Papers in the Biological Sciences

 

Date of this Version

2016

Citation

Landeen EL, Muirhead CA, Wright L, Meiklejohn CD, Presgraves DC (2016) Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline. PLoS Biol 14(7): e1002499.

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© 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.

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