Arabidopsis MSH1 Mutation Alters the Epigenome and Produces Heritable Changes in Plant Growth

Plant phenotypes respond to environmental change, an adaptive capacity that is, at least in part, trans-generational. Genotype x environment interaction in plant populations involves both genetic and epigenetic factors to define a plant’s phenotypic range of response. The epigenetic aspect of this interplay is generally difficult to measure. Previously we showed that depletion of a nuclear-encoded protein, MSH1, from the plastid causes dramatic and heritable changes in development. Here we show that crossing these altered plants with isogenic wild type restores normal growth and can produce epi-lines with enhanced growth vigor that is heritable. The msh1 mutants and progeny from crossing demonstrate changes in DNA methylation. Large chromosomal segments of differential methylation in epi-lines indicating genome-wide reprogramming. When wild type floral stems are grafted to mutant rosettes, the resulting progeny show enhanced growth similar to epi-lines, suggesting a mobile nature of signals emanating from vegetative tissues when msh1 is downregulated. We demonstrate that these heritable, graft-mediated outcomes also produce genome-wide methylation changes strikingly similar in pattern to those effected by crossing to the msh1 mutant. We propose that MSH1 depletion from the plastid constitutes a novel means of inducing epigenetic changes in plants