Sequestration of a Transposon-Derived siRNA by a Target Mimic Imprinted Gene Induces Postzygotic Reproductive Isolation in Arabidopsis

Genomic imprinting is an epigenetic phenomenon occurring in mammals and flowering plants, causing genes to be expressed depending on their parent of origin. In plants, genomic imprinting is mainly confined to the endosperm, a nutritive tissue supporting embryo growth, similar to the placenta in mammals. Here, we show that the paternally expressed imprinted gene PEG2 transcript sequesters the transposable element (TE)-derived small interfering RNA (siRNA) siRNA854 in the endosperm. siRNA854 is present in the vegetative cell of pollen and transferred to the central cell of the female gametophyte after fertilization, where it is captured by PEG2. Depletion of siRNA854 as a consequence of increased PEG2 transcript levels establishes a reproductive barrier and prevents successful hybridizations between plants differing in chromosome number (ploidy). Thus, the balance of a male gamete accumulating TE-derived siRNA and a paternally expressed imprinted gene regulate triploid seed viability, revealing a transgenerational speciation mechanism. •The imprinted gene PEG2 acts as a sponge for the transposon-derived siRNA854•Depletion of siRNA854 in the endosperm causes triploid seed abortion•siRNA854 is generated in pollen and acts transgenerationally in the endosperm•Regulation of UBP1b by siRNA854 is causally connected to triploid seed viability Hybridizations of plants that differ in chromosome number (ploidy) frequently lead to seed abortion. Wang et al. show that the imprinted gene PEG2 acts as a sponge for the transposon-derived siRNA854 in the endosperm. Increased dosage of PEG2 depletes siRNA854, causing triploid seed abortion.