Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline
Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline
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DOI：
10.1371/journal.pbio.1002499
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发表时间：
2016-07-01
期刊：
影响因子：
9.8
通讯作者：
Presgraves, Daven C.
中科院分区：
文献类型：
--
作者：
Landeen, Emily L.;Muirhead, Christina A.;Presgraves, Daven C.
异形性染色体的进化多次导致性染色体特异性调控形式的进化，包括体细胞中的性染色体剂量补偿和种系中的减数分裂性染色体失活。在果蝇的雄性种系中，出现了一种新颖但知之甚少的性染色体特异性转录调控形式，它与典型的性染色体剂量补偿或减数分裂失活不同。先前的研究表明，与常染色体位置相比，插入 X 染色体的转基因由睾丸特异性启动子驱动的报告基因的表达要低得多，大约低 3 倍或更多。在这里，我们描述了雄性种系中 X 连锁基因的转录抑制及其进化后果。通过转基因和转座，我们发现大多数内源性 X 连锁基因（不仅仅是睾丸特异性基因）在果蝇雄性种系中的转录被抑制数倍。在野生型睾丸中，这种性染色体范围内的转录抑制通常无法检测到，但可以通过 X 染色体上强启动子的逐个基因进化招募来有效补偿。我们鉴定并通过实验验证了一个启动子元件序列基序，该基序富集在数百个睾丸表达基因的转录起始位点的上游；在物种间进化上保守；与睾丸中强基因表达水平相关；并且在 X 染色体上的比例过高。这些发现表明，果蝇睾丸中X连锁基因的表达反映了全染色体表观遗传转录抑制与性连锁基因的长期补偿性适应之间的平衡。我们的结果对果蝇雄性种系基因表达的进化和基因组进化具有广泛的影响。
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.