Epialleles, generally referring to alleles whose expression is altered due to differential DNA methylation levels, have important roles in plant morphology, development, and various physiological processes. However, the influence of environmental factors on the plant epialleles under natural conditions is unclear. Meanwhile, the role and mechanism of epialleles in the environmental adaptive evolution of plants remain elusive. In this study, we collected the transcriptome, methylome and climate data from 623 Arabidopsis accessions, derived from worldwide distributions. Then the data were subject to multi-omics association analysis combined with protein interaction network and gene enrichment analysis to identify epialleles related to specific environmental factors and to explore their possible mechanisms involved in the environmental adaptive evolution of Arabidopsis thaliana. We focused on spring and summer precipitation and identified five potential epialleles with differential DNA methylation levels located in specific regions of the genes: AGL36, AT2G34100, AT4G09360, LSU4 and AT5G56910. Interestingly, the imprinted gene AGL36 related to seed development was discovered as an epiallele involved in the environmental adaptive evolution of Arabidopsis thaliana, and the other four genes are related to the response to biotic stress. By protein interaction, GO enrichment, and KEGG pathway analysis, we also found that LSU4 may participate in the sulfur metabolism network like other members of the LSU gene family, and be involved in the biotic stress response by affecting glucosinolate metabolism. In natural conditions low precipitation may affect the severity of local pests and diseases. Therefore, we speculate that DNA methylation associates with the expression of the four genes to regulate the resistance of Arabidopsis thaliana to local pests and diseases, and ultimately participates in the adaptation to local environments.
表观等位基因一般是指仅由DNA甲基化差异引起的表达量不同的等位基因,对植物形态结构和各种生理过程具有重要影响。但自然条件下环境因素对植物表观等位基因的影响还不清楚,同时表观等位基因在植物环境适应性进化中的作用和机制还亟待探究。为了在全基组水平鉴定拟南芥(Arabidopsis thaliana)中与特定环境因素相关的表观等位基因,并分析它们参与拟南芥环境适应性进化的可能机制,本研究利用623株拟南芥生态型的转录组、甲基化组和种源地气候数据进行多组学关联分析,并同时进行了蛋白互作网络和基因富集分析。以春季和夏季降水量为例,本研究最终鉴定到5个基因(AGL36、AT2G34100、AT4G09360、LSU4和AT5G56910)可能具有相应的表观等位基因,基因内部或附近特定区域不同甲基化水平对它们的表达可能具有调控作用。其中与种子发育有关的印记基因AGL36首次被发现可能作为表观等位基因参与拟南芥环境适应性进化,其他4个基因均与生物胁迫响应有关。自然条件下降水量能影响当地病虫害的严重程度,而DNA甲基化能通过影响这4个免疫基因的表达来影响拟南芥免疫能力。在长期演化过程中有利于个体适应当地降水模式的表观等位基因受到正向选择,这可能是这些表观等位基因参与拟南芥降水适应性进化的潜在机制。通过蛋白互作网络、GO功能分析和KEGG通路分析,本研究还首次发现LSU4可能与LSU基因家族其他成员一样参与硫代谢网络,并通过影响硫代葡萄糖苷代谢参与拟南芥生物胁迫响应。.
Keywords: Arabidopsis thaliana; environmental adaptive evolution; epiallele; multi-omics association analysis; plant ecological epigenetics.