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.
Highlights
Heteromorphic sex chromosomes—e.g., XY males in Drosophila and mammals and ZW females in birds and butterflies—have evolved independently numerous times in animals and in plants [1,2]
Understanding how the X is regulated in the male germline has implications for gene expression, the evolution of sex chromosome-specific gene content, and speciation
We show that the X chromosome has evolved strong testis-specific promoters via the gene-by-gene recruitment of sequence elements that counteract transcriptional suppression of the X chromosome
Summary
Heteromorphic sex chromosomes—e.g., XY males in Drosophila and mammals and ZW females in birds and butterflies—have evolved independently numerous times in animals and in plants [1,2]. Two types of sex chromosome regulation have evolved independently in disparate taxa: sex chromosome dosage compensation, a process that results in roughly equal X:autosome expression levels between the sexes [9,10], and meiotic sex chromosome inactivation (MSCI), the precocious heterochromatinization and transcriptional silencing of the sex chromosomes during meiosis I in the heterogametic sex [11,12,13]. Sex chromosome dosage compensation has evolved in taxa with XY (Drosophila, mammal), XO (nematode), and, to varying degrees, ZW systems [14,15,16,17]. Sex chromosome-specific dosage compensation up-regulates X-linked genes a further ~1.35-fold via the recruitment of the Male-Specific Lethal (MSL) protein-RNA complex to chromatin entry sites enriched for a GA-rich ~21-bp MSL recognition element (MRE) [20,21]. In several Drosophila lineages, neo-X chromosomes—i.e., ancestral autosomes that segregate as sex chromosomes—have independently co-opted MSL-mediated dosage compensation via the de novo evolution of MREs [22,23,24]
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