Paternal easiRNAs regulate parental genome dosage in Arabidopsis

Abstract

The regulation of parental genome dosage is of fundamental importance in animals and plants, as exemplified by X-chromosome inactivation and dosage compensation. The 'triploid block' is a classic example of dosage regulation in plants that establishes a reproductive barrier between species differing in chromosome number. This barrier acts in the embryo-nourishing endosperm tissue and induces the abortion of hybrid seeds through a yet unknown mechanism . Here we show that depletion of paternal epigenetically activated small interfering RNAs (easiRNAs) bypasses the triploid block in response to increased paternal ploidy in Arabidopsis thaliana. Paternal loss of the plant-specific RNA polymerase IV suppressed easiRNA formation and rescued triploid seeds by restoring small-RNA-directed DNA methylation at transposable elements (TEs), correlating with reduced expression of paternally expressed imprinted genes (PEGs). Our data suggest that easiRNAs form a quantitative signal for paternal chromosome number and that their balanced dosage is required for post-fertilization genome stability and seed viability.

Maternal components of RNA‐directed DNA methylation are required for seed development in Brassica rapa

“…Loss of RdDM could negatively affect seed development in several possible ways. Massive deregulation of transposons would explain the asynchronous and nearly complete seed abortion we observed, and is consistent with reports of transposon deregulation linked to seed abortion during the triploid block (Erdmann et al ., ; Borges et al ., ; Martínez et al ., ). It is also possible that mobile maternal p4‐siRNAs are required for correct expression of specific transposon‐associated genes, such as AGAMOUS‐like transcription factors, which are upregulated in Arabidopsis seeds lacking maternal NRPD1 (Lu et al ., ).…”

“…Neither paternal easiRNAs nor maternal p4‐siRNAs are required for normal seed development in Arabidopsis (Mosher et al ., ; Martínez et al ., ), although paternal 21 nt siRNAs have been implicated in failure of triploid endosperm during unbalanced crosses (Borges et al ., ; Martínez et al ., ). However, Arabidopsis is an inbreeding species with few active transposons and therefore might be a poor system to study the function of small RNAs during reproduction.…”

Intercellular delivery of small RNAs in plant gametes

“…Consistent with the involvement of the DCL1–AGO1–RDR6–DCL4 pathway for easiRNA biogenesis, fewer easiRNAs were produced in dcl1 , ago1 , rdr6 and dcl4 mutants (Creasey et al ., ). However, recent studies showed that Pol IV is necessary to produce easiRNAs (Borges et al ., ; Martinez et al ., ), indicating alternative pathways might exist for easiRNA biogenesis.…”

“…The mechanism by which the dosage imbalance of hybridization barriers is maintained has long been puzzling. However, two recent studies (Borges et al ., ; Martinez et al ., ) showed that paternal easiRNAs are required for post‐fertilization genome stability and seed viability by monitoring chromosome dosage and imprinting in the developing seed. miR845, one of the most abundant and highly conserved miRNAs in pollen (Borges et al ., ), targets Gypsy and Copia retrotransposons reactivated in the vegetative cell to generate easiRNAs.…”

“…Furthermore, Martinez et al . () showed that loss of paternal easiRNAs bypasses the triploid block by restoring easiRNA‐directed DNA methylation at TE regions, which correlated with reduced expression of paternally expressed imprinted genes. Together, these studies uncovered new insights into easiRNAs in the regulation of chromosome dosage, providing a potential means of monitoring easiRNA levels to bypass hybridization barriers in molecular breeding.…”