A variably imprinted epiallele impacts seed development.

Daniela Pignatta,P R V Satyaki,Mary Gehring,Katherine Novitzky,Claudia Köhler

doi:10.1371/journal.pgen.1007469

Daniela Pignatta, P R V Satyaki + Show 3 more

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https://doi.org/10.1371/journal.pgen.1007469

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Abstract

The contribution of epigenetic variation to phenotypic variation is unclear. Imprinted genes, because of their strong association with epigenetic modifications, represent an opportunity for the discovery of such phenomena. In mammals and flowering plants, a subset of genes are expressed from only one parental allele in a process called gene imprinting. Imprinting is associated with differential DNA methylation and chromatin modifications between parental alleles. In flowering plants imprinting occurs in a seed tissue - endosperm. Proper endosperm development is essential for the production of viable seeds. We previously showed that in Arabidopsis thaliana intraspecific imprinting variation is correlated with naturally occurring DNA methylation polymorphisms. Here, we investigated the mechanisms and function of allele-specific imprinting of the class IV homeodomain leucine zipper (HD-ZIP) transcription factor HDG3. In imprinted strains, HDG3 is expressed primarily from the methylated paternally inherited allele. We manipulated the methylation state of endogenous HDG3 in a non-imprinted strain and demonstrated that methylation of a proximal transposable element is sufficient to promote HDG3 expression and imprinting. Gain of HDG3 imprinting was associated with earlier endosperm cellularization and changes in seed weight. These results indicate that epigenetic variation alone is sufficient to explain imprinting variation and demonstrate that epialleles can underlie variation in seed development phenotypes.

Highlights

DNA methylation is a heritable epigenetic mark that can, on occasion, effect gene transcription and influence development
It is challenging to disentangle genetic variation from epigenetic variation, as what appears to be epigenetic variation might have an underlying genetic basis
HOMEDOMAIN GLABROUS3 (HDG3) encodes an endosperm specific transcription factor that exists in two states in A. thaliana natural populations: methylated and expressed and hypomethylated and repressed

Summary

Introduction

DNA methylation is a heritable epigenetic mark that can, on occasion, effect gene transcription and influence development. DNA methylation is a influential regulator of gene expression in endosperm, a triploid extraembryonic seed tissue that supports embryo development. Methylation differences between maternal and paternal alleles identify their parent-of-origin and establish imprinting, an epigenetic phenomenon in which a gene is expressed primarily from one parental allele [4]. Imprinting is theorized to have evolved over conflict between maternally and paternally inherited alleles in offspring over the extent of maternal investment [5,6]. Over evolutionary time silencing of the maternally inherited allele and expression of the paternally inherited allele is predicted to result for genes where the paternally inherited allele’s optimum expression level in offspring is higher than the maternally inherited allele’s [7]. Comparison of imprinting between species in the Arabidopsis genus has provided empirical support for this hypothesis [8,9]

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