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

Abstract

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.

High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements

“…Consistent with our findings, a recent study found that spontaneous retrotransposon mutations are much more frequent through the male than the female in certain maize lines [31]. This conservation suggests that the roles of TE and TE-induced small RNAs during reproductive development may also be conserved between monocots and eudicots [35,56,57].…”

Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage

“…We failed to obtain a significant increase in viable paternal excess seeds using 4n rdr6-15 pollen ( Figure 1A; Supplemental Figure 1B), suggesting that any sRNAs exclusively dependent on RDR6 are not linked to paternal excess seed abortion. Consistent with this result, paternally produced siR-NA854, which is dependent on DCL2/4 and RDR6, is required for the viability of paternal excess seeds (McCue et al, 2012;Wang et al, 2018). By contrast, we found that multiple members of the canonical RdDM pathway restore paternal excess seed viability (Figure 1; Supplemental Figures 1A and 1C).…”

“…The ability of maternal sporophytic mutations in the flavonoid pathway to repress paternal excess seed abortion is consistent with this model (Dilkes et al, 2008;Doughty et al, 2014). The expression levels of AGAMOUS-LIKE genes (AGLs), the small RNA (sRNA) siRNA854, chromatin regulators, cell wall genes, and defense response genes, all presumed to act in the endosperm, have been linked to paternal excess seed abortion (Walia et al, 2009;Burkart-Waco et al, 2013;Kradolfer et al, 2013;Wolff et al, 2015;Jiang et al, 2017;Wang et al, 2018).…”

“…It is important to note that the increase in the maternal fraction could be observed in both lethal and viable paternal excess endosperm and is thus unlinked to the repression of seed abortion brought about by paternal loss of RdDM. Other buffering mechanisms might also play important roles and could act through posttranscriptional pathways (Wang et al, 2018), protein degradation pathways, or via signaling pathways that have been shown to influence paternal excess crosses (Doughty et al, 2014;Batista et al, 2019). One striking observation is that even wild-type paternal excess crosses produce ;20% viable seeds (Figure 1; Supplemental Figure 1), suggesting that seed lethality and viability exist on a continuum.…”

A Resource for Inactivation of MicroRNAs Using Short Tandem Target Mimic Technology in Model and Crop Plants

“…This allows STTMs to be used to knock down unrelated miRNAs, belonging to different families. Beyond miRNAs, STTMs have also been successfully used to silence the expression of siRNAs (McCue et al, 2013;Wang et al, 2018).…”