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Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans

In sexually reproducing organisms, germ cells faithfully transmit the genome to the next generation by forming haploid gametes, such as eggs and sperm. Although most meiotic proteins are conserved between eggs and sperm, many aspects of meiosis are sexually dimorphic, including the regulation of rec...

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Autores principales: Cahoon, Cori K, Richter, Colette M, Dayton, Amelia E, Libuda, Diana E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10611432/
https://www.ncbi.nlm.nih.gov/pubmed/37796106
http://dx.doi.org/10.7554/eLife.84538
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author Cahoon, Cori K
Richter, Colette M
Dayton, Amelia E
Libuda, Diana E
author_facet Cahoon, Cori K
Richter, Colette M
Dayton, Amelia E
Libuda, Diana E
author_sort Cahoon, Cori K
collection PubMed
description In sexually reproducing organisms, germ cells faithfully transmit the genome to the next generation by forming haploid gametes, such as eggs and sperm. Although most meiotic proteins are conserved between eggs and sperm, many aspects of meiosis are sexually dimorphic, including the regulation of recombination. The synaptonemal complex (SC), a large ladder-like structure that forms between homologous chromosomes, is essential for regulating meiotic chromosome organization and promoting recombination. To assess whether sex-specific differences in the SC underpin sexually dimorphic aspects of meiosis, we examined Caenorhabditis elegans SC central region proteins (known as SYP proteins) in oogenesis and spermatogenesis and uncovered sex-specific roles for the SYPs in regulating meiotic recombination. We find that SC composition, specifically SYP-2, SYP-3, SYP-5, and SYP-6, is regulated by sex-specific mechanisms throughout meiotic prophase I. During pachytene, both oocytes and spermatocytes differentially regulate the stability of SYP-2 and SYP-3 within an assembled SC. Further, we uncover that the relative amount of SYP-2 and SYP-3 within the SC is independently regulated in both a sex-specific and a recombination-dependent manner. Specifically, we find that SYP-2 regulates the early steps of recombination in both sexes, while SYP-3 controls the timing and positioning of crossover recombination events across the genomic landscape in only oocytes. Finally, we find that SYP-2 and SYP-3 dosage can influence the composition of the other SYPs in the SC via sex-specific mechanisms during pachytene. Taken together, we demonstrate dosage-dependent regulation of individual SC components with sex-specific functions in recombination. These sexual dimorphic features of the SC provide insights into how spermatogenesis and oogenesis adapted similar chromosome structures to differentially regulate and execute recombination.
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spelling pubmed-106114322023-10-28 Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans Cahoon, Cori K Richter, Colette M Dayton, Amelia E Libuda, Diana E eLife Chromosomes and Gene Expression In sexually reproducing organisms, germ cells faithfully transmit the genome to the next generation by forming haploid gametes, such as eggs and sperm. Although most meiotic proteins are conserved between eggs and sperm, many aspects of meiosis are sexually dimorphic, including the regulation of recombination. The synaptonemal complex (SC), a large ladder-like structure that forms between homologous chromosomes, is essential for regulating meiotic chromosome organization and promoting recombination. To assess whether sex-specific differences in the SC underpin sexually dimorphic aspects of meiosis, we examined Caenorhabditis elegans SC central region proteins (known as SYP proteins) in oogenesis and spermatogenesis and uncovered sex-specific roles for the SYPs in regulating meiotic recombination. We find that SC composition, specifically SYP-2, SYP-3, SYP-5, and SYP-6, is regulated by sex-specific mechanisms throughout meiotic prophase I. During pachytene, both oocytes and spermatocytes differentially regulate the stability of SYP-2 and SYP-3 within an assembled SC. Further, we uncover that the relative amount of SYP-2 and SYP-3 within the SC is independently regulated in both a sex-specific and a recombination-dependent manner. Specifically, we find that SYP-2 regulates the early steps of recombination in both sexes, while SYP-3 controls the timing and positioning of crossover recombination events across the genomic landscape in only oocytes. Finally, we find that SYP-2 and SYP-3 dosage can influence the composition of the other SYPs in the SC via sex-specific mechanisms during pachytene. Taken together, we demonstrate dosage-dependent regulation of individual SC components with sex-specific functions in recombination. These sexual dimorphic features of the SC provide insights into how spermatogenesis and oogenesis adapted similar chromosome structures to differentially regulate and execute recombination. eLife Sciences Publications, Ltd 2023-10-05 /pmc/articles/PMC10611432/ /pubmed/37796106 http://dx.doi.org/10.7554/eLife.84538 Text en © 2023, Cahoon et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Chromosomes and Gene Expression
Cahoon, Cori K
Richter, Colette M
Dayton, Amelia E
Libuda, Diana E
Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans
title Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans
title_full Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans
title_fullStr Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans
title_full_unstemmed Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans
title_short Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans
title_sort sexual dimorphic regulation of recombination by the synaptonemal complex in c. elegans
topic Chromosomes and Gene Expression
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10611432/
https://www.ncbi.nlm.nih.gov/pubmed/37796106
http://dx.doi.org/10.7554/eLife.84538
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