Systemic silencing and DNA methylation of a host reporter gene induced by a beneficial fungal root endophyte

A growing body of evidence suggests that RNA interference (RNAi) plays a pivotal role in the communication between plants and pathogenic fungi, where a bi-directional cross-kingdom RNAi is established to the advantage of either the host or the pathogen. Similar mechanisms acting during plant association with non-pathogenic symbiotic microorganisms have been elusive to this date. Here, we report on an RNAi-based mechanism of communication between a beneficial fungal endophyte, Fusarium solani strain K (FsK) and its host plants. This soil-borne endophyte that confers resistance and/or tolerance to biotic and abiotic stress in tomato and, as shown in this study, promotes plant growth in Nicotiana benthamiana, is restricted to the root system in both host plants. We first showed that the fungus has a functional core RNAi machinery; double stranded RNAs (dsRNAs) are processed into short interfering RNAs (siRNAs) of predominantly 21-nt in size, which lead to the degradation of homologous mRNAs. Importantly, by using an RNAi sensor system, we demonstrated that root colonization of N. benthamiana by FsK led to the induction of systemic silencing and DNA methylation of a host reporter gene.. These data reflect a more general but so far unrecognized mechanism wherein root endophytes systemically translocate RNAi signals to the aboveground tissues of their hosts to modulate gene expression during symbiosis, which may be translated to the beneficial phenotypes. HighlightA root-restricted, beneficial fungal endophyte can induce systemic silencing and epigenetic modifications to its host plant.