Plant Evolutionary Ecology, Institute of Evolution and Ecology, University of Tübingen, Tübingen, Germany.
Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria.
PLoS Genet. 2022 Oct 12;18(10):e1010452. doi: 10.1371/journal.pgen.1010452. eCollection 2022 Oct.
Natural plant populations often harbour substantial heritable variation in DNA methylation. However, a thorough understanding of the genetic and environmental drivers of this epigenetic variation requires large-scale and high-resolution data, which currently exist only for a few model species. Here, we studied 207 lines of the annual weed Thlaspi arvense (field pennycress), collected across a large latitudinal gradient in Europe and propagated in a common environment. By screening for variation in DNA sequence and DNA methylation using whole-genome (bisulfite) sequencing, we found significant epigenetic population structure across Europe. Average levels of DNA methylation were strongly context-dependent, with highest DNA methylation in CG context, particularly in transposable elements and in intergenic regions. Residual DNA methylation variation within all contexts was associated with genetic variants, which often co-localized with annotated methylation machinery genes but also with new candidates. Variation in DNA methylation was also significantly associated with climate of origin, with methylation levels being lower in colder regions and in more variable climates. Finally, we used variance decomposition to assess genetic versus environmental associations with differentially methylated regions (DMRs). We found that while genetic variation was generally the strongest predictor of DMRs, the strength of environmental associations increased from CG to CHG and CHH, with climate-of-origin as the strongest predictor in about one third of the CHH DMRs. In summary, our data show that natural epigenetic variation in Thlaspi arvense is significantly associated with both DNA sequence and environment of origin, and that the relative importance of the two factors strongly depends on the sequence context of DNA methylation. T. arvense is an emerging biofuel and winter cover crop; our results may hence be relevant for breeding efforts and agricultural practices in the context of rapidly changing environmental conditions.
自然植物群体通常在 DNA 甲基化方面具有大量可遗传的变异。然而，要全面了解这种表观遗传变异的遗传和环境驱动因素，需要大规模的高分辨率数据，而这些数据目前仅存在于少数模式物种中。在这里，我们研究了 207 条欧洲一年生杂草拟南芥（田野菥蓂）的种群，这些种群横跨了一个很大的纬度梯度，并在一个共同的环境中繁殖。通过全基因组（亚硫酸氢盐）测序筛选 DNA 序列和 DNA 甲基化的变异，我们发现欧洲存在显著的表观遗传种群结构。平均 DNA 甲基化水平强烈依赖于上下文，CG 背景下的 DNA 甲基化程度最高，尤其是在转座元件和基因间区。所有背景下的残余 DNA 甲基化变异与遗传变异有关，这些遗传变异通常与注释的甲基化机制基因共定位，也与新的候选基因共定位。DNA 甲基化的变异也与起源地的气候显著相关，在较冷地区和气候较不稳定的地区，甲基化水平较低。最后，我们使用方差分解来评估与差异甲基化区域（DMRs）相关的遗传和环境因素。我们发现，虽然遗传变异通常是 DMRs 的最强预测因子，但环境关联的强度从 CG 增加到 CHG 和 CHH，在大约三分之一的 CHH DMRs 中，起源地的气候是最强的预测因子。总之，我们的数据表明，拟南芥的自然表观遗传变异与 DNA 序列和起源环境都有显著的关联，而这两个因素的相对重要性强烈依赖于 DNA 甲基化的序列背景。拟南芥是一种新兴的生物燃料和冬季覆盖作物；因此，我们的研究结果可能与快速变化的环境条件下的育种工作和农业实践有关。
