title: Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline.
abstract: The evolution of heteromorphic sex chromosomes has repeatedly resulted in the evolution of sex chromosome-specific forms of regulation, including sex chromosome dosage compensation in the soma and meiotic sex chromosome inactivation in the germline. In the male germline of Drosophila melanogaster, a novel but poorly understood form of sex chromosome-specific transcriptional regulation occurs that is distinct from canonical sex chromosome dosage compensation or meiotic inactivation. Previous work shows that expression of reporter genes driven by testis-specific promoters is considerably lower-approximately 3-fold or more-for transgenes inserted into X chromosome versus autosome locations. Here we characterize this transcriptional suppression of X-linked genes in the male germline and its evolutionary consequences. Using transgenes and transpositions, we show that most endogenous X-linked genes, not just testis-specific ones, are transcriptionally suppressed several-fold specifically in the Drosophila male germline. In wild-type testes, this sex chromosome-wide transcriptional suppression is generally undetectable, being effectively compensated by the gene-by-gene evolutionary recruitment of strong promoters on the X chromosome. We identify and experimentally validate a promoter element sequence motif that is enriched upstream of the transcription start sites of hundreds of testis-expressed genes; evolutionarily conserved across species; associated with strong gene expression levels in testes; and overrepresented on the X chromosome. These findings show that the expression of X-linked genes in the Drosophila testes reflects a balance between chromosome-wide epigenetic transcriptional suppression and long-term compensatory adaptation by sex-linked genes. Our results have broad implications for the evolution of gene expression in the Drosophila male germline and for genome evolution.
authors.affiliation: Department of Biology, University of Rochester, Rochester, New York, United States of America.
authors.forename: Emily L
authors.initials: EL
authors.lastname: Landeen
authors.affiliation: Department of Biology, University of Rochester, Rochester, New York, United States of America.|The Ronin Institute, Montclair, New Jersey, United States of America.
authors.forename: Christina A
authors.initials: CA
authors.lastname: Muirhead
authors.affiliation: Department of Biology, University of Rochester, Rochester, New York, United States of America.
authors.forename: Lori
authors.identifier: 0000-0003-3017-6608
authors.initials: L
authors.lastname: Wright
authors.affiliation: School of Biological Sciences, University of Nebraska, Lincoln, Nebraska, United States of America.
authors.forename: Colin D
authors.initials: CD
authors.lastname: Meiklejohn
authors.affiliation: Department of Biology, University of Rochester, Rochester, New York, United States of America.
authors.forename: Daven C
authors.initials: DC
authors.lastname: Presgraves
mesh_terms: D000818:Animals; D001483:Base Sequence; D017124:Conserved Sequence; D029721:Drosophila Proteins / Q000096:biosynthesis / Q000235:genetics; D004331:Drosophila melanogaster / Q000235:genetics*; D005260:Female; D020043:Genes, Essential; D050172:Genes, X-Linked; D005854:Germ Cells / Q000378:metabolism; D008297:Male; D011401:Promoter Regions, Genetic; D013737:Testis / Q000378:metabolism; D014158:Transcription, Genetic; D014960:X Chromosome; D049951:X Chromosome Inactivation
chemical_list: D029721:Drosophila Proteins