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

Hardik Kundariya, Xiaodong Yang, Kyla Morton, Robersy Sanchez, Michael J. Axtell, Samuel F. Hutton, Michael Fromm and Sally A. Mackenzie ()
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Hardik Kundariya: University of Nebraska
Xiaodong Yang: The Pennsylvania State University
Kyla Morton: EpiCrop Technologies, Inc.
Robersy Sanchez: The Pennsylvania State University
Michael J. Axtell: The Pennsylvania State University
Samuel F. Hutton: IFAS, University of Florida
Michael Fromm: EpiCrop Technologies, Inc.
Sally A. Mackenzie: The Pennsylvania State University

Nature Communications, 2020, vol. 11, issue 1, 1-14

Abstract: Abstract 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.

Date: 2020
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DOI: 10.1038/s41467-020-19140-x

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