ArticlePLoS biology2016
Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline.
Article in PLoS biology, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 32 papers.
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32 citing papers in PubMed, 49 citations in OpenAlex.
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- Single-cell consequences of X-linked meiotic drive in stalk-eyed flies.PLoS genetics · 2025Article
- Meiotic Sex Chromosome Inactivation: Conservation across the Drosophila genus.PLoS genetics · 2025Article
- Single cell RNA-sequencing reveals no evidence for meiotic sex chromosome inactivation in the threespine stickleback fish.bioRxiv : the preprint server for biology · 2025Article
- Different complex regulatory phenotypes underlie hybrid male sterility in divergent rodent crosses.Genetics · 2025Article
- Different complex regulatory phenotypes underlie hybrid male sterility in divergent rodent crosses.bioRxiv : the preprint server for biology · 2024Article
- Comprehensive Identification and Characterization of HML-9 Group in Chimpanzee Genome.Viruses · 2024Article
- Single-cell RNA-seq of Drosophila miranda testis reveals the evolution and trajectory of germline sex chromosome regulation.PLoS biology · 2024Article
- scRNA-seq Reveals Novel Genetic Pathways and Sex Chromosome Regulation in Tribolium Spermatogenesis.Genome biology and evolution · 2024Article
- Sex-specific estimation of cis and trans regulation of gene expression in heads and gonads of Drosophila melanogaster.G3 (Bethesda, Md.) · 2023Article
- Unraveling patterns of disrupted gene expression across a complex tissue.Evolution; international journal of organic evolution · 2022Article
- Population biology of accessory gland-expressed de novo genes in Drosophila melanogaster.Genetics · 2022Article
- Rhino breaks the deadlock in Drosophila testis.PLoS genetics · 2021Article
- A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster.PLoS genetics · 2021Article
- Single-cell RNA-sequencing reveals pre-meiotic X-chromosome dosage compensation in Drosophila testis.PLoS genetics · 2021Article
- Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From theFrontiers in genetics · 2021Review
- The Influence of Chromosomal Environment on X-Linked Gene Expression in Drosophila melanogaster.Genome biology and evolution · 2020Article
- The Y Chromosome as a Battleground for Intragenomic Conflict.Trends in genetics : TIG · 2020Review
- Article
- High-resolution transcriptional profiling of Anopheles gambiae spermatogenesis reveals mechanisms of sex chromosome regulation.Scientific reports · 2019Article
Corrections and comments
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Authors and funding
5 authors at 3 institutions in 1 country.
Funding
No grant is acknowledged in the PubMed record.
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.
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