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.
Highlights
Chromosome segregation is an essential process that is highly conserved across eukaryotes
To gain insight into the function of Cid1 and Cid5, we investigated their localization in dividing somatic cells, ovaries, testes, and embryos of D. virilis flies
In D. melanogaster, Cid-GFP transgenic flies, in which GFP was inserted between the N-terminal tail and histone fold domain (HFD) of Cid, can complement Cid function (Schuh et al, 2007a)
Summary
Chromosome segregation is an essential process that is highly conserved across eukaryotes. Condensed chromosomes attach to the spindle via a specialized region of chromatin called the centromere, ensuring equal partitioning of DNA into daughter cells. First identified as Cenp-A in mammals (Earnshaw & Rothfield, 1985; Palmer et al, 1991), CenH3 localizes to centromeric DNA and helps recruit other components of the kinetochore, which mediates chromosome segregation. The loss of CenH3 results in catastrophic chromosome segregation defects and lethality in protists, yeast, flies, nematodes, mice, and plants (Stoler et al, 1995; Buchwitz et al, 1999; Howman et al, 2000; Blower & Karpen, 2001). Some lineages lack CenH3 altogether (Akiyoshi & Gull, 2014; Drinnenberg et al, 2014), in most eukaryotes that encode CenH3, it is essential for chromosome segregation in both mitosis and meiosis
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