Paramutation-like features of multiple natural epialleles in tomato

Quentin Gouil,David C Baulcombe

doi:10.1186/s12864-018-4590-4

Quentin Gouil, David C Baulcombe

Open Access

https://doi.org/10.1186/s12864-018-4590-4

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Abstract

BackgroundFreakish and rare or the tip of the iceberg? Both phrases have been used to refer to paramutation, an epigenetic drive that contravenes Mendel’s first law of segregation. Although its underlying mechanisms are beginning to unravel, its understanding relies only on a few examples that may involve transgenes or artificially generated epialleles.ResultsBy using DNA methylation of introgression lines as an indication of past paramutation, we reveal that the paramutation-like properties of the H06 locus in hybrids of Solanum lycopersicum and a range of tomato relatives and cultivars depend on the timing of sRNA production and conform to an RNA-directed mechanism. In addition, by scanning the methylomes of tomato introgression lines for shared regions of differential methylation that are absent in the S. lycopersicum parent, we identify thousands of candidate regions for paramutation-like behaviour. The methylation patterns for a subset of these regions segregate with non Mendelian ratios, consistent with secondary paramutation-like interactions to variable extents depending on the locus.ConclusionTogether these results demonstrate that paramutation-like epigenetic interactions are common for natural epialleles in tomato, but vary in timing and penetrance.

Highlights

Freakish and rare or the tip of the iceberg? Both phrases have been used to refer to paramutation, an epigenetic drive that contravenes Mendel’s first law of segregation
Paramutation is an epigenetic process in plants and animals that is associated with gene silencing
We identify other methylated DNA epialleles in the Introgression line (IL) with paramutation-like properties: they are absent from the parental lines, present in multiple ILs independently of a specific introgressed region from S. pennelli and they transfer their epigenetic mark to a non-methylated allele following backcrossing to M82

Summary

Introduction

Freakish and rare or the tip of the iceberg? Both phrases have been used to refer to paramutation, an epigenetic drive that contravenes Mendel’s first law of segregation. Paramutation is an epigenetic process in plants (including pea, maize, tomato [1]) and animals (worm [2], fruit fly [3], mouse [4]) that is associated with gene silencing. It is unlike other epigenetic mechanisms, in that it involves transfer of the silent state from an allele with epigenetic modification to its active homologue. Based on these findings the dominant model of paramutation implicates RdDM in the establishment and/or maintenance of the epigenetic mark

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