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Plants transmit signals long distances, as evidenced in grafting experiments that create distinct rootstock-scion junctions. Noncoding small RNA is a signaling molecule that is graft transmissible, participating in RNA-directed DNA methylation; but the meiotic transmissibility of graft-mediated epigenetic changes remains unclear. Here, we exploit the  MSH1  system in  Arabidopsis  and tomato to introduce rootstock epigenetic variation to grafting experiments. Introducing mutations  dcl2 ,  dcl3  and  dcl4  to the  msh1  rootstock disrupts siRNA production and reveals RdDM targets of methylation repatterning. Progeny from grafting experiments show enhanced growth vigor relative to controls. This heritable enhancement-through-grafting phenotype is RdDM-dependent, involving 1380 differentially methylated genes, many within auxin-related gene pathways. Growth vigor is associated with robust root growth of  msh1  graft progeny, a phenotype associated with auxin transport based on inhibitor assays. Large-scale field experiments show  msh1  grafting effects on tomato plant performance, heritable over five generations, demonstrating the agricultural potential of epigenetic variation.

MSH1-induced heritable enhanced growth vigor through grafting is associated with the RdDM pathway in plants