Epigenetic diversity of genes with copy number variations among natural populations of the three-spined stickleback

IF 3.5 2区 生物学 Q1 EVOLUTIONARY BIOLOGY
Frédéric J. J. Chain, Britta S. Meyer, Melanie J. Heckwolf, Sören Franzenburg, Christophe Eizaguirre, Thorsten B. H. Reusch
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Abstract

Duplicated genes provide the opportunity for evolutionary novelty and adaptive divergence. In many cases, having more gene copies increases gene expression, which might facilitate adaptation to stressful or novel environments. Conversely, overexpression or misexpression of duplicated genes can be detrimental and subject to negative selection. In this scenario, newly duplicate genes may evade purifying selection if they are epigenetically silenced, at least temporarily, leading them to persist in populations as copy number variations (CNVs). In animals and plants, younger gene duplicates tend to have higher levels of DNA methylation and lower levels of gene expression, suggesting epigenetic regulation could promote the retention of gene duplications via expression repression or silencing. Here, we test the hypothesis that DNA methylation variation coincides with young duplicate genes that are segregating as CNVs in six populations of the three-spined stickleback that span a salinity gradient from 4 to 30 PSU. Using reduced-representation bisulfite sequencing, we found DNA methylation and CNV differentiation outliers rarely overlapped. Whereas lineage-specific genes and young duplicates were found to be highly methylated, just two gene CNVs showed a significant association between promoter methylation level and copy number, suggesting that DNA methylation might not interact with CNVs in our dataset. If most new duplications are regulated for dosage by epigenetic mechanisms, our results do not support a strong contribution from DNA methylation soon after duplication. Instead, our results are consistent with a preference to duplicate genes that are already highly methylated.

Abstract Image

三刺鱼自然种群中拷贝数变异基因的表观遗传多样性。
重复的基因为进化的新颖性和适应性分化提供了机会。在许多情况下,拥有更多的基因拷贝可以增加基因表达,从而促进对压力或新环境的适应。反之,重复基因的过度表达或表达不当也可能是有害的,会受到负面选择的影响。在这种情况下,新复制的基因如果在表观遗传学上被沉默(至少是暂时沉默),就可能逃避纯化选择,从而以拷贝数变异(CNV)的形式在种群中持续存在。在动物和植物中,较年轻的重复基因往往具有较高的DNA甲基化水平和较低的基因表达水平,这表明表观遗传调控可通过表达抑制或沉默促进重复基因的保留。在此,我们在盐度梯度为 4 至 30 PSU 的六个三刺鱼种群中检验了 DNA 甲基化变异与作为 CNVs 分离的年轻重复基因相吻合的假设。通过减少代表性的亚硫酸氢盐测序,我们发现 DNA 甲基化和 CNV 分化异常值很少重叠。我们发现特定品系的基因和年轻的重复基因甲基化程度很高,而只有两个基因的CNV在启动子甲基化水平和拷贝数之间存在显著关联,这表明在我们的数据集中,DNA甲基化可能与CNV之间没有相互作用。如果大多数新的重复是通过表观遗传机制来调节剂量的,那么我们的结果并不支持 DNA 甲基化在重复后不久就会产生强大的贡献。相反,我们的结果符合人们对已经高度甲基化基因的复制偏好。
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来源期刊
Evolutionary Applications
Evolutionary Applications 生物-进化生物学
CiteScore
8.50
自引率
7.30%
发文量
175
审稿时长
6 months
期刊介绍: Evolutionary Applications is a fully peer reviewed open access journal. It publishes papers that utilize concepts from evolutionary biology to address biological questions of health, social and economic relevance. Papers are expected to employ evolutionary concepts or methods to make contributions to areas such as (but not limited to): medicine, agriculture, forestry, exploitation and management (fisheries and wildlife), aquaculture, conservation biology, environmental sciences (including climate change and invasion biology), microbiology, and toxicology. All taxonomic groups are covered from microbes, fungi, plants and animals. In order to better serve the community, we also now strongly encourage submissions of papers making use of modern molecular and genetic methods (population and functional genomics, transcriptomics, proteomics, epigenetics, quantitative genetics, association and linkage mapping) to address important questions in any of these disciplines and in an applied evolutionary framework. Theoretical, empirical, synthesis or perspective papers are welcome.
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