Abstract

Plant phenotypes respond to environmental change, an adaptive capacity that is at least partly transgenerational. However, epigenetic components of this interplay are difficult to measure. Depletion of the nuclear-encoded protein MSH1 causes dramatic and heritable changes in plant development, and here we show that crossing these altered plants with isogenic wild type produces epi-lines with heritable, enhanced growth vigour. Pericentromeric DNA hypermethylation occurs in a subset of msh1 mutants, indicative of heightened transposon repression, while enhanced growth epi-lines show large chromosomal segments of differential CG methylation, reflecting genome-wide reprogramming. When seedlings are treated with 5-azacytidine, root growth of epi-lines is restored to wild-type levels, implicating hypermethylation in enhanced growth. Grafts of wild-type floral stems to mutant rosettes produce progeny with enhanced growth and altered CG methylation strikingly similar to epi-lines, indicating a mobile signal when MSH1 is downregulated, and confirming the programmed nature of methylome and phenotype changes.

Highlights

  • Plant phenotypes respond to environmental change, an adaptive capacity that is at least partly transgenerational

  • We demonstrate a link between plastid perturbation and nuclear epigenetic reprogramming through suppression of the nuclearencoded MutS HOMOLOGUE 1 (MSH1) gene

  • This study evaluates the evidence for heritable, epigenetic changes in association with MSH1 depletion in Arabidopsis and following genetic crossing of the msh[1] mutant to wild type

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Summary

Introduction

Plant phenotypes respond to environmental change, an adaptive capacity that is at least partly transgenerational. To investigate the possibility that similar phenotypes arise through epigenetic means and are heritable after restoration of MSH1 in Arabidopsis, we carried out crossing experiments between msh[1] mutants and wild-type plants (Fig. 1). Crossing of wild-type Columbia-0 (Col-0) with a first-generation msh[1] mutant of chm[1], which contains a point mutation[10], resulted in increased phenotypic variation in the F2 progeny.

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