Imprinting of the Polycomb Group Gene MEDEA Serves as a Ploidy Sensor in Arabidopsis

Abstract

Balanced maternal and paternal genome contributions are a requirement for successful seed development. Unbalanced contributions often cause seed abortion, a phenomenon that has been termed “triploid block.” Misregulation of imprinted regulatory genes has been proposed to be the underlying cause for abnormalities in growth and structure of the endosperm in seeds with deviating parental contributions. We identified a mutant forming unreduced pollen that enabled us to investigate direct effects of unbalanced parental genome contributions on seed development and to reveal the underlying molecular mechanism of dosage sensitivity. We provide evidence that parent-of-origin–specific expression of the Polycomb group (PcG) gene MEDEA is causally responsible for seed developmental aberrations in Arabidopsis seeds with increased paternal genome contributions. We propose that imprinted expression of PcG genes is an evolutionary conserved mechanism to balance parental genome contributions in embryo nourishing tissues.

Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier inArabidopsis

“…Increased paternal genome dosage has been shown to cause preferential deregulation of target genes of FIS-PRC2 (Erilova et al, 2009;Tiwari et al, 2010). Consistent with these data, we found strong enrichment of H3K27m3 on genes showing increased expression levels in triploid seeds compared with diploid seeds ( Figure 7A).…”

“…Triploid paternal excess seeds have phenotypic defects and gene expression profiles similar to seeds lacking FIS-PRC2 function (Erilova et al, 2009;Tiwari et al, 2010), suggesting that FIS-PRC2 function is affected in triploid seeds. However, our data reveal that met1-mediated triploid seed rescue is not caused by restoring FIS-PRC2 function, but acts via a different mechanism.…”

“…We addressed the question whether increased paternal genome dosage causes altered DNA methylation patterns in sperm that in turn cause global changes of gene expression after fertilization. The meiotic mutant jason (jas) forms diploid pollen containing 2n sperm cells at ;60% frequency (Erilova et al, 2009;De Storme and Geelen, 2011), allowing the simultaneous isolation of 1n and 2n sperm cells. We isolated 1n and 2n sperm nuclei of jas-3 pollen by fluorescence-activated cell sorting and analyzed genome-wide DNA methylation profiles of 1n and 2n sperm genomes by shotgun bisulfite sequencing.…”

“…Target gene repression by PRC2 is mediated by trimethylation of lysine 27 of histone H3 (H3K27m3) (Simon and Kingston, 2013). Mutants in FIS-PRC2 subunits phenotypically mimic triploid seeds, suggesting that deregulation of FIS-PRC2 target genes are causally responsible for triploid seed failure (Erilova et al, 2009;Tiwari et al, 2010). Supporting this view, mutations in the paternally expressed imprinted FIS-PRC2 target gene ADMETOS (ADM) can suppress triploid seed abortion (Kradolfer et al, 2013b).…”

Mechanisms and evolution of genomic imprinting in plants

“…Developmental defects are associated with increased expression of PHE1 and many other genes in the endosperm (Kang et al, 2008;Kö hler et al, 2003b;Erilova et al, 2009), suggesting that the main function of the FIS PcG complex is to suppress dosage sensitive genes in the endosperm. Support for this idea stems from experiments showing that fis mutants can form viable seeds if a sexually derived fis embryo is supported by an autonomously developing diploid endosperm (Nowack et al, 2007).…”