A Small RNA Pathway Mediates Allelic Dosage in Endosperm

Abstract

Balance between maternal and paternal genomes within the triploid endosperm is necessary for normal seed development. The majority of endosperm genes are expressed in a 2:1 maternal:paternal ratio, reflecting genomic DNA content. Here, we find that the 2:1 transcriptional ratio is, unexpectedly, actively regulated. In A. thaliana and A. lyrata, endosperm 24-nt small RNAs are reduced in transposable elements and enriched in genes compared with the embryo. We find an inverse relationship between the parent of origin of sRNAs and mRNAs, with genes more likely to be associated with maternally than paternally biased sRNAs. Disruption of the Pol IV sRNA pathway causes a shift toward maternal allele mRNA expression for many genes. Furthermore, paternal inheritance of an RNA Pol IV mutation is sufficient to rescue seed abortion caused by excess paternal genome dosage. Thus, RNA Pol IV mediates the transcriptional balance between maternally and paternally inherited genomes in endosperm. The endosperm is a triploid seed tissue critical for seed viability. Imprinted expression occurs there, but whether active regulation of maternal:paternal transcript ratios occurs on a broader scale is unknown. Erdmann et al. show that the RNA Pol IV small RNA pathway mediates dosage interactions between maternal and paternal genomes. Keywords: endosperm; RNA Pol IV; dosage; imprinting; small RNA; DNA methylation; A. thaliana; A. lyrata