DNA methylation in plant heterosis: mechanisms and prospects

Heterosis is defined as the occurrence in which F1 hybrids exhibit superior traits compared to their parental, and it plays a crucial role in the process of selecting and breeding superior plant varieties. DNA methylation, as a crucial epigenetic modification, significantly contributes to the formation of heterosis. However, the underlying mechanisms are not entirely clear. Here, this review systematically elaborates the regulatory mechanisms of DNA methylation and its epigenetic basis in heterosis. Specifically, it emphasizes deciphering its synergistic role in establishing hybrid vigor through interactions with other epigenetic factors. DNA methylation is dynamically regulated by three processes: establishment, maintenance, and removal of methylation. Parental methylation patterns, as well as the level and sites of DNA methylation, can influence the formation of heterosis. Furthermore, DNA methylation primarily contributes to heterosis by regulating transposable elements (TEs) and the expression of key genes. Additionally, DNA methylation, in conjunction with small RNAs (sRNAs) and histone modifications, collectively regulates heterosis through the RNA-directed DNA methylation (RdDM) pathway and chromatin remodeling. This review lays a foundation for the in-depth study of DNA methylation in hybrid plants, which may serve as a pivotal tool to dissect the molecular mechanisms underlying heterosis. Simultaneously, this will facilitate the application of heterosis in plant breeding, and unlock its untapped potential for hybrid trait optimization in yield, stress resilience, and ecological adaptation.