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

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.