| 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 |
