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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...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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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. |
format | Online Article Text |
id | pubmed-9169913 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
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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