Gametic specialization of centromeric histone paralogs in Drosophila virilis

Abstract

In most eukaryotes, centromeric histone (CenH3) proteins mediate mitosis and meiosis and ensure epigenetic inheritance of centromere identity. We hypothesized that disparate chromatin environments in soma versus germline might impose divergent functional requirements on single CenH3 genes, which could be ameliorated by gene duplications and subsequent specialization. Here, we analyzed the cytological localization of two recently identified CenH3 paralogs, Cid1 and Cid5, in Drosophila virilis using specific antibodies and epitope-tagged transgenic strains. We find that only ancestral Cid1 is present in somatic cells, whereas both Cid1 and Cid5 are expressed in testes and ovaries. However, Cid1 is lost in male meiosis but retained throughout oogenesis, whereas Cid5 is lost during female meiosis but retained in mature sperm. Following fertilization, only Cid1 is detectable in the early embryo, suggesting that maternally deposited Cid1 is rapidly loaded onto paternal centromeres during the protamine-to-histone transition. Our studies reveal mutually exclusive gametic specialization of divergent CenH3 paralogs. Duplication and divergence might allow essential centromeric genes to resolve an intralocus conflict between maternal and paternal centromeric requirements in many animal species.

Recurrent but short-lived duplications of centromeric proteins in holocentricCaenorhabditisspecies

“…Overall, our analyses reveal that hcp-3 has duplicated at least ten independent times within Caenorhabditis species. In contrast to plants, Drosophila , and mosquito species (Kursel and Malik 2017; Kursel, et al 2020; Kursel, et al 2021), we observed only a few cases of hcp-3L paralogs that are shared across two or three Caenorhabditis sister species, although this may partly reflect density of species sampling in these different taxonomic groups. Our findings suggest that most of the hcp-3L paralogs we have found are relatively young, if the relative ages of Caenorhabditis and Drosophila species analyzed are comparable (Cutter 2008).…”

“…Conflicting evolutionary selective pressures on CenH3 between these functions (e.g., mitotic versus meiotic, conserved versus rapidly evolving) could be resolved by gene duplication, which allows the duplicate (paralog) and ancestral genes to specialize in different functions (Gallach and Betrán 2011). Indeed, CenH3 genes have also undergone repeated gene duplications not just in plant but also in several animal species including cows, fruit flies, mosquitoes, and nematodes (Li and (Kursel, et al 2021).…”

“…Conflicting evolutionary selective pressures on CenH3 between these functions ( e.g ., mitotic versus meiotic, conserved versus rapidly evolving) could be resolved by gene duplication, which allows the duplicate (paralog) and ancestral genes to specialize in different functions (Gallach and Betrán 2011). Indeed, CenH3 genes have also undergone repeated gene duplications not just in plant but also in several animal species including cows, fruit flies, mosquitoes, and nematodes (Li and Huang 2008; Zedek and Bureš 2016; Kursel and Malik 2017; Ishii, et al 2020; Kursel, et al 2020; Despot-Slade, et al 2021; Elisafenko, et al 2021; Kursel, et al 2021). Cytological evidence in Drosophila virilis suggests that divergent CenH3 paralogs can acquire separate, tissue-specific functions (Kursel, et al 2021).…”

“…Indeed, CenH3 genes have also undergone repeated gene duplications not just in plant but also in several animal species including cows, fruit flies, mosquitoes, and nematodes (Li and Huang 2008; Zedek and Bureš 2016; Kursel and Malik 2017; Ishii, et al 2020; Kursel, et al 2020; Despot-Slade, et al 2021; Elisafenko, et al 2021; Kursel, et al 2021). Cytological evidence in Drosophila virilis suggests that divergent CenH3 paralogs can acquire separate, tissue-specific functions (Kursel, et al 2021).…”

An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development

“…The ‘out-of-testis’ hypothesis predicts that the male germline provides an initial ‘gene nursery’ for evolutionary innovation, with diversification subsequently broadening its expression profile ( Assis and Bachtrog, 2013 ; Vinckenbosch et al, 2006 ; Nyberg and Carthew, 2017 ). Recent studies of histone variants, which were originally thought to be ‘testis-specific’ in Drosophila and mammals, based on RT-PCR data, demonstrated that their expression and function also extends to females ( Kursel et al, 2021 ; Molaro, 2020 ). Similarly, Umbrea, which is highly testis-enriched, is required for chromosome segregation more broadly ( Ross et al, 2013 ).…”