AGO5 restricts virus vertical transmission in plant gametophytes

The propagation of a viral infection from a host parent to its progeny is known as vertical transmission, or seed transmission in plants. It allows viral infections to rapidly spread locally via pollen and worldwide through seeds. To be vertically transmitted to each progeny, a virus must pass through the tight bottleneck of at least one cell per parent - the gametes. Therefore, stopping infection during sexual reproduction is of vital importance to generate healthy offspring. Accordingly, vertical transmission of plant viruses often occurs at very low rates, if at all, suggesting the existence of highly effective - yet unknown - antiviral defenses in pre-meiotic cells, gametes and/or embryos. In this study, we show that AGO5, an RNA interference factor expressed specifically in shoot apical meristem stem cells and the germline of Arabidopsis thaliana, drastically reduces the vertical transmission of Turnip yellow mosaic virus (TYMV). Through a series of controlled pollination experiments leveraging different zygosity of ago5 knock-out, cell type-specific rescue of ago5 and TYMV detection in whole-mount reproductive tissues, we provide evidence that AGO5 acts in pollen and sperm cells to restrict virus transmission to progeny. We further show that triggering antiviral RNA interference specifically in sperm cells leads to a significant reduction in TYMV vertical transmission. In summary, this study provides the first description of a gamete-specific antiviral defense mechanism restricting virus vertical transmission, paving the way for new strategies to prevent the spread of pollen- and seed-borne viral epidemics.