Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupials

In eutherian mammals, hundreds of programmed DNA double-strand breaks (DSBs) are generated at the onset of meiosis. The DNA damage response is then triggered. Although the dynamics of this response is well studied in eutherian mammals, recent findings have revealed different patterns of DNA damage s...

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Autores: Valero-Regalón, F. Javier, Solé i Canal, Mireia, López-Jiménez, Pablo, Valerio-de Arana, María, Martín-Ruiz, Marta, Fuente, Roberto de la, Marin-Gual, Laia, Renfree, Marilyn B., Shaw, Geoff, Berríos, Soledad, Fernández-Donoso, Raúl, Waters, Paul D., Ruiz-Herrera, Aurora, Gómez Lencero, Rocío, Page Utrilla, Jesús
Tipo de recurso: artículo
Fecha de publicación:2023
País:España
Institución:Universidad Autónoma de Madrid
Repositorio:Biblos-e Archivo. Repositorio Institucional de la UAM
Idioma:inglés
OAI Identifier:oai:repositorio.uam.es:10486/707856
Acceso en línea:http://hdl.handle.net/10486/707856
https://dx.doi.org/10.3389/fcell.2023.1147610
Access Level:acceso abierto
Palabra clave:Synaptonemal Complex
Meiosis
Genetic Recombination
Biología y Biomedicina / Biología
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spelling Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupialsValero-Regalón, F. JavierSolé i Canal, MireiaLópez-Jiménez, PabloValerio-de Arana, MaríaMartín-Ruiz, MartaFuente, Roberto de laMarin-Gual, LaiaRenfree, Marilyn B.Shaw, GeoffBerríos, SoledadFernández-Donoso, RaúlWaters, Paul D.Ruiz-Herrera, AuroraGómez Lencero, RocíoPage Utrilla, JesúsSynaptonemal ComplexMeiosisGenetic RecombinationBiología y Biomedicina / BiologíaIn eutherian mammals, hundreds of programmed DNA double-strand breaks (DSBs) are generated at the onset of meiosis. The DNA damage response is then triggered. Although the dynamics of this response is well studied in eutherian mammals, recent findings have revealed different patterns of DNA damage signaling and repair in marsupial mammals. To better characterize these differences, here we analyzed synapsis and the chromosomal distribution of meiotic DSBs markers in three different marsupial species (Thylamys elegans, Dromiciops gliorides, and Macropus eugenii) that represent South American and Australian Orders. Our results revealed inter-specific differences in the chromosomal distribution of DNA damage and repair proteins, which were associated with differing synapsis patterns. In the American species T. elegans and D. gliroides, chromosomal ends were conspicuously polarized in a bouquet configuration and synapsis progressed exclusively from the telomeres towards interstitial regions. This was accompanied by sparse H2AX phosphorylation, mainly accumulating at chromosomal ends. Accordingly, RAD51 and RPA were mainly localized at chromosomal ends throughout prophase I in both American marsupials, likely resulting in reduced recombination rates at interstitial positions. In sharp contrast, synapsis initiated at both interstitial and distal chromosomal regions in the Australian representative M. eugenii, the bouquet polarization was incomplete and ephemeral, γH2AX had a broad nuclear distribution, and RAD51 and RPA foci displayed an even chromosomal distribution. Given the basal evolutionary position of T. elegans, it is likely that the meiotic features reported in this species represent an ancestral pattern in marsupials and that a shift in the meiotic program occurred after the split of D. gliroides and the Australian marsupial clade. Our results open intriguing questions about the regulation and homeostasis of meiotic DSBs in marsupials. The low recombination rates observed at the interstitial chromosomal regions in American marsupials can result in the formation of large linkage groups, thus having an impact in the evolution of their genomesThis work was supported by grants CGL 2014-53106-P to JP (Ministerio de Ecomonía y Competitividad, Spain), BIOUAM02- 2020 to JP and RG (Departamento de Biología, Universidad Autónoma de Madrid), PID 2020-112557 GB-I00 to AR-H. (Ministerio de Ciencia e Innovación, Spain) and from the Australian Research Council to MBR, GS, and PDW. (DP21103512 and DP220101429). PW is also supported by the NHMRC (APP1182667 and APP2021172). LM-G was supported by a FPU predoctoral fellowship from the Ministry of Science, Innovation and University (FPU18/03867)Frontiers MediaDepartamento de BiologíaFacultad de Ciencias20232023-04-25research articlehttp://purl.org/coar/resource_type/c_2df8fbb1VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10486/707856https://dx.doi.org/10.3389/fcell.2023.1147610reponame:Biblos-e Archivo. Repositorio Institucional de la UAMinstname:Universidad Autónoma de MadridInglésengopen accesshttp://purl.org/coar/access_right/c_abf2info:eu-repo/semantics/openAccessoai:repositorio.uam.es:10486/7078562026-06-23T12:46:27Z
dc.title.none.fl_str_mv Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupials
title Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupials
spellingShingle Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupials
Valero-Regalón, F. Javier
Synaptonemal Complex
Meiosis
Genetic Recombination
Biología y Biomedicina / Biología
title_short Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupials
title_full Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupials
title_fullStr Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupials
title_full_unstemmed Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupials
title_sort Divergent patterns of meiotic double strand breaks and synapsis initiation dynamics suggest an evolutionary shift in the meiosis program between American and Australian marsupials
dc.creator.none.fl_str_mv Valero-Regalón, F. Javier
Solé i Canal, Mireia
López-Jiménez, Pablo
Valerio-de Arana, María
Martín-Ruiz, Marta
Fuente, Roberto de la
Marin-Gual, Laia
Renfree, Marilyn B.
Shaw, Geoff
Berríos, Soledad
Fernández-Donoso, Raúl
Waters, Paul D.
Ruiz-Herrera, Aurora
Gómez Lencero, Rocío
Page Utrilla, Jesús
author Valero-Regalón, F. Javier
author_facet Valero-Regalón, F. Javier
Solé i Canal, Mireia
López-Jiménez, Pablo
Valerio-de Arana, María
Martín-Ruiz, Marta
Fuente, Roberto de la
Marin-Gual, Laia
Renfree, Marilyn B.
Shaw, Geoff
Berríos, Soledad
Fernández-Donoso, Raúl
Waters, Paul D.
Ruiz-Herrera, Aurora
Gómez Lencero, Rocío
Page Utrilla, Jesús
author_role author
author2 Solé i Canal, Mireia
López-Jiménez, Pablo
Valerio-de Arana, María
Martín-Ruiz, Marta
Fuente, Roberto de la
Marin-Gual, Laia
Renfree, Marilyn B.
Shaw, Geoff
Berríos, Soledad
Fernández-Donoso, Raúl
Waters, Paul D.
Ruiz-Herrera, Aurora
Gómez Lencero, Rocío
Page Utrilla, Jesús
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Departamento de Biología
Facultad de Ciencias
dc.subject.none.fl_str_mv Synaptonemal Complex
Meiosis
Genetic Recombination
Biología y Biomedicina / Biología
topic Synaptonemal Complex
Meiosis
Genetic Recombination
Biología y Biomedicina / Biología
description In eutherian mammals, hundreds of programmed DNA double-strand breaks (DSBs) are generated at the onset of meiosis. The DNA damage response is then triggered. Although the dynamics of this response is well studied in eutherian mammals, recent findings have revealed different patterns of DNA damage signaling and repair in marsupial mammals. To better characterize these differences, here we analyzed synapsis and the chromosomal distribution of meiotic DSBs markers in three different marsupial species (Thylamys elegans, Dromiciops gliorides, and Macropus eugenii) that represent South American and Australian Orders. Our results revealed inter-specific differences in the chromosomal distribution of DNA damage and repair proteins, which were associated with differing synapsis patterns. In the American species T. elegans and D. gliroides, chromosomal ends were conspicuously polarized in a bouquet configuration and synapsis progressed exclusively from the telomeres towards interstitial regions. This was accompanied by sparse H2AX phosphorylation, mainly accumulating at chromosomal ends. Accordingly, RAD51 and RPA were mainly localized at chromosomal ends throughout prophase I in both American marsupials, likely resulting in reduced recombination rates at interstitial positions. In sharp contrast, synapsis initiated at both interstitial and distal chromosomal regions in the Australian representative M. eugenii, the bouquet polarization was incomplete and ephemeral, γH2AX had a broad nuclear distribution, and RAD51 and RPA foci displayed an even chromosomal distribution. Given the basal evolutionary position of T. elegans, it is likely that the meiotic features reported in this species represent an ancestral pattern in marsupials and that a shift in the meiotic program occurred after the split of D. gliroides and the Australian marsupial clade. Our results open intriguing questions about the regulation and homeostasis of meiotic DSBs in marsupials. The low recombination rates observed at the interstitial chromosomal regions in American marsupials can result in the formation of large linkage groups, thus having an impact in the evolution of their genomes
publishDate 2023
dc.date.none.fl_str_mv 2023
2023-04-25
dc.type.none.fl_str_mv research article
http://purl.org/coar/resource_type/c_2df8fbb1
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10486/707856
https://dx.doi.org/10.3389/fcell.2023.1147610
url http://hdl.handle.net/10486/707856
https://dx.doi.org/10.3389/fcell.2023.1147610
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:Biblos-e Archivo. Repositorio Institucional de la UAM
instname:Universidad Autónoma de Madrid
instname_str Universidad Autónoma de Madrid
reponame_str Biblos-e Archivo. Repositorio Institucional de la UAM
collection Biblos-e Archivo. Repositorio Institucional de la UAM
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,300724

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