Transcription reactivation during the first meiotic prophase in bugs is not dependent on synapsis

Abstract

During meiosis, transcription is precisely regulated in relation to the process of chromosome synapsis. In mammals, transcription is very low until the completion of synapsis in early pachytene, and then reactivates during mid pachytene, up to the end of diplotene. Moreover, chromosomes or chromosomal regions that do not achieve synapsis undergo a specific process of inactivation called meiotic silencing of unpaired chromatin (MSUC). Sex chromosomes, which are mostly unsynapsed, present a special case of inactivation named meiotic sex chromosome inactivation (MSCI). Although processes that are similar to MSUC/MSCI have been described in other species like Sordaria and Caenorhabditis elegans, very few studies have been developed in insects. We present a study on the relationships between synapsis and transcription in two hemipteran species (Graphosoma italicum and Carpocoris fuscispinus) that possess holocentric chromosomes but develop different synaptic patterns. We have found that transcription, revealed by the presence of RNA polymerase II, is very low at the beginning of meiosis, but robustly increases during zygotene, long before the completion of synapsis, excepting in the sex chromosomes. In fact, we show that histone H3 methylation at lysine 9 (H3K9me3) may be present in the sex chromosomes at leptotene, thus acting as a likely epigenetic mark for this inactive state. Our results suggest that the meiotic transcription in these two species is differently regulated from that of mammals and, therefore, offer new opportunities to understand the relationship between synapsis and transcription and the mechanisms that govern MSUC/MSCI processes.

X Chromosome Inactivation during Grasshopper Spermatogenesis

“…We found that these regions were positioned at both ends of the SMC3 axis and corresponded to chromosome ends (Figure S1B). A similar labeling was previously reported in other insect species [51,55,62], most probably representing telomeric/subtelomeric heterochromatin at chromosome ends, or the pericentromeric heterochromatin at the centromeric end.…”

“…Thus, the disruption of either recombination or synapsis hampers the whole normal program of transcription and the epigenetic transitions that encompass meiosis progression [ 26 ]. However, this model might not be completely applied to other model organisms such as Caenorhabditis elegans [ 42 ] or Drosophila melanogaster [ 47 ], and neither to several species of grasshoppers [ 43 , 46 , 48 ] and true bugs [ 49 , 51 ], in which transcriptional activity in early spermatocytes is abundant prior to synapsis achievement.…”

“…Histone H3 trimethylated at lysine 9 (H3K9me3) was revealed with a rabbit polyclonal serum (Abcam, Cambridge, UK, ab-8898) at a 1:100 dilution [ 55 ]. RNA polymerase II phosphorylated at serine 2 (p-RNApol-II) was revealed with a mouse monoclonal antibody (Abcam, Cambridge, UK, 24758) at a 1:100 dilution [ 51 ]. Following three washes in PBS, the slides were incubated for 30 min at room temperature with the corresponding secondary antibodies.…”

“…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.…”

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

“…In Drosophila , for example, transcription is maintained constant throughout meiosis I (Hennig and Weyrich, 2013). In Hemiptera, Viera et al (2017) reported that transcription is reactivated during the zygotene stage and proceeds until the end of prophase I in autosomes.…”