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Multi-omics association analysis revealed the role and mechanism of epialleles in environmental adaptive evolution of Arabidopsis thaliana.

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.