Meiosis in the scorpion Tityus silvestris: new insights into achiasmatic chromosomes

Abstract

Achiasmatic male meiosis in scorpions is characterized by a high frequency of gaps, asynaptic regions and multivalent associations. Here, we performed an immunocytogenetic analysis to investigate recombination, and synapsis and chromatin-remodeling events during meiosis of the scorpion Tityus silvestris . Our results demonstrate that the synaptonemal complex (SC) begins its organization in the zygotene stage and persists until metaphase I. The advancement of the synaptic process is related to the epigenetic modification histone H3 lysine 27 trimethylation (H3K27m3). The distribution and dynamics patterns of variant γH2AX and recombinase Rad51 during achiasmatic meiosis suggests formation and repair of DNA double-strand breaks (DSBs) during early stages of prophase I. The epigenetic modifications, histone H3 lysine 4 trimethylation (H3K4m3) and histone H3 lysine 9 acetylation (H3K9ac), showed a dispersed distribution along the bivalents, suggesting that transcriptional activity is maintained constitutively during prophase I. However, H3K9ac modifications are absent in constitutive heterochromatin carrying the 45S rDNA in pachytene and post-pachytene stages. Collectively, our data demonstrate that T. silvestris exhibits adaptations to the achiasmatic mode, and suggest that epigenetic modifications may act in the regulation of these mechanisms to favor the normal continuation of meiosis in this scorpion.

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

“…Moreover, this is the first study to show the presence of an epigenetic marker in the centromere of an anuran. In other species, H3K27me3 is generally related to facultative heterochromatin, promoting the reversible inactivation of (i) genes presents on the X chromosome 59 ; (ii) repetitive DNA associated with synaptonemal complex organization 60,61 ; (iii) the nonsynapsed autosomal region 24 ; and (iv) the ZW chromatin of birds 26 . DSBs tend not to form in repetitive regions, as they may promote crossing-over in non-allelic regions, generating genomic instability, harmful rearrangements to chromosomal segregation 62,63 .…”

Kinetic Activity of Chromosomes and Expression of Recombination Genes in Achiasmatic Meiosis of Tityus (Archaeotityus) Scorpions

“…In these species, changes in the synaptonemal complex (gaps, non-synaptic lateral elements) were observed using ultrastructural microscopy [ 10 ]. Analysis of the behavior of the synaptonemal complex in Tityus and other arthropods can also be inferred by the structural maintenance of chromosome protein 3 (SMC3) immunofluorescence, a component of the cohesins axis that bind to the lateral elements during prophase I [ 13 ]. Despite this, to date, no study has investigated the occurrence of meiotic silencing of unsynapsed chromatin (MSUC) during Tityus prophase I.…”

“…Achiasmate meiosis was previously confirmed to be associated only with heterogametic sex in plants, tardigrades, crustaceans, insects, and arachnids or in both gonads (testis and ovary) of some annelids, flatworms, and hermaphroditic mollusks [ 24 ]. Among scorpion species, cytogenetically investigated males showed achiasmatic meiosis [ 10 , 12 , 13 ]. Regarding females, the presence of chiasmata is questionable, most being considered achiasmatic, with only one case of chiasma-like structures in Zabius (Buthidae) [ 8 , 25 , 26 ].…”

“…Regarding females, the presence of chiasmata is questionable, most being considered achiasmatic, with only one case of chiasma-like structures in Zabius (Buthidae) [ 8 , 25 , 26 ]. The absence of chiasmata in Tityus , as in other genera, is considered an adaptation to the high incidence of rearrangements, since the decrease in the rate of crossing-over favors the correct segregation of homologous components of meiotic multivalents [ 10 , 13 ]. The molecular processes that generate achiasmatic meiosis are poorly understood and vary among the groups mentioned above.…”

X Chromosome Inactivation during Grasshopper Spermatogenesis

“…Studies in species from other different taxa, particularly insects, have revealed deviations from the well-characterized patterns of the regulation of transcription and MSUC/MSCI displayed by eutherian mammals. For instance, transcriptional activity in grasshoppers, moths, true bugs and scorpions is rather abundant in early stages of meiosis [ 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 ]. Interestingly, many of these species present a sex chromosomal determinism of the type XX for females and X0 for males, which is especially interesting.…”