tian, Zhongyu
Zhai, Binyuan
Yang, Xuan
Tan, Yingjin
Cao, Yanding
Dai, Shaojun
Wang, Shunxin
Zhang, Liangran
author_facet Yang, Xiao
Song, Meihui
Wang, Ying
Tan, Taicong
Tian, Zhongyu
Zhai, Binyuan
Yang, Xuan
Tan, Yingjin
Cao, Yanding
Dai, Shaojun
Wang, Shunxin
Zhang, Liangran
author_sort Yang, Xiao
collection PubMed
description Meiotic crossover (CO) recombination is tightly regulated by chromosome architecture to ensure faithful chromosome segregation and to reshuffle alleles between parental chromosomes for genetic diversity of progeny. However, regulation of the meiotic chromosome loop/axis organization is poorly understood. Here, we identify a molecular pathway for axis length regulation. We show that the cohesin regulator Pds5 can interact with proteasomes. Meiosis-specific depletion of proteasomes and/or Pds5 results in a similarly shortened chromosome axis, suggesting proteasomes and Pds5 regulate axis length in the same pathway. Protein ubiquitination is accumulated in pds5 and proteasome mutants. Moreover, decreased chromosome axis length in these mutants can be largely rescued by decreasing ubiquitin availability and thus decreasing protein ubiquitination. Further investigation reveals that two ubiquitin E3 ligases, SCF (Skp–Cullin–F-box) and Ufd4, are involved in this Pds5–ubiquitin/proteasome pathway to cooperatively control chromosome axis length. These results support the hypothesis that ubiquitination of chromosome proteins results in a shortened chromosome axis, and cohesin–Pds5 recruits proteasomes onto chromosomes to regulate ubiquitination level and thus axis length. These findings reveal an unexpected role of the ubiquitin–proteasome system in meiosis and contribute to our knowledge of how Pds5 regulates meiotic chromosome organization. A conserved regulatory mechanism probably exists in higher eukaryotes.
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spelling pubmed-91699132022-10-19 The ubiquitin–proteasome system regulates meiotic chromosome organization Yang, Xiao Song, Meihui Wang, Ying Tan, Taicong Tian, Zhongyu Zhai, Binyuan Yang, Xuan Tan, Yingjin Cao, Yanding Dai, Shaojun Wang, Shunxin Zhang, Liangran Proc Natl Acad Sci U S A Biological Sciences Meiotic crossover (CO) recombination is tightly regulated by chromosome architecture to ensure faithful chromosome segregation and to reshuffle alleles between parental chromosomes for genetic diversity of progeny. However, regulation of the meiotic chromosome loop/axis organization is poorly understood. Here, we identify a molecular pathway for axis length regulation. We show that the cohesin regulator Pds5 can interact with proteasomes. Meiosis-specific depletion of proteasomes and/or Pds5 results in a similarly shortened chromosome axis, suggesting proteasomes and Pds5 regulate axis length in the same pathway. Protein ubiquitination is accumulated in pds5 and proteasome mutants. Moreover, decreased chromosome axis length in these mutants can be largely rescued by decreasing ubiquitin availability and thus decreasing protein ubiquitination. Further investigation reveals that two ubiquitin E3 ligases, SCF (Skp–Cullin–F-box) and Ufd4, are involved in this Pds5–ubiquitin/proteasome pathway to cooperatively control chromosome axis length. These results support the hypothesis that ubiquitination of chromosome proteins results in a shortened chromosome axis, and cohesin–Pds5 recruits proteasomes onto chromosomes to regulate ubiquitination level and thus axis length. These findings reveal an unexpected role of the ubiquitin–proteasome system in meiosis and contribute to our knowledge of how Pds5 regulates meiotic chromosome organization. A conserved regulatory mechanism probably exists in higher eukaryotes. National Academy of Sciences 2022-04-19 2022-04-26 /pmc/articles/PMC9169913/ /pubmed/35439061 http://dx.doi.org/10.1073/pnas.2106902119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Yang, Xiao
Song, Meihui
Wang, Ying
Tan, Taicong
Tian, Zhongyu
Zhai, Binyuan
Yang, Xuan
Tan, Yingjin
Cao, Yanding
Dai, Shaojun
Wang, Shunxin
Zhang, Liangran
The ubiquitin–proteasome system regulates meiotic chromosome organization
title The ubiquitin–proteasome system regulates meiotic chromosome organization
title_full The ubiquitin–proteasome system regulates meiotic chromosome organization
title_fullStr The ubiquitin–proteasome system regulates meiotic chromosome organization
title_full_unstemmed The ubiquitin–proteasome system regulates meiotic chromosome organization
title_short The ubiquitin–proteasome system regulates meiotic chromosome organization
title_sort ubiquitin–proteasome system regulates meiotic chromosome organization
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9169913/
https://www.ncbi.nlm.nih.gov/pubmed/35439061
http://dx.doi.org/10.1073/pnas.2106902119
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