Mobile small RNAs as mediators of stress-induced epigenomic remodeling and systemic stress adaptation

Plants rely on sophisticated long-distance communication networks to coordinate adaptive responses to changing environmental conditions. Among these, mobile small RNAs (sRNAs), including microRNAs (miRNAs) and small interfering RNAs (siRNAs), function as critical systemic signaling molecules that move between tissues through plasmodesmata and the phloem. While their roles in post-transcriptional gene regulation are well established, emerging evidence indicates that mobile sRNAs also mediate stress-induced epigenomic remodeling in recipient tissues. Specifically, 24-nt siRNAs can direct RNA-dependent DNA methylation (RdDM) and chromatin modifications at distal genomic loci, thereby altering transcriptional states, stabilizing stress-responsive gene networks, and modulating transposon activity. Such epigenetic reprogramming can extend beyond transient stress responses, contributing to stress memory and, in some cases, to transgenerational inheritance of adaptive traits. This review synthesizes current knowledge on the biogenesis, transport, and functional integration of mobile sRNAs, with special emphasis on their capacity to reshape DNA methylation landscapes and chromatin architecture during environmental stress. We further discuss experimental evidence from grafting studies, methylome profiling, and mutant analyses that support systemic epigenetic regulation mediated by sRNAs. Finally, we explore the practical applications of leveraging mobile sRNA-driven epigenomic remodeling for sustainable crop improvement, including epi-grafting and targeted epigenome engineering strategies. By positioning mobile sRNAs as mediators of systemic epigenetic plasticity, this review emphasizes their central role in coordinating plant stress adaptation in a changing climate.