High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis Endosperm.

Pawel Roszak,Philip Wolff,Isabelle Weinhofer,Claudia Köhler,Christian Beisel,Marc Rehmsmeier,Tetsuji Kakutani,Magnus Nordborg,Mark T. A. Donoghue,Charles Spillane,Jonathan Seguin

doi:10.1371/journal.pgen.1002126

Abstract

Genomic imprinting is an epigenetic phenomenon leading to parent-of-origin specific differential expression of maternally and paternally inherited alleles. In plants, genomic imprinting has mainly been observed in the endosperm, an ephemeral triploid tissue derived after fertilization of the diploid central cell with a haploid sperm cell. In an effort to identify novel imprinted genes in Arabidopsis thaliana, we generated deep sequencing RNA profiles of F1 hybrid seeds derived after reciprocal crosses of Arabidopsis Col-0 and Bur-0 accessions. Using polymorphic sites to quantify allele-specific expression levels, we could identify more than 60 genes with potential parent-of-origin specific expression. By analyzing the distribution of DNA methylation and epigenetic marks established by Polycomb group (PcG) proteins using publicly available datasets, we suggest that for maternally expressed genes (MEGs) repression of the paternally inherited alleles largely depends on DNA methylation or PcG-mediated repression, whereas repression of the maternal alleles of paternally expressed genes (PEGs) predominantly depends on PcG proteins. While maternal alleles of MEGs are also targeted by PcG proteins, such targeting does not cause complete repression. Candidate MEGs and PEGs are enriched for cis-proximal transposons, suggesting that transposons might be a driving force for the evolution of imprinted genes in Arabidopsis. In addition, we find that MEGs and PEGs are significantly faster evolving when compared to other genes in the genome. In contrast to the predominant location of mammalian imprinted genes in clusters, cluster formation was only detected for few MEGs and PEGs, suggesting that clustering is not a major requirement for imprinted gene regulation in Arabidopsis.

Highlights

Genomic imprinting is an epigenetic phenomenon present in mammals and flowering plants that leads to differential expression of alleles of the same gene dependent on the parent-of-origin
Genomic imprinting predominantly occurs in the endosperm, which is derived after fertilization of the diploid central cell with a haploid sperm cell
We show that maternally expressed genes are regulated by DNA methylation or Polycomb group (PcG)-mediated repression, while paternally expressed genes are predominantly regulated by PcG proteins

Summary

Introduction

Genomic imprinting is an epigenetic phenomenon present in mammals and flowering plants that leads to differential expression of alleles of the same gene dependent on the parent-of-origin. Imprinted genes are differentially marked in the gametes, making maternal and paternal alleles functionally different [1]. Whereas in mammals imprinting occurs in the placenta as well as the embryo and tissues of the adult organism, most examples of imprinted genes in plants to date are confined to the endosperm [2]. Examples of imprinted genes in the plant embryo exist [3], they seem to be rare. The endosperm is a functional analog of the mammalian placenta and serves to support embryo growth [4]. It is a triploid tissue that is derived after fertilization of the homodiploid central cell with a haploid sperm cell, whereas the second sperm cell will fertilize the haploid egg cell, leading to the formation of the diploid embryo [5]

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