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Evolutionarily young genes that serve essential functions represent a paradox; they must perform a function that either was not required until after their birth or was redundant with another gene. How young genes rapidly acquire essential function is largely unknown. We traced the evolutionary steps by which the Drosophila gene Umbrea acquired an essential role in chromosome segregation in D. melanogaster since the gene's origin less than 15 million years ago. Umbrea neofunctionalization occurred via loss of an ancestral heterochromatin-localizing domain, followed by alterations that rewired its protein interaction network and led to species-specific centromere localization. Our evolutionary cell biology approach provides temporal and mechanistic detail about how young genes gain essential function. Such innovations may constantly alter the repertoire of centromeric proteins in eukaryotes.

Heterochromatin is the gene-poor, satellite-rich eukaryotic genome compartment that supports many essential cellular processes. The functional diversity of proteins that bind and often epigenetically define heterochromatic DNA sequence reflects the diverse functions supported by this enigmatic genome compartment. Moreover, heterogeneous signatures of selection at chromosomal proteins often mirror the heterogeneity of evolutionary forces that act on heterochromatic DNA. To identify new such surrogates for dissecting heterochromatin function and evolution, we conducted a comprehensive phylogenomic analysis of the Heterochromatin Protein 1 gene family across 40 million years of Drosophila evolution. Our study expands this gene family from 5 genes to at least 26 genes, including several uncharacterized genes in Drosophila melanogaster. The 21 newly defined HP1s introduce unprecedented structural diversity, lineage-restriction, and germline-biased expression patterns into the HP1 family. We find little evidence of positive selection at these HP1 genes in both population genetic and molecular evolution analyses. Instead, we find that dynamic evolution occurs via prolific gene gains and losses. Despite this dynamic gene turnover, the number of HP1 genes is relatively constant across species. We propose that karyotype evolution drives at least some HP1 gene turnover. For example, the loss of the male germline-restricted HP1E in the obscura group coincides with one episode of dramatic karyotypic evolution, including the gain of a neo-Y in this lineage. This expanded compendium of ovary- and testis-restricted HP1 genes revealed by our study, together with correlated gain/loss dynamics and chromosome fission/fusion events, will guide functional analyses of novel roles supported by germline chromatin., Competing Interests: HSM is a Section Editor of PLoS Genetics.

Heterochromatin is the gene-poor, transposon-rich, late-replicating chromatin compartment that was first cytologically defined more than 70 years ago. The identification of heterochromatin protein 1 (HP1) paved the way for a molecular dissection of this important component of complex eukaryotic genomes. Although initial studies revealed HP1's key role in heterochromatin maintenance and function, more recent studies have discovered a role for HP1 in numerous processes including, surprisingly, euchromatic gene expression. Drosophila genomes possess at least five HP1 paralogs that have significantly different roles, ranging from canonical heterochromatic function at pericentric and telomeric regions to exclusive localization and regulation of euchromatic genes. They also possess paralogs exclusively involved in defending the germline against mobile elements. Pursuing a survey of recent genetic and evolutionary findings, we highlight how Drosophila genomes represent the best opportunity to dissect the diversity and incredible versatility of HP1 proteins in organizing and protecting eukaryotic genomes.

Centromeres require specialized nucleosomes; however, the mechanism of localization is unknown. Drosophila sp. centromeric nucleosomes contain the Cid H3-like protein. We have devised a strategy for identifying elements within Cid responsible for its localization to centromeres. By expressing Cid from divergent Drosophila species fused to green fluorescent protein in Drosophila melanogaster cells, we found that D. bipectinata Cid fails to localize to centromeres. Cid chimeras consisting of the D. bipectinata histone fold domain (HFD) replaced with segments from D. melanogaster identified loop I of the HFD as being critical for targeting to centromeres. Conversely, substitution of D. bipectinata loop I into D. melanogaster abolished centromeric targeting. In either case, loop I was the only segment capable of conferring targeting. Within loop I, we identified residues that are critical for targeting. Most mutations of conserved residues abolished targeting, and length reductions were deleterious. Taken together with the fact that H3 loop I makes numerous contacts with DNA and with the adaptive evolution of Cid, our results point to the importance of DNA specificity for targeting. We suggest that the process of deposition of (Cid.H4)2 tetramers allows for discriminating contacts to be made between loop I and DNA, providing the specificity needed for targeting.