Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline

Emily L. Landeen, Christina A. Muirhead, Lori Wright, Colin D Meiklejohn, Daven C. Presgraves

Research output: Contribution to journalArticle

15 Citations (Scopus)

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.

Original languageEnglish (US)
Article numbere1002499
JournalPLoS biology
Volume14
Issue number7
DOIs
StatePublished - Jul 12 2016

Fingerprint

Sex Chromosomes
sex chromosomes
Gene expression
Drosophila
germ cells
Genes
Testis
testes
Gene Expression
gene expression
X-Linked Genes
X Chromosome
Chromosomes
X chromosome
genes
promoter regions
Transgenes
transgenes
inactivation
sex linkage

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline. / Landeen, Emily L.; Muirhead, Christina A.; Wright, Lori; Meiklejohn, Colin D; Presgraves, Daven C.

In: PLoS biology, Vol. 14, No. 7, e1002499, 12.07.2016.

Research output: Contribution to journalArticle

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