Recurrent Gene Duplication Leads to Diverse Repertoires of Centromeric Histones in Drosophila Species.
Despite their essential role in the process of chromosome segregation in most eukaryotes, centromeric histones show remarkable evolutionary lability. Not only have they been lost in multiple insect lineages, but they have also undergone gene duplication in multiple plant lineages. Based on detailed study of a handful of model organisms including Drosophila melanogaster, centromeric histone duplication is considered to be rare in animals. Using a detailed phylogenomic study, we find that Cid, the centromeric histone gene, has undergone at least four independent gene duplications during Drosophila evolution. We find duplicate Cid genes in D. eugracilis (Cid2), in the montium species subgroup (Cid3, Cid4) and in the entire Drosophila subgenus (Cid5). We show that Cid3, Cid4, and Cid5 all localize to centromeres in their respective species. Some Cid duplicates are primarily expressed in the male germline. With rare exceptions, Cid duplicates have been strictly retained after birth, suggesting that they perform nonredundant centromeric functions, independent from the ancestral Cid. Indeed, each duplicate encodes a distinct N-terminal tail, which may provide the basis for distinct protein-protein interactions. Finally, we show some Cid duplicates evolve under positive selection whereas others do not. Taken together, our results support the hypothesis that Drosophila Cid duplicates have subfunctionalized. Thus, these gene duplications provide an unprecedented opportunity to dissect the multiple roles of centromeric histones.
Molecular and Cellular Biology Graduate Program, University of Washington, Seattle, WA.|Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA.
Lisa E
LE
Kursel
Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA.|Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, Seattle, WA.
Harmit S
HS
Malik
D000595:Amino Acid Sequence; D000818:Animals; D002503:Centromere / Q000235:genetics* / Q000378:metabolism; D000076247:Centromere Protein A; D004268:DNA-Binding Proteins / Q000235:genetics*; D029721:Drosophila Proteins / Q000235:genetics*; D004331:Drosophila melanogaster / Q000235:genetics*; D019143:Evolution, Molecular; D005785:Gene Conversion / Q000235:genetics; D020440:Gene Duplication / Q000235:genetics; D006657:Histones / Q000235:genetics* / Q000378:metabolism; D008957:Models, Genetic; D010802:Phylogeny; D012641:Selection, Genetic / Q000235:genetics
D000076247:Centromere Protein A; C427237:Cid protein, Drosophila; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D006657:Histones
gene conversion; molecular evolution; positive selection; protein motifs