Population wide methylome analysis

DNA methylation is an important chromatin modification involved in the transcriptional regulation of gene and transposable elements. Heritable changes in DNA methylation, so-called epialleles, can lead to variations in gene expression and phenotypic traits, with potential implications for crop diversity, as exemplified by fruit ripening or vitamin E variation in tomato. However, our understanding of intraspecific DNA methylation variation in crops, its potential causes, and phenotypic consequences remains limited. Here, we characterise the methylomes of 183 tomato accessions, including wild species, early domesticated and modern cultivars. We identified over 2 million differentially methylated regions that, although delineating global phylogenetic relationships among accessions, exhibit a rapid decay of linkage disequilibrium, indicative of partial independence from genetic variation. Indeed, we found that the strong domestication and improvement sweeps imprinted in the genome are largely absent from the epigenome. Such uncoupling could be accounted for by the remarkably fast epigenetic substitution rate, which decelerates with increased divergences. Last, we show that DNA methylation states are associated with gene expression levels and using epigenome wide association studies we identified epialleles potentially underlying natural variations in metabolic traits in leaves. Our comprehensive epigenomic study uncovered the sources of natural epigenetic variation, its population dynamics, and contribution to tomato diversity.