Regulation of imprinted gene expression in Arabidopsis endosperm

Abstract

Imprinted genes are expressed primarily or exclusively from either the maternal or paternal allele, a phenomenon that occurs in flowering plants and mammals. Flowering plant imprinted gene expression has been described primarily in endosperm, a terminal nutritive tissue consumed by the embryo during seed development or after germination. Imprinted expression in Arabidopsis thaliana endosperm is orchestrated by differences in cytosine DNA methylation between the paternal and maternal genomes as well as by Polycomb group proteins. Currently, only 11 imprinted A. thaliana genes are known. Here, we use extensive sequencing of cDNA libraries to identify 9 paternally expressed and 34 maternally expressed imprinted genes in A. thaliana endosperm that are regulated by the DNA-demethylating glycosylase DEMETER, the DNA methyltransferase MET1, and/or the core Polycomb group protein FIE. These genes encode transcription factors, proteins involved in hormone signaling, components of the ubiquitin protein degradation pathway, regulators of histone and DNA methylation, and small RNA pathway proteins. We also identify maternally expressed genes that may be regulated by unknown mechanisms or deposited from maternal tissues. We did not detect any imprinted genes in the embryo. Our results show that imprinted gene expression is an extensive mechanistically complex phenomenon that likely affects multiple aspects of seed development.

Imprinting meets genomics: new insights and new challenges

“…For some genes expression of the maternal allele was also upregulated. This and another study concluded that PRC2 can regulate maternal and paternal alleles of MEGs and maternal alleles of PEGs [5] [6]. In endosperm, paternal alleles of PEGs might be protected from PRC2 repression because of DNA methylation continuously present at those loci [25].…”

“…Deep sequencing of mRNA libraries derived from reciprocal intraspecific crosses of Arabidopsis thaliana, rice, and maize has proven to be an effective strategy to identify genes that are preferentially expressed from one parental allele during seed development [4][5][6][7][8][9]. These studies have confirmed that imprinting is mostly endosperm-specific and have significantly expanded the number of imprinted genes to between about 50-200 in each species.…”

“…Comparisons of candidate imprinted genes identified by independent groups often have limited overlap, as illustrated by two Arabidopsis and two maize studies that utilized the same genetic backgrounds [4,5,7,8]. The Arabidopsis studies identified 208 and 126 candidate imprinted genes, with only 20 genes in common [4].…”

“…Among paternally expressed imprinted genes (PEGs), transcription factors and chromatin-related proteins are enriched [4]. Examples of imprinted genes include 5-methylcytosine binding proteins, histone lysine methyltransferases, a Class IV homeodomain transcription factor, and several members of the MADS-box transcription factor family [4][5][6]. Interestingly, different members of the HDG and MADS families are maternally expressed imprinted genes (MEGs).…”

“…MEDEA and FWA, two MEGs, and PHERES1, a PEG, are the most extensively studied endosperm imprinted genes in terms of mechanism of monoallelic expression. By performing expression analysis on seeds with mutations in known regulators of imprinting, many more imprinted genes regulated like MEA, FWA, or PHE1 were discovered [5,6].…”