Plant Conservation and Population Biology, University of Leuven, Kasteelpark Arenberg 31-2435, BE-3001, Leuven, Belgium.
Department of Agricultural Sciences, Viikki Plant Science Centre, University of Helsinki, Latokartanonkaari 7, 00790, Helsinki, Finland.
New Phytol. 2022 Aug;235(4):1501-1514. doi: 10.1111/nph.18225. Epub 2022 Jun 10.
Epigenetic inheritance can drive adaptive evolution independently of DNA sequence variation. However, to what extent epigenetic variation represents an autonomous evolutionary force remains largely elusive. Through gene ontology and comparative analyses of genomic and epigenomic variation of wild strawberry plants raised in distinct drought settings, we characterised genome-wide covariation between single nucleotide polymorphisms (SNPs) and differentially methylated cytosines (DMCs). Covariation between SNPs and DMCs was independent of genomic proximity, but instead associated with fitness-related processes such as stress responses, genome regulation and reproduction. We expected this functional SNP-DMC covariation to be driven by adaptive evolution canalising SNP and DMC variation, but instead observed significantly lower covariation with DMCs for adaptive rather than for neutral SNPs. Drought-induced DMCs frequently co-varied with tens of SNPs, suggesting high genomic redundancy as a broad potential basis for polygenic adaptation of gene expression. Our findings suggest that stress-responsive DMCs initially co-vary with many SNPs under increased environmental stress, and that natural selection acting upon several of these SNPs subsequently reduces standing covariation with stress-responsive DMCs. Our study supports DNA methylation profiles that represent complex quantitative traits rather than autonomous evolutionary forces. We provide a conceptual framework for polygenic regulation and adaptation shaping genome-wide methylation patterns in plants.
表观遗传继承可以独立于 DNA 序列变异驱动适应性进化。然而，表观遗传变异在多大程度上代表了一种自主的进化力量，在很大程度上仍然难以捉摸。通过对在不同干旱环境中培养的野生草莓植物的基因组和表观基因组变异进行基因本体论和比较分析，我们描述了单核苷酸多态性 (SNP) 和差异甲基化胞嘧啶 (DMC) 之间全基因组的共变关系。SNP 和 DMC 之间的共变与基因组的接近程度无关，而是与与适应相关的过程（如应激反应、基因组调控和繁殖）相关联。我们期望这种与功能相关的 SNP-DMC 共变是由适应进化对 SNP 和 DMC 变异的定向作用驱动的，但实际上我们观察到，与中性 SNP 相比，适应性 SNP 与 DMC 的共变显著降低。干旱诱导的 DMC 经常与数十个 SNP 共变，这表明高基因组冗余是基因表达多基因适应的广泛潜在基础。我们的研究结果表明，最初在环境压力增加下，应激响应的 DMC 与许多 SNP 共变，而自然选择对其中的一些 SNP 起作用后，与应激响应的 DMC 的共变减少。我们的研究支持 DNA 甲基化图谱代表复杂的定量性状，而不是自主的进化力量。我们为多基因调控和适应提供了一个概念框架，塑造了植物全基因组甲基化模式。
