Widespread imprinting of transposable elements and variable genes in the maize endosperm

Sarah N Anderson,Yaniv Brandvain,Peng Zhou,Nathan M Springer,Kaitlin Higgins,Gregory P Copenhaver

doi:10.1371/journal.pgen.1009491

Abstract

Fertilization and seed development is a critical time in the plant life cycle, and coordinated development of the embryo and endosperm are required to produce a viable seed. In the endosperm, some genes show imprinted expression where transcripts are derived primarily from one parental genome. Imprinted gene expression has been observed across many flowering plant species, though only a small proportion of genes are imprinted. Understanding how imprinted expression arises has been complicated by the reliance on single nucleotide polymorphisms between alleles to enable testing for imprinting. Here, we develop a method to use whole genome assemblies of multiple genotypes to assess for imprinting of both shared and variable portions of the genome using data from reciprocal crosses. This reveals widespread maternal expression of genes and transposable elements with presence-absence variation within maize and across species. Most maternally expressed features are expressed primarily in the endosperm, suggesting that maternal de-repression in the central cell facilitates expression. Furthermore, maternally expressed TEs are enriched for maternal expression of the nearest gene, and read alignments over maternal TE-gene pairs indicate that these are fused rather than independent transcripts.

Highlights

Imprinted genes showing parent-of-origin based patterns of expression were first identified in maize [1] and have since been identified in a variety of flowering plants [2,3,4,5,6]
We present a new method which identifies imprinted genes and transposable elements using all parental differences in sequence, including presenceabsence variation between parents, rather than single nucleotide polymorphisms alone
We find that the majority of imprinted genes with maternal expression are genes and transposable elements that are present in only one genome and that are not shared with other grass species

Summary

Introduction

Imprinted genes showing parent-of-origin based patterns of expression were first identified in maize [1] and have since been identified in a variety of flowering plants [2,3,4,5,6]. The central cell is epigenetically distinct from most vegetative cells in the plant due to DNA demethylation targeted primarily to Transposable Elements (TEs) [7,8,9]. This demethylation acts as a primary imprint that distinguishes the female and the male alleles in the endosperm. Many genes and TEs exhibit PAV among genotypes [18,19,20] This limits the ability to use SNP-based allele-specific expression analyses to study imprinting, especially for transposons and variable genes. We develop an alternative approach that relies upon comparisons of expression in reciprocal crosses to assess the imprinting of both conserved and variable genes and TEs across maize genotypes with whole genome assemblies, revealing imprinting for many transposable elements and variable genic sequences

Methods

Results

Conclusion