LEC2 induces somatic cell reprogramming through epigenetic activation of plant cell totipotency regulators

Many plant species can develop embryos from somatic cells without fertilization. During this process, known as somatic embryogenesis, changes in the DNA methylation patterns are characteristic of reprogramming somatic cells into an embryogenic state. However, the underlying mechanisms connecting DNA methylation and activating totipotency-regulating genes have remained largely unknown. Here, we show that during somatic embryogenesis induced by overexpressing the totipotency-regulating transcription factor LEAFY COTYLEDON2 (LEC2) in Arabidopsis, CHH hypermethylation is deposited by the LEC2-activated RNA-directed DNA methylation (RdDM) pathway. A reader complex composed of SU(VAR)3-9 HOMOLOGS (SUVH) and its chaperone SUVH-INTERACTING DNAJ DOMAIN-CONTAINING PROTEIN (SDJ) binds to the CHH hypermethylated regions and recruits AT-HOOK MOTIF CONTAINING NUCLEAR LOCALIZED (AHL) chromatin modification proteins to increase chromatin accessibility, resulting in the transcriptional activation of totipotency-regulating genes. Our work reveals a molecular framework of how epigenetic modifications mediate somatic cell reprogramming, offering a pathway toward enhancing somatic embryogenesis in agricultural regeneration biology.