Epigenetic regulation modulates seasonal temperature-dependent growth of soybean in southern China

Epigenetic variations, including DNA methylation and small RNAs, are crucial for plant stress adaptation. However, their association with soybean adaptation to natural environments remains unclear. Through multi-omics analyses, we investigate soybeans from distinct geographical regions (Northern China: HH43, Southern China: HX3, and Wm82) and grown under contrasting South Winter (SW) and South Summer (SS) conditions in China. Transcriptomic clustering classifies soybeans into two distinct groups based on SW and SS. Methylome demonstrates increased CHH methylation in SW, accompanied by HDA6 up-regulation, leading to chromatin compaction and transcriptional repression. Substantial Copia retrotransposons and DNA transposons are also repressed in SW. Interestingly, DNA methylation predominantly influences down-regulated/up-regulated COR genes for HH43 and HX3 through increased/decreased DNA methylation, respectively. In contrast, lower CG/CHG methylation in SW coincided with reduced DNA methyltransferases expression. Notably, non-CG methylation contributes more to DSR in adaptive traits under selective pressure. Such as the E2 domesticated gene exhibits lower CHG methylation within the gene body region and down-regulated expression in SW for HH43. Furthermore, 22-nt siRNA are substantially degraded in SW, and GmDCL2a/2b mutation results in increased plant sensitivity to low temperatures. These highlight the dynamic interplay between DNA methylation, small RNAs and gene expression in soybean adaptation to natural environments.