Identification and Characterization of an Epi-Allele of FIE1 Reveals a Regulatory Linkage between Two Epigenetic Marks in Rice

Abstract

DNA methylation and histone H3 Lys 9 dimethylation (H3K9me2) are important epigenetic repression marks for silencing transposons in heterochromatin and for regulating gene expression. However, the mechanistic relationship to other repressive marks, such as histone H3 Lys 27 trimethylation (H3K27me3) is unclear. FERTILIZATION-INDEPENDENT ENDOSPERM1 (FIE1) encodes an Esc-like core component of the Polycomb repressive complex 2, which is involved in H3K27me3-mediated gene repression. Here, we identify a gain-of-function epi-allele (Epi-df) of rice (Oryza sativa) FIE1; this allele causes a dwarf stature and various floral defects that are inherited in a dominant fashion. We found that Epi-df has no changes in nucleotide sequence but is hypomethylated in the 59 region of FIE1 and has reduced H3K9me2 and increased H3K4me3. In Epi-df, FIE1 was ectopically expressed and its imprinting was disrupted. FIE1 interacted with rice Enhancer of Zeste homologs, consistent with its role in H3K27me3 repression. Ectopic expression of FIE1 in Epi-df resulted in alteration of H3K27me3 levels in hundreds of genes. In summary, this work identifies an epi-allele involved in H3K27me3-mediated gene repression that itself is highly regulated by DNA methylation and histone H3K9me2, thereby shedding light on the link between DNA methylation and histone methylation, the two important epigenetic marks regulating rice development.

The Birth of a Black Rice Gene and Its Local Spread by Introgression

“…Epialleles have been reported in several plant species, including maize (Brink, 1956;Banks et al, 1988;Das and Messing, 1994;Hollick and Chandler, 2001) and rice (Miura et al, 2009(Miura et al, , 2010Wang et al, 2010;Zhang et al, 2012;Li et al, 2014). The phenotypes of these epialleles are affected by DNA methylation status and/or histone modification resulting in the alteration of gene expression.…”

Epigenetic Mutation of RAV6 Affects Leaf Angle and Seed Size in Rice

“…Thus, Epi-rav6 has similar features to the Arabidopsis fwa mutant, the first DNA-hypomethylated mutant identified in plants, with hypomethylation at two direct repeats in the 59 region of FWA and ectopic expression of FWA (Soppe et al, 2000). In rice, only two epialleles, Epi-d1 and Epi-df, were identified previously, with hyper-and hypomethylation at the causal genes, respectively (Miura et al, 2009;Zhang et al, 2012). Although both Epi-df and Epi-rav6 are hypomethylated, the methylation sites of the two epialleles differ.…”

“…In tomato (Solanum lycopersicum), the Colorless nonripening phenotype results from hypermethylation at the promoter of SQUAMOSA promoter-binding protein like (Manning et al, 2006). In melon (Cucumis melo), the transition from male to female flowers results from DNA hypermethylation in the promoter of CmWIP1, as mediated by a transposon insertion in gynoecious varieties (Martin et al, 2009).Work in rice (Oryza sativa) has found only two epialleles, Epi-d1 and Epi-df, both of which show a dwarf phenotype (Miura et al, 2009;Zhang et al, 2012). Epi-d1 is a spontaneous epiallele that shows a metastable dwarf phenotype caused by DNA hypermethylation in the promoter region of DWARF1 (Miura et al, 2009).…”

“…Work in rice (Oryza sativa) has found only two epialleles, Epi-d1 and Epi-df, both of which show a dwarf phenotype (Miura et al, 2009;Zhang et al, 2012). Epi-d1 is a spontaneous epiallele that shows a metastable dwarf phenotype caused by DNA hypermethylation in the promoter region of DWARF1 (Miura et al, 2009).…”

“…Epi-df is a gain-of-function epiallele caused by hypomethylation in the 59 region of FERTILIZATION-INDEPENDENT ENDOSPERM1 (FIE1). The ectopic expression of FIE1 in Epi-df results in dwarf and various floral defects that are inherited in a dominant manner (Zhang et al, 2012).…”