title: Recurrent Gene Duplication Diversifies Genome Defense Repertoire in Drosophila.
abstract: Transposable elements (TEs) comprise large fractions of many eukaryotic genomes and imperil host genome integrity. The host genome combats these challenges by encoding proteins that silence TE activity. Both the introduction of new TEs via horizontal transfer and TE sequence evolution requires constant innovation of host-encoded TE silencing machinery to keep pace with TEs. One form of host innovation is the adaptation of existing, single-copy host genes. Indeed, host suppressors of TE replication often harbor signatures of positive selection. Such signatures are especially evident in genes encoding the piwi-interacting-RNA pathway of gene silencing, for example, the female germline-restricted TE silencer, HP1D/Rhino Host genomes can also innovate via gene duplication and divergence. However, the importance of gene family expansions, contractions, and gene turnover to host genome defense has been largely unexplored. Here, we functionally characterize Oxpecker, a young, tandem duplicate gene of HP1D/rhino We demonstrate that Oxpecker supports female fertility in Drosophila melanogaster and silences several TE families that are incompletely silenced by HP1D/Rhino in the female germline. We further show that, like Oxpecker, at least ten additional, structurally diverse, HP1D/rhino-derived daughter and "granddaughter" genes emerged during a short 15-million year period of Drosophila evolution. These young paralogs are transcribed primarily in germline tissues, where the genetic conflict between host genomes and TEs plays out. Our findings suggest that gene family expansion is an underappreciated yet potent evolutionary mechanism of genome defense diversification.
authors.affiliation: Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA.
authors.forename: Mia T
authors.initials: MT
authors.lastname: Levine
authors.affiliation: Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA.
authors.forename: Helen M
authors.initials: HM
authors.lastname: Vander Wende
authors.affiliation: Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA.
authors.forename: Emily
authors.initials: E
authors.lastname: Hsieh
authors.affiliation: Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA.
authors.forename: EmilyClare P
authors.initials: EP
authors.lastname: Baker
authors.affiliation: Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, Seattle, hsmalik@fhcrc.org.
authors.forename: Harmit S
authors.initials: HS
authors.lastname: Malik
mesh_terms: D000818:Animals; D002868:Chromosomal Proteins, Non-Histone / Q000235:genetics*; D004251:DNA Transposable Elements / Q000235:genetics; D029721:Drosophila Proteins / Q000235:genetics*; D004331:Drosophila melanogaster / Q000235:genetics*; D019143:Evolution, Molecular; D005260:Female; D020440:Gene Duplication; D020868:Gene Silencing; D014644:Genetic Variation; D049750:Genome, Insect; D042822:Genomic Instability; D034741:RNA, Small Interfering / Q000235:genetics; D012641:Selection, Genetic
chemical_list: D002868:Chromosomal Proteins, Non-Histone; D004251:DNA Transposable Elements; D029721:Drosophila Proteins; D034741:RNA, Small Interfering; C449641:rhi protein, Drosophila
keywords: HP1 proteins; gene duplication; genome defense; heterochromatin; transposable elements