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...
| Authors: | ; ; ; ; ; ; ; ; ; ; ; ; ; ; |
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| Format: | Article |
| Publication date: | 2023 |
| Country: | España |
| Institution: | Universidad Autónoma de Madrid |
| Repository: | Biblos-e Archivo. Repositorio Institucional de la UAM |
| Language: | English |
| OAI Identifier: | oai:repositorio.uam.es:10486/707856 |
| Online Access: | http://hdl.handle.net/10486/707856 https://dx.doi.org/10.3389/fcell.2023.1147610 |
| Access Level: | Open access |
| Keyword: | Synaptonemal Complex Meiosis Genetic Recombination Biología y Biomedicina / Biología |
| _version_ | 1878734618597785600 |
|---|---|
| author | Valero-Regalón, F. Javier |
| 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 |
| author_browse | Berríos, Soledad Fernández-Donoso, Raúl Fuente, Roberto de la Gómez Lencero, Rocío López-Jiménez, Pablo Marin-Gual, Laia Martín-Ruiz, Marta Page Utrilla, Jesús Renfree, Marilyn B. Ruiz-Herrera, Aurora Shaw, Geoff Solé i Canal, Mireia Valerio-de Arana, María Valero-Regalón, F. Javier Waters, Paul D. |
| 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 |
| collection | Biblos-e Archivo. Repositorio Institucional de la UAM |
| 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 |
| eu_rights_str_mv | openAccess |
| format | article |
| id | ES_6cf0caa3df887edb350ec1dad7b1c14c |
| institution | Universidad Autónoma de Madrid |
| instname_str | Universidad Autónoma de Madrid |
| language | eng |
| network_acronym_str | ES |
| network_name_str | España |
| oai_identifier_str | oai:repositorio.uam.es:10486/707856 |
| publishDate | 2023 |
| publishDateSort | 2023 |
| publisher | Frontiers Media |
| publisherStr | Frontiers Media |
| reponame_str | Biblos-e Archivo. Repositorio Institucional de la UAM |
| spelling | 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 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 Synaptonemal Complex Meiosis Genetic Recombination Biología y Biomedicina / Biología 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 This 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 Media http://hdl.handle.net/10486/707856 https://dx.doi.org/10.3389/fcell.2023.1147610 |
| 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 | 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_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_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 |
| topic | Synaptonemal Complex Meiosis Genetic Recombination Biología y Biomedicina / Biología |
| topic_facet | Synaptonemal Complex Meiosis Genetic Recombination Biología y Biomedicina / Biología |
| url | http://hdl.handle.net/10486/707856 https://dx.doi.org/10.3389/fcell.2023.1147610 |