Muts Homolog 1-Induced Heritable Stress Memory and Enhanced Growth Vigor Through Grafting Are Associated with the RdDM Pathway

Rapid response to stress in plants is thought to involve epigenomic effects, but the extent to which these changes are inherited is not well characterized. RNAi suppression of MSH1, a plant-specific gene, produces a range of developmental changes. Following segregation of the RNAi transgene, transgene-null progenies with restored MSH1 display a non-genetic phenotype termed msh1 “memory”. Methylation and gene expression analyses of a six-generation inheritance study of memory identified key pathways including circadian rhythm, phytohormone signaling, and stress response. The msh1 memory induction is dependent on HDA6, MET1, and DRM1/2, genes known to participate in targeted DNA methylation. Grafting of wild-type floral stems to the msh1 rootstock produces progeny with heritable enhanced growth vigor in Arabidopsis and tomato, suggesting the involvement of a mobile signal. Disruption of small interfering RNA (siRNA) production in the msh1 rootstock by introducing RdDM mutations obviates the enhanced vigor in graft progeny. Comparison between enhanced and non-enhanced progenies identified differentially methylated loci enriched for auxin-related pathways, and an association to robust root growth in msh1 progeny was confirmed through chemical inhibitor assays. Field studies of msh1 graft progenies in tomato showed significant increase in yield. Together, these results suggest that msh1-induced epigenetic variation could provide environmental resilience and enhanced yield in plants