Imprinting in rice: the role of DNA and histone methylation in modulating parent‐of‐origin specific expression and determining transcript start sites

Abstract

These authors contributed equally. SUMMARYOver 200 imprinted genes in rice endosperm are known, but the mechanisms modulating their parental allele-specific expression are poorly understood. Here we use three imprinted genes, OsYUCCA11, yellow2-like and ubiquitin hydrolase, to show that differential DNA methylation and tri-methylation of histone H3 lysine 27 (H3K27me 3 ) in the promoter and/or gene body influences allele-specific expression or the site of transcript initiation. Paternal expression of OsYUCCA11 required DNA methylation in the gene body whereas the gene body of the silenced maternal allele was hypomethylated and marked with H3K27me 3 . These differential markings mirror those proposed to modulate paternal expression of two Arabidopsis genes, PHERES1 and a YUCCA homolog, indicating conservation of imprinting mechanisms. At yellow2-like, DNA hypomethylation in the upstream flanking region resulted in maternal transcripts that were longer than paternal transcripts; the maternal transcript initiation site was marked by DNA methylation in the paternal allele, and transcription initiated~700 bp downstream. The paternal allele of an ubiquitin hydrolase gene exhibited gene body DNA methylation and produced full-length transcripts, while the maternal allele was hypomethylated in the 5 0 gene body and transcripts initiated from a downstream promoter. Inhibition of DNA methylation by 5-azacytidine or zebularine activated the long transcripts from yellow2-like and enhanced expression of the short transcripts from the ubiquitin hydrolase in seedlings, indicating that DNA methylation prevents transcript initiation from cryptic promoters. These observations suggest a paradigm whereby maternal genome hypomethylation is associated with the production of distinct transcripts, potentially diversifying the gene products from the two alleles.

Both maternally and paternally imprinted genes regulate seed development in rice

“…In Arabidopsis, PEGs in the endosperm are regulated by the maternally expressed MEA that encodes a subunit of PRC2, which serves as a maternal buffer of paternal effects (Pires et al, 2016). In addition, Os12g08780 (OsYUCCA11) is a PEG and is expressed specifically in the endosperm (Luo et al, 2011;Abu-Zaitoon et al, 2012;Du et al, 2014); OsYUCCA11 is a seed-specific auxin biosynthetic gene important to starch deposition in rice (Abu-Zaitoon et al, 2012). YUCCA homologs of maize and Arabidopsis play an important role in endosperm development (Won et al, 2011;Bernardi et al, 2012).…”

Endosperm‐based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers

“…On the molecular level, genomic imprinting is regulated by epigenetic modifications, namely DNA methylation and histone modifications (Gehring et al 2009;Hsieh et al 2011;Waters et al 2011;Wolff et al 2011;Rodrigues et al 2013;Du et al 2014;Zhang et al 2014). Repressive histone modifications that impact on imprinted gene expression are established by Polycomb group proteins assembling into the Polycomb Repressive Complex 2 (PRC2) (Mozgova et al 2015).…”

Endosperm and Imprinting, Inextricably Linked

“…However, this relatively simple regulatory scenario describes a minority of imprinted genes. DNA hypomethylation also appears to influence transcriptional start site choice, leading to the production of different transcripts from maternal and paternal alleles (Luo et al, 2011;Du et al, 2014). The association between DMRs and imprinted genes in maize, rice, and Arabidopsis is much stronger for PEGs than for MEGs.…”