Transposon wave remodeled the epigenomic landscape in the rapid evolution of X-Chromosome dosage compensation

Transposon wave remodeled the epigenomic landscape in the rapid evolution of X-Chromosome dosage compensation
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DOI:
10.1101/gr.278127.123
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发表时间:
2023-11-01
期刊:
影响因子:
7
通讯作者:
Mank,Judith E.
Mank,Judith E.
中科院分区:
生物学1区
文献类型:
--
作者:
Metzger,David C. H.;Porter,Imogen;Mank,Judith E.

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性染色体剂量补偿是理解转录协调进化的模型;然而,模型系统中性染色体的高龄使得难以研究染色体范围剂量补偿的复杂调控机制如何进化。Poecilia picta的性染色体最近发生了迅速的分化,导致雄性Y染色体上广泛的基因丢失,加上完整的X染色体剂量补偿,这是鱼类中报道的第一例。最近的从头起源的剂量补偿提供了一个独特的机会,了解协调染色体基因调控的遗传和进化基础。通过将一个新的染色体水平组装的P。picta与全基因组亚硫酸氢盐测序和RNA-seq数据,我们确定YY 1转录因子(YY 1)DNA结合基序与X上的男性特异性低甲基化区域相关,但不与常染色体相关。这些YY 1基序是最近在P上快速重复元件扩展的结果。pictaX染色体,在缺乏剂量补偿的近缘物种中不存在。总之,我们的研究结果提供了令人信服的支持,即携带YY 1基序的重复元件插入的破坏性浪潮导致了X染色体表观基因组景观的重塑和剂量补偿系统的快速从头起源。
Sex chromosome dosage compensation is a model to understand the coordinated evolution of transcription; however, the advanced age of the sex chromosomes in model systems makes it difficult to study how the complex regulatory mechanisms underlying chromosome-wide dosage compensation can evolve. The sex chromosomes ofPoecilia pictahave undergone recent and rapid divergence, resulting in widespread gene loss on the male Y, coupled with complete X Chromosome dosage compensation, the first case reported in a fish. The recent de novo origin of dosage compensation presents a unique opportunity to understand the genetic and evolutionary basis of coordinated chromosomal gene regulation. By combining a new chromosome-level assembly ofP. pictawith whole-genome bisulfite sequencing and RNA-seq data, we determine that the YY1 transcription factor (YY1) DNA binding motif is associated with male-specific hypomethylated regions on the X, but not the autosomes. These YY1 motifs are the result of a recent and rapid repetitive element expansion on theP. pictaX Chromosome, which is absent in closely related species that lack dosage compensation. Taken together, our results present compelling support that a disruptive wave of repetitive element insertions carrying YY1 motifs resulted in the remodeling of the X Chromosome epigenomic landscape and the rapid de novo origin of a dosage compensation system.