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Rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish

During meiosis I, ring-shaped cohesin complexes play important roles in aiding the proper segregation of homologous chromosomes. RAD21L is a meiosis-specific vertebrate cohesin that is required for spermatogenesis in mice but is dispensable for oogenesis in young animals. The role of this cohesin in...

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Autores principales: Blokhina, Yana P., Frees, Michelle A., Nguyen, An, Sharifi, Masuda, Chu, Daniel B., Bispo, Kristi, Olaya, Ivan, Draper, Bruce W., Burgess, Sean M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8291703/
https://www.ncbi.nlm.nih.gov/pubmed/34138874
http://dx.doi.org/10.1371/journal.pgen.1009127
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author Blokhina, Yana P.
Frees, Michelle A.
Nguyen, An
Sharifi, Masuda
Chu, Daniel B.
Bispo, Kristi
Olaya, Ivan
Draper, Bruce W.
Burgess, Sean M.
author_facet Blokhina, Yana P.
Frees, Michelle A.
Nguyen, An
Sharifi, Masuda
Chu, Daniel B.
Bispo, Kristi
Olaya, Ivan
Draper, Bruce W.
Burgess, Sean M.
author_sort Blokhina, Yana P.
collection PubMed
description During meiosis I, ring-shaped cohesin complexes play important roles in aiding the proper segregation of homologous chromosomes. RAD21L is a meiosis-specific vertebrate cohesin that is required for spermatogenesis in mice but is dispensable for oogenesis in young animals. The role of this cohesin in other vertebrate models has not been explored. Here, we tested if the zebrafish homolog Rad21l1 is required for meiotic chromosome dynamics during spermatogenesis and oogenesis. We found that Rad21l1 localizes to unsynapsed chromosome axes. It is also found between the axes of the mature tripartite synaptonemal complex (SC) in both sexes. We knocked out rad21l1 and found that nearly all rad21l1(-/-) mutants develop as fertile males, suggesting that the mutation causes a defect in juvenile oogenesis, since insufficient oocyte production triggers female to male sex reversal in zebrafish. Sex reversal was partially suppressed by mutation of the checkpoint gene tp53, suggesting that the rad21l1 mutation activates Tp53-mediated apoptosis or arrest in females. This response, however, is not linked to a defect in repairing Spo11-induced double-strand breaks since deletion of spo11 does not suppress the sex reversal phenotype. Compared to tp53 single mutant controls, rad21l1(-/-) tp53(-/-) double mutant females produce poor quality eggs that often die or develop into malformed embryos. Overall, these results indicate that the absence of rad21l1(-/-) females is due to a checkpoint-mediated response and highlight a role for a meiotic-specific cohesin subunit in oogenesis but not spermatogenesis.
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spelling pubmed-82917032021-07-31 Rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish Blokhina, Yana P. Frees, Michelle A. Nguyen, An Sharifi, Masuda Chu, Daniel B. Bispo, Kristi Olaya, Ivan Draper, Bruce W. Burgess, Sean M. PLoS Genet Research Article During meiosis I, ring-shaped cohesin complexes play important roles in aiding the proper segregation of homologous chromosomes. RAD21L is a meiosis-specific vertebrate cohesin that is required for spermatogenesis in mice but is dispensable for oogenesis in young animals. The role of this cohesin in other vertebrate models has not been explored. Here, we tested if the zebrafish homolog Rad21l1 is required for meiotic chromosome dynamics during spermatogenesis and oogenesis. We found that Rad21l1 localizes to unsynapsed chromosome axes. It is also found between the axes of the mature tripartite synaptonemal complex (SC) in both sexes. We knocked out rad21l1 and found that nearly all rad21l1(-/-) mutants develop as fertile males, suggesting that the mutation causes a defect in juvenile oogenesis, since insufficient oocyte production triggers female to male sex reversal in zebrafish. Sex reversal was partially suppressed by mutation of the checkpoint gene tp53, suggesting that the rad21l1 mutation activates Tp53-mediated apoptosis or arrest in females. This response, however, is not linked to a defect in repairing Spo11-induced double-strand breaks since deletion of spo11 does not suppress the sex reversal phenotype. Compared to tp53 single mutant controls, rad21l1(-/-) tp53(-/-) double mutant females produce poor quality eggs that often die or develop into malformed embryos. Overall, these results indicate that the absence of rad21l1(-/-) females is due to a checkpoint-mediated response and highlight a role for a meiotic-specific cohesin subunit in oogenesis but not spermatogenesis. Public Library of Science 2021-06-17 /pmc/articles/PMC8291703/ /pubmed/34138874 http://dx.doi.org/10.1371/journal.pgen.1009127 Text en © 2021 Blokhina et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Blokhina, Yana P.
Frees, Michelle A.
Nguyen, An
Sharifi, Masuda
Chu, Daniel B.
Bispo, Kristi
Olaya, Ivan
Draper, Bruce W.
Burgess, Sean M.
Rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish
title Rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish
title_full Rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish
title_fullStr Rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish
title_full_unstemmed Rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish
title_short Rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish
title_sort rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8291703/
https://www.ncbi.nlm.nih.gov/pubmed/34138874
http://dx.doi.org/10.1371/journal.pgen.1009127
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