Epigenetic Rewiring Shapes Divergent Genome Plasticity in Virus Response Circuitry in Soybean

Epigenetic modifications play pivotal roles in regulating plant adaptive responses to viral infection and various other stresses. However, how viral infection rewires and shapes chromatin-based epigenetic regulatory networks in crops with contrasting resistance remains unclear. To this end, we investigated the consequences of epigenetic variations in resistant and susceptible soybean cultivars following soybean mosaic virus (SMV) infection. SMV infection mediates the depletion of 24-nucleotide small interfering RNAs (24-nt siRNAs) in susceptible cultivars and induces the accumulation of 24-nt siRNAs in resistant cultivars. Twenty-four-nucleotide siRNA-dependent DNA methylation variable regions are preferentially enriched in euchromatic CHH contexts, and highly variable DNA methylation regions in heterochromatic long terminal repeat (LTR) retrotransposons are independent of 24-nt siRNAs. Moreover, SMV infection triggers extensive chromatin remodelling in susceptible cultivar, where the depletion of 24-nt siRNAs is related to reduced chromatin accessibility. Conversely, SMV infection mildly remodels chromatin accessibility at heterochromatic LTR retrotransposons in the resistant cultivar. Variations in 24-nt siRNA levels and DNA methylation in upstream regions of autophagy-related genes in susceptible cultivars may influence their expression. Our work provides insights into SMV-triggered divergent epigenetic regulatory networks in soybeans with contrasting resistance and provides a valuable foundation for investigating gene regulatory programmes based on epigenetic variations.