Meiotic chromosome dynamics and double strand break formation in reptiles

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: the Australian central bearded dragon (Pogona vitticeps), two geckos (Paroedura picta and Coleonyx variegatus) and the painted turtle (Chrysemys picta). We first performed a histological characterization of the spermatogenesis process in both the bearded dragon and the painted turtle. We then analyzed prophase I dynamics, including chromosome pairing, synapsis and the formation of double strand breaks (DSBs). We show that meiosis progression is highly conserved in reptiles with telomeres clustering forming the bouquet, which we propose promotes homologous pairing and synapsis, along with facilitating the early pairing of micro-chromosomes during prophase I (i.e., early zygotene). Moreover, we detected low levels of meiotic DSB formation in all taxa. Our results provide new insights into reptile meiosis.

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

“…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.…”

“…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observations indicate that γH2AX is not detected during prophase I in some reptiles (Marín-Gual et al, 2022a) (Page, unpublished).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.…”

“…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.…”

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

“…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.…”

Study on the pattern of spermatogenesis during the breeding season of the Chinese soft-shelled turtle, Pelodiscus sinensis (Reptilia: Trionychidae)

“…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.…”