Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)

Detalhes bibliográficos
Autor(a) principal: Noronha, Renata Coelho Rodrigues
Data de Publicação: 2020
Outros Autores: de Almeida, Bruno Rafael Ribeiro, da Costa, Marlyson Jeremias Rodrigues, Nagamachi, Cleusa Yoshiko, Martins, Cesar [UNESP], Pieczarka, Julio Cesar
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1038/s41598-020-72867-x
http://hdl.handle.net/11449/208007
Resumo: Heterozygous chromosomal rearrangements can result in failures during the meiotic cycle and the apoptosis of germline, making carrier individuals infertile. The Amazon frog Leptodactylus pentadactylus has a meiotic multivalent, composed of 12 sex chromosomes. The mechanisms by which this multi-chromosome system maintains fertility in males of this species remain undetermined. In this study we investigated the meiotic behavior of this multivalent to understand how synapse, recombination and epigenetic modifications contribute to maintaining fertility and chromosomal sexual determination in this species. Our sample had 2n = 22, with a ring formed by ten chromosomes in meiosis, indicating a new system of sex determination for this species (X1Y1X2Y2X3Y3X4Y4X5Y5). Synapsis occurs in the homologous terminal portion of the chromosomes, while part of the heterologous interstitial regions performed synaptic adjustment. The multivalent center remains asynaptic until the end of pachytene, with interlocks, gaps and rich-chromatin in histone H2A phosphorylation at serine 139 (γH2AX), suggesting transcriptional silence. In late pachytene, paired regions show repair of double strand-breaks (DSBs) with RAD51 homolog 1 (Rad51). These findings suggest that Rad51 persistence creates positive feedback at the pachytene checkpoint, allowing meiosis I to progress normally. Additionally, histone H3 trimethylation at lysine 27 in the pericentromeric heterochromatin of this anuran can suppress recombination in this region, preventing failed chromosomal segregation. Taken together, these results indicate that these meiotic adaptations are required for maintenance of fertility in L. pentadactylus.
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spelling Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)Heterozygous chromosomal rearrangements can result in failures during the meiotic cycle and the apoptosis of germline, making carrier individuals infertile. The Amazon frog Leptodactylus pentadactylus has a meiotic multivalent, composed of 12 sex chromosomes. The mechanisms by which this multi-chromosome system maintains fertility in males of this species remain undetermined. In this study we investigated the meiotic behavior of this multivalent to understand how synapse, recombination and epigenetic modifications contribute to maintaining fertility and chromosomal sexual determination in this species. Our sample had 2n = 22, with a ring formed by ten chromosomes in meiosis, indicating a new system of sex determination for this species (X1Y1X2Y2X3Y3X4Y4X5Y5). Synapsis occurs in the homologous terminal portion of the chromosomes, while part of the heterologous interstitial regions performed synaptic adjustment. The multivalent center remains asynaptic until the end of pachytene, with interlocks, gaps and rich-chromatin in histone H2A phosphorylation at serine 139 (γH2AX), suggesting transcriptional silence. In late pachytene, paired regions show repair of double strand-breaks (DSBs) with RAD51 homolog 1 (Rad51). These findings suggest that Rad51 persistence creates positive feedback at the pachytene checkpoint, allowing meiosis I to progress normally. Additionally, histone H3 trimethylation at lysine 27 in the pericentromeric heterochromatin of this anuran can suppress recombination in this region, preventing failed chromosomal segregation. Taken together, these results indicate that these meiotic adaptations are required for maintenance of fertility in L. pentadactylus.Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)Laboratório de Citogenética Centro de Estudos Avançados em Biodiversidade Instituto de Ciências Biológicas Universidade Federal do Pará, Campus Guamá, Rua Augusto Corrêa, no. 01, GuamáDepartamento de Biologia Estrutural e Funcional Instituto de Biociências de Botucatu Universidade Estadual Paulista (UNESP), Campus BotucatuDepartamento de Biologia Estrutural e Funcional Instituto de Biociências de Botucatu Universidade Estadual Paulista (UNESP), Campus BotucatuCNPq: 475013/2012-3Universidade Federal do Pará (UFPA)Universidade Estadual Paulista (Unesp)Noronha, Renata Coelho Rodriguesde Almeida, Bruno Rafael Ribeiroda Costa, Marlyson Jeremias RodriguesNagamachi, Cleusa YoshikoMartins, Cesar [UNESP]Pieczarka, Julio Cesar2021-06-25T11:04:49Z2021-06-25T11:04:49Z2020-12-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1038/s41598-020-72867-xScientific Reports, v. 10, n. 1, 2020.2045-2322http://hdl.handle.net/11449/20800710.1038/s41598-020-72867-x2-s2.0-8509177449388588006994253520000-0003-3534-974XScopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengScientific Reportsinfo:eu-repo/semantics/openAccess2021-10-23T22:14:28Zoai:repositorio.unesp.br:11449/208007Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462021-10-23T22:14:28Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)
title Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)
spellingShingle Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)
Noronha, Renata Coelho Rodrigues
title_short Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)
title_full Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)
title_fullStr Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)
title_full_unstemmed Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)
title_sort Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)
author Noronha, Renata Coelho Rodrigues
author_facet Noronha, Renata Coelho Rodrigues
de Almeida, Bruno Rafael Ribeiro
da Costa, Marlyson Jeremias Rodrigues
Nagamachi, Cleusa Yoshiko
Martins, Cesar [UNESP]
Pieczarka, Julio Cesar
author_role author
author2 de Almeida, Bruno Rafael Ribeiro
da Costa, Marlyson Jeremias Rodrigues
Nagamachi, Cleusa Yoshiko
Martins, Cesar [UNESP]
Pieczarka, Julio Cesar
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade Federal do Pará (UFPA)
Universidade Estadual Paulista (Unesp)
dc.contributor.author.fl_str_mv Noronha, Renata Coelho Rodrigues
de Almeida, Bruno Rafael Ribeiro
da Costa, Marlyson Jeremias Rodrigues
Nagamachi, Cleusa Yoshiko
Martins, Cesar [UNESP]
Pieczarka, Julio Cesar
description Heterozygous chromosomal rearrangements can result in failures during the meiotic cycle and the apoptosis of germline, making carrier individuals infertile. The Amazon frog Leptodactylus pentadactylus has a meiotic multivalent, composed of 12 sex chromosomes. The mechanisms by which this multi-chromosome system maintains fertility in males of this species remain undetermined. In this study we investigated the meiotic behavior of this multivalent to understand how synapse, recombination and epigenetic modifications contribute to maintaining fertility and chromosomal sexual determination in this species. Our sample had 2n = 22, with a ring formed by ten chromosomes in meiosis, indicating a new system of sex determination for this species (X1Y1X2Y2X3Y3X4Y4X5Y5). Synapsis occurs in the homologous terminal portion of the chromosomes, while part of the heterologous interstitial regions performed synaptic adjustment. The multivalent center remains asynaptic until the end of pachytene, with interlocks, gaps and rich-chromatin in histone H2A phosphorylation at serine 139 (γH2AX), suggesting transcriptional silence. In late pachytene, paired regions show repair of double strand-breaks (DSBs) with RAD51 homolog 1 (Rad51). These findings suggest that Rad51 persistence creates positive feedback at the pachytene checkpoint, allowing meiosis I to progress normally. Additionally, histone H3 trimethylation at lysine 27 in the pericentromeric heterochromatin of this anuran can suppress recombination in this region, preventing failed chromosomal segregation. Taken together, these results indicate that these meiotic adaptations are required for maintenance of fertility in L. pentadactylus.
publishDate 2020
dc.date.none.fl_str_mv 2020-12-01
2021-06-25T11:04:49Z
2021-06-25T11:04:49Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1038/s41598-020-72867-x
Scientific Reports, v. 10, n. 1, 2020.
2045-2322
http://hdl.handle.net/11449/208007
10.1038/s41598-020-72867-x
2-s2.0-85091774493
8858800699425352
0000-0003-3534-974X
url http://dx.doi.org/10.1038/s41598-020-72867-x
http://hdl.handle.net/11449/208007
identifier_str_mv Scientific Reports, v. 10, n. 1, 2020.
2045-2322
10.1038/s41598-020-72867-x
2-s2.0-85091774493
8858800699425352
0000-0003-3534-974X
dc.language.iso.fl_str_mv eng
language eng
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eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
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instname_str Universidade Estadual Paulista (UNESP)
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institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
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