Innate, translation-dependent silencing of an invasive transposon in Arabidopsis

Co-evolution between hosts and parasites genomes shapes diverse pathways of acquired immunity based on silencing small (s)RNAs. In plants, sRNAs cause heterochromatinization, sequence-degeneration and, ultimately, loss-of-autonomy of most transposable elements (TEs). Recognition of newly-invasive plant TEs, by contrast, involves an innate antiviral-like silencing response. To investigate this responses activation, we studied the single-copy element EVADE (EVD), one of few representatives of the large Ty1/Copia family able to proliferate in Arabidopsis when epigenetically-reactivated. In Ty1/Copia-elements, a short subgenomic mRNA (shGAG) provides the necessary excess of structural GAG protein over the catalytic components encoded by the full-length genomic flGAG-POL. We show here that the predominant cytosolic distribution of shGAG strongly favors its translation over mostly-nuclear flGAG-POL, during which an unusually intense ribosomal stalling event coincides precisely with the starting-point of sRNA production exclusively on shGAG. mRNA breakage occurring at this starting-point yields unconventional 5OH RNA fragments that evade RNA-quality-control and concomitantly likely stimulate RNA-DEPENDENT-RNA-POLYMERASE-6 (RDR6) to initiate sRNA production. This hitherto-unrecognized "translation-dependent silencing" (TdS) is independent of codon-usage or GC-content and is not observed on TE remnants populating the Arabidopsis genome, consistent with their poor association, if any, with polysomes. We propose that TdS forms a primal defense against de novo invasive TEs that underlies their associated sRNA patterns.