Faster-X evolution of gene expression in Drosophila.

Faster-X evolution of gene expression in Drosophila.
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DOI:
10.1371/journal.pgen.1003013
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发表时间:
2012
期刊:
影响因子:
4.5
通讯作者:
Clark AG
Clark AG
中科院分区:
生物学2区
文献类型:
--
作者:
Meisel RP;Malone JH;Clark AG

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X染色体上的DNA序列通常比常染色体上的类似基因座进化速度更快,并且清晰的模型提供了X连锁遗传模式可能导致X连锁基因更快进化的原因。我们分析了从六种果蝇的雌性和雄性中收集的微阵列和RNA-seq数据,发现X连锁基因的表达水平也比常染色体基因表达更快地发散,类似于DNA序列进化中经常观察到的“faster-X”效应。最近在哺乳动物中描述了基因表达的快速X进化,但它仅限于兽X染色体产生后不久的进化谱系。相比之下,我们检测到一个更快的X效应沿着深谱系和那些对提示的果蝇染色体。在果蝇雄性中,剂量补偿复合物(DCC)结合X染色体,创造了一个独特的染色质环境,促进X连锁基因的超表达。我们发现,DCC结合,染色质环境,和表达的广度都是预测基因表达进化的速度。此外,种内遗传多态性的基因表达变异的估计表明,X连锁的表达水平不放松的选择性约束。因此,我们假设基因表达的快速X进化是在X连锁基因座上改变顺式表达水平的有益突变的适应性固定的结果。这种适应性的基因表达的快速X进化仅限于在单一组织中狭窄表达的基因,这表明放松的多效性限制允许对选择的更快反应。最后,我们提出了一个概念框架来解释快速X表达的演变,我们用这个框架来研究果蝇和哺乳动物之间的快速X效应的差异。随着物种在进化过程中的分化,它们积累了基因序列以及这些基因表达方式的差异。我们表明,基因表达的变化积累更快的基因在X染色体上的基因比其他染色体(常染色体)在果蝇(“更快的X”效应)。X染色体在男性中只有一个拷贝,而常染色体在两性中都有两个拷贝。为了补偿雄性中X连锁基因的减少,一种分子复合物结合果蝇X染色体以上调雄性中的基因表达。我们证明,逃避这种剂量补偿过程的基因具有更快的表达水平。X连锁基因以独特的方式遗传,我们假设这允许更快的适应性进化,从而驱动基因表达的更快的X进化。我们将这些观察结果与最近描述的哺乳动物基因表达的快速X进化进行比较,并解释了剂量补偿,突变率和种群大小的差异如何影响快速X效应的程度。
DNA sequences on X chromosomes often have a faster rate of evolution when compared to similar loci on the autosomes, and well articulated models provide reasons why the X-linked mode of inheritance may be responsible for the faster evolution of X-linked genes. We analyzed microarray and RNA–seq data collected from females and males of six Drosophila species and found that the expression levels of X-linked genes also diverge faster than autosomal gene expression, similar to the “faster-X” effect often observed in DNA sequence evolution. Faster-X evolution of gene expression was recently described in mammals, but it was limited to the evolutionary lineages shortly following the creation of the therian X chromosome. In contrast, we detect a faster-X effect along both deep lineages and those on the tips of the Drosophila phylogeny. In Drosophila males, the dosage compensation complex (DCC) binds the X chromosome, creating a unique chromatin environment that promotes the hyper-expression of X-linked genes. We find that DCC binding, chromatin environment, and breadth of expression are all predictive of the rate of gene expression evolution. In addition, estimates of the intraspecific genetic polymorphism underlying gene expression variation suggest that X-linked expression levels are not under relaxed selective constraints. We therefore hypothesize that the faster-X evolution of gene expression is the result of the adaptive fixation of beneficial mutations at X-linked loci that change expression level in cis. This adaptive faster-X evolution of gene expression is limited to genes that are narrowly expressed in a single tissue, suggesting that relaxed pleiotropic constraints permit a faster response to selection. Finally, we present a conceptional framework to explain faster-X expression evolution, and we use this framework to examine differences in the faster-X effect between Drosophila and mammals. As species diverge over evolutionary time, they accumulate differences in the sequences of their genes and how those genes are expressed. We show that gene expression changes accumulate faster for genes on the X chromosome than for genes on the other chromosomes (autosomes) in Drosophila (the “faster-X” effect). The X chromosome is only found in a single copy in males, whereas the autosomes are found in two copies in both sexes. To compensate for the reduced dosage of X-linked genes in males, a molecular complex binds the Drosophila X chromosome to upregulate gene expression in males. We demonstrate that genes that escape this dosage compensation process have faster evolving expression levels. X-linked genes are inherited in a unique manner, and we hypothesize that this permits a faster rate of adaptive evolution, thereby driving the faster-X evolution of gene expression. We compare these observations with the recently described faster-X evolution of gene expression in mammals, and we explain how differences in dosage compensation, mutation rate, and population size could affect the extent of the faster-X effect.
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