RRC ID 47649
Author Landeen EL, Muirhead CA, Wright L, Meiklejohn CD, Presgraves DC.
Title Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline.
Journal PLoS Biol
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.
Volume 14(7)
Pages e1002499
Published 2016-7-1
DOI 10.1371/journal.pbio.1002499
PII PBIOLOGY-D-16-00236
PMID 27404402
PMC PMC4942098
MeSH Animals Base Sequence Conserved Sequence Drosophila Proteins / biosynthesis Drosophila Proteins / genetics Drosophila melanogaster / genetics* Female Genes, Essential Genes, X-Linked Germ Cells / metabolism Male Promoter Regions, Genetic Testis / metabolism Transcription, Genetic* X Chromosome X Chromosome Inactivation*
IF 7.076
Times Cited 18
WOS Category BIOLOGY BIOCHEMISTRY & MOLECULAR BIOLOGY
Resource
Drosophila DGRC#102067