Papers in the Biological Sciences
Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis- Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline
© 2016 Landeen et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
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 wildtype
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.