A Small RNA Pathway Mediates Global Allelic Dosage in Endosperm

Balance between maternal and paternal genomes within the triploid endosperm is necessary for normal seed development. The majority of genes in Arabidopsis endosperm are expressed in a 2:1 maternal:paternal ratio, reflecting endosperm genomic DNA content. Here we find that the 2:1 transcriptional ratio is not, unexpectedly, a passive default but is actively regulated. We describe an inverse relationship between the parent-of-origin of small RNAs and mRNAs in endosperm on a genome-wide scale. Disruption of the Pol IV small RNA pathway causes the entire transcriptome to become more maternally biased. Furthermore, paternal inheritance of a RNA Pol IV mutation is sufficient to rescue seed abortion caused by excess paternal genome dosage. These results indicate that maintenance of the maternal:paternal transcriptome ratio in endosperm is an active process and reveal a function for RNA Pol IV in mediating the global transcriptional balance between maternally and paternally inherited genomes in endosperm.