Lesheng Cao, Tianxu Zhang, Shuang Ma, Lishan Wang, Wanpeng Wang, Peng Zhang, Min Wang, Bowei Chen, Zihui Zhang, Yile Guo, Haowen Chen, Luzia Valentina Modolo, Jiang Wang, Linan Xie, Qingzhu Zhang
Although chromatin states are closely associated with epigenetic modifications, how they influence each other remains to be fully elucidated. In this study, we found that mutation of DECREASED IN DNA METHYLATION 1 (DDM1) in soybean leads to genome-wide chromatin homogenization, characterized by a loosening of heterochromatin and a tightening of euchromatin. This remodeling triggers two distinct molecular pathways: in heterochromatin, increased release of small RNAs activates the non-canonical RdDM pathway; while in euchromatin, transposable elements (TEs) are enriched with H3K9me2 modifications, which in turn activate the CMT2 pathway. Together, these pathways drive a pronounced burst of CHH methylation at the whole genome level. This epigenetic remodeling correlates with massive transcriptional dysregulation, upregulating stress responses and downregulating photosynthesis, linking local H3K9me2 changes on TEs, ultimately leading to severe phenotypes. Our findings reveal a unique, bidirectional pathway for CHH regulation in plants with complex chromatin states remodeling.