Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen.

Plant pathogenic fungi represent the largest group of disease-causing agents on crop plants, and are a constant and major threat to agriculture worldwide. Recent studies have shown that engineered production of RNA interference (RNAi)-inducing dsRNA in host plants can trigger specific fungal gene silencing and confer resistance to fungal pathogens1-7. Although these findings illustrate efficient uptake of host RNAi triggers by pathogenic fungi, it is unknown whether or not such an uptake mechanism has been evolved for a natural biological function in fungus-host interactions. Here, we show that in response to infection with Verticillium dahliae (a vascular fungal pathogen responsible for devastating wilt diseases in many crops) cotton plants increase production of microRNA 166 (miR166) and miR159 and export both to the fungal hyphae for specific silencing. We found that two V. dahliae genes encoding a Ca2+-dependent cysteine protease (Clp-1) and an isotrichodermin C-15 hydroxylase (HiC-15), and targeted by miR166 and miR159, respectively, are both essential for fungal virulence. Notably, V. dahliae strains expressing either Clp-1 or HiC-15 rendered resistant to the respective miRNA exhibited drastically enhanced virulence in cotton plants. Together, our findings identify a novel defence strategy of host plants by exporting specific miRNAs to induce cross-kingdom gene silencing in pathogenic fungi and confer disease resistance.

The dual edge of RNA silencing suppressors in the virus-host interactions.

RNA silencing (or RNA interference, RNAi) plays a key role in the plant antiviral defense. To facilitate infection, viruses encode suppressors of RNA silencing (VSRs) to counteract antiviral defense. In the co-evolutionary arms race between hosts and viruses, extreme viral accumulation does not benefit either hosts or viruses. During viral infection, antiviral silencing and VSRs have dual effects to maintain the balance between plant development and virus accumulation. Here, we summarize and discuss the multiple functions of the antiviral RNAi defense and VSRs, revealing the central hub regulators of VSRs in dynamically integrated connections between hosts and viruses.