Abstract:During meiotic prophase I, tightly regulated processes take place, from pairing and synapsis of homologous chromosomes to recombination, which are essential for the generation of genetically variable haploid gametes. These processes have canonical meiotic features conserved across different phylogenetic groups. However, the dynamics of meiotic prophase I in non-mammalian vertebrates are poorly known. Here, we compare four species from Sauropsida to understand the regulation of meiotic prophase I in reptiles: t… Show more
“…This is what we observed in the third marsupial species analyzed in this study, M. eugenii, which mimics the pattern described in mouse. Considering the phylogenetic relationships between the marsupials studied here (Figure 1) (Duchêne et al, 2017), and previous reports in other vertebrates (Blokhina et al, 2019;Marín-Gual et al, 2022a), the most parsimonious explanation is that bouquet polarization is an ancestral character in marsupials, and most probably in all vertebrates.…”
Section: The Conspicuous Bouquet Conformation Could Be An Ancient Fea...supporting
confidence: 66%
“…Previous reports in monotreme mammals (Daish et al, 2015) and some insects (Viera et al, 2017) have indicated that γH2AX is not necessarily a marker of DNA damage during prophase I. Our own observations indicate that γH2AX is not detected during prophase I in some reptiles (Marín-Gual et al, 2022a) (Page, unpublished). Therefore, is seems that some aspects of DNA damage signaling during meiosis in mammals and other vertebrates are yet to be properly characterized.…”
Section: Induction Of Dsbs and Synapsis Initiation And Progressionmentioning
confidence: 50%
“…Likewise, the features observed in T. elegans , clearly basal to the rest of the marsupial groups, could have been shared with the ancestor of the eutherian mammals before they split apart about 165 million years ago. In view of recent reports, these features could be even dated back to the appearance of early vertebrates (Blokhina et al, 2019; Marín-Gual et al, 2022a). Expansion of meiosis studies to uncharacterized mammals, including eutherians, marsupials and monotremes, as well as to other vertebrates (i.e., reptiles, amphibians or fishes), will shed light on the evolution of meiosis across taxa.…”
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, synapsis progressed exclusively from the chromosomal ends towards interstitial regions. This was accompanied by sparse H2AX phosphorylation, mainly accumulating at chromosomal ends, which appeared conspicuously polarized in a bouquet configuration at early stages of prophase I. Accordingly, RAD51 and RPA were mainly localized at chromosomal ends throughout prophaseI 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, 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 is what we observed in the third marsupial species analyzed in this study, M. eugenii, which mimics the pattern described in mouse. Considering the phylogenetic relationships between the marsupials studied here (Figure 1) (Duchêne et al, 2017), and previous reports in other vertebrates (Blokhina et al, 2019;Marín-Gual et al, 2022a), the most parsimonious explanation is that bouquet polarization is an ancestral character in marsupials, and most probably in all vertebrates.…”
Section: The Conspicuous Bouquet Conformation Could Be An Ancient Fea...supporting
confidence: 66%
“…Previous reports in monotreme mammals (Daish et al, 2015) and some insects (Viera et al, 2017) have indicated that γH2AX is not necessarily a marker of DNA damage during prophase I. Our own observations indicate that γH2AX is not detected during prophase I in some reptiles (Marín-Gual et al, 2022a) (Page, unpublished). Therefore, is seems that some aspects of DNA damage signaling during meiosis in mammals and other vertebrates are yet to be properly characterized.…”
Section: Induction Of Dsbs and Synapsis Initiation And Progressionmentioning
confidence: 50%
“…Likewise, the features observed in T. elegans , clearly basal to the rest of the marsupial groups, could have been shared with the ancestor of the eutherian mammals before they split apart about 165 million years ago. In view of recent reports, these features could be even dated back to the appearance of early vertebrates (Blokhina et al, 2019; Marín-Gual et al, 2022a). Expansion of meiosis studies to uncharacterized mammals, including eutherians, marsupials and monotremes, as well as to other vertebrates (i.e., reptiles, amphibians or fishes), will shed light on the evolution of meiosis across taxa.…”
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, synapsis progressed exclusively from the chromosomal ends towards interstitial regions. This was accompanied by sparse H2AX phosphorylation, mainly accumulating at chromosomal ends, which appeared conspicuously polarized in a bouquet configuration at early stages of prophase I. Accordingly, RAD51 and RPA were mainly localized at chromosomal ends throughout prophaseI 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, 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.
“…Thus, the synapsis pattern of homologous chromosomes seems to be conditioned by the way DNA damage is produced during prophase I. The pattern observed in T. elegans and D. gliroides seems to be ancestral, and even shared by other non-mammalian vertebrates (Blokhina et al, 2019;Marín-Gual et al, 2022a). Finally, we highlight the possibility that a part of the DNA damage occurring in T. elegans and D. gliroides was not accompanied by H2AX phosphorylation.…”
Section: Induction Of Dsbs and Synapsis Initiation And Progressionmentioning
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.
“…The excised testicular tissue (from September) was cut into 5 mm square blocks and fixed with 4% paraformaldehyde for 48 h. After alcohol dehydration, xylene clearing, and paraffin treatment, the paraffin-embedded tissues were sectioned at a thickness of 6 μm. After staining with hematoxylin and eosin (H&E), According to morphological characteristics of cytoarchitecture, spermatogenic cell types were judged ( Zhang et al 2008 , Marín-Gual et al 2022 ). The changes of spermatogenic cell assemblages in spermatogenic epithelium were compared in different seasons.…”
The Chinese soft-shelled turtle, Pelodiscus sinensis (Reptilia: Trionychidae) is a typical seasonal breeding species and its spermatogenesis pattern is complex. In this study, the process of sperm cell development was studied using histology. The process of sperm cell development may be divided into six stages based on a combination of different cell types in the seminiferous epithelium. A close examination revealed two patterns of sperm cell development in the seminiferous tubules during the breeding season. The first is a normal sperm cell development pattern, in which the process of sperm cell development and maturation are completed in the seminiferous epithelium without round spermatozoa in the lumen. The second is rapid sperm cell development, in which the first batches of round spermatozoa fall off the seminiferous epithelium before they mature, thus beginning a second batch of sperm cell development. The round sperm cells are shed into the lumen and further mature in the seminiferous tubules and epididymis. This rapid sperm cell development process of the Chinese soft-shelled turtle is rare in other vertebrate species and may be an adaptation to cope with seasonal breeding. The results of this study provide insight into the theory of seasonal reproduction in reptiles.
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