Asymmetric variation in DNA methylation during domestication and de-domestication of rice

Abstract

Hundreds of plant species have been domesticated to feed human civilization, while some crops have undergone de-domestication into agricultural weeds, threatening global food security. To understand the genetic and epigenetic basis of crop domestication and de-domestication, we generated DNA methylomes from 95 accessions of wild rice (Oryza rufipogon L.), cultivated rice (Oryza sativa L.) and weedy rice (Oryza sativa f. spontanea). We detected a significant decrease in DNA methylation over the course of rice domestication but observed an unexpected increase in DNA methylation through de-domestication. Notably, DNA methylation changes occurred in distinct genomic regions for these two opposite stages. Variation in DNA methylation altered the expression of nearby and distal genes through affecting chromatin accessibility, histone modifications, transcription factor binding and the formation of chromatin loops, which may contribute to morphological changes during domestication and de-domestication of rice. These insights into population epigenomics underlying rice domestication and de-domestication provide resources and tools for epigenetic breeding and sustainable agriculture.

Epigenetic differences between wild and cultivated grapevines highlight the contribution of DNA methylation during crop domestication

“…Cultivated accessions consistently exhibit significantly higher global levels of DNA methylation across all sequence contexts and all genomic features. These observations, are in contradiction with previous studies showing that domestication induces a significant decrease in DNA methylation in rice [ 29 ] and tomato [ 30 ]. This is perhaps explained by the differences in the type of propagation used during the domestication of each species (i.e., vegetative vs. sexual propagation), which could have resulted in diametrically opposed domestication epigenetic syndromes [ 2 , 6 ].…”

“…A reduction that is reversed in the resynthesized hexaploid wheat [ 27 ]. More recently, detailed analysis of DNA methylation in rice [ 29 ] and tomato [ 30 ] has shown that domesticated cultivars present lower levels of DNA methylation than their wild counterparts. Moreover, multiple studies have shown that differentially methylated regions associated to domestication overlap with genes linked to traits known to be under selection during domestication of soybean [ 31 ], tomato [ 30 ], maize [ 32 ], and cotton [ 28 ].…”

Epigenetic Regulation of Nitrogen Signaling and Adaptation in Plants

“…However, this approach primarily focuses on DNA variations within coding regions or proximal promoter regions. It is essential to recognize that variations in DNA methylation status, rather than the sequence itself, can also be associated with traits in crop plants [ 80 ], such as domestication in rice [ 81 ]. For instance, a naturally occurring DNA methylation variation in the promoter of Colorless non-ripening (Cnr) locus is associated with the fruit ripening in tomato [ 82 ], demonstrating the significance of DNA methylation in trait association.…”

The Development of Plant Genome Sequencing Technology and Its Conservation and Application in Endangered Gymnosperms

“…DNA methylation influences chromatin accessibility and histone modifications, which in turn controls the expression of nearby and distant genes throughout the domestication process of rice. Domesticated rice experiences a decrease in the DNA methylation linked to stress tolerance, but weedy rice, which can withstand more severe stress, may show an increase in this link [143]. The drought response regulatory network of Fragaria nilgerrensis was revealed by means of a thorough examination of gene expression profiles, whole-genome DNA methylation maps, and physiological parameters at four distinct time points under drought stress treatment [144].…”