A perspective on cross-kingdom RNA interference in mutualistic symbioses

Abstract

RNA interference (RNAi) is arguably one of the more versatile mechanisms in cell biology, facilitating the fine regulation of gene expression and protection against mobile genomic elements, whilst also constituting a key aspect of induced plant immunity. More recently, the use of this mechanism to regulate gene expression in heterospecific partners - cross-kingdom RNAi (ckRNAi) - has been shown to form a critical part of bidirectional interactions between hosts and endosymbionts, regulating the interplay between microbial infection mechanisms and host immunity. Here, we review the current understanding of ckRNAi as it relates to interactions between plants and their pathogenic and mutualistic endosymbionts, with particular emphasis on evidence in support of ckRNAi in the arbuscular mycorrhizal symbiosis.

Keywords: RNA interference; arbuscular mycorrhizal symbiosis; cross-kingdom RNAi; endosymbiosis; plant-microbe interactions; plant-pathogen interactions.

Fig. 1

Proposed models for the functioning of ckRNAi in pathogenic and mutualistic symbiosis. (a) A representation of the ckRNAi processes occurring between the plant host and a pathogen, such as the Arabidopsis–B.cinerea pathosystem. Fungal components – AGO proteins, extracellular vesicles (EVs) and RNAs – are illustrated in pink and purple; plant components – AGO1 proteins, EVs, RNAs and multivesicular bodies (MVBs) – are illustrated in green and blue. Several possibilities for the transport of sRNAs are represented here (see Box 1), including the transport of sRNAs associated with RNA‐binding proteins and with some level of association with EVs (He et al., 2021); the fungal mechanism is largely unknown and is here represented as a mirror of proposed plant mechanisms. Question marks represent areas of uncertainty in pathogenic ckRNAi. CME, clathrin mediated endocytosis (b) An overview of the ckRNAi interactions that have thus far been described in mutualistic symbioses. ckRNAi has been described in root nodulating symbioses with two different bacterial strains (Ren et al., 2019); whilst ckRNAi in ectomycorrhizal symbiosis has currently been documented in one interaction (Wong‐Bajracharya et al., ; see Table 1 for full gene names). Note the inhibition of membrane remodelling and defence in the AM symbiosis remains to be experimentally verified (Silvestri et al., 2019). Memtubs – membranous tubules – are illustrated in the AM symbiosis. These have been observed between the fungal cell wall (FCW) and fungal arbuscular membrane (FAM) during symbiosis and pathogenic infections of plant tissue, and have been proposed as a source of EVs in AM symbiosis (Roth et al., 2019); this, however, remains unverified, and is represented by the question mark. Dotted lines and question marks represent uncertainty surrounding whether reciprocal ckRNAi from plant to mutualist occurs. AGO, Argonaute, FAM, fungal arbuscular membrane; MPA, mitogen‐activated protein; PAM, peri‐arbuscular membrane; TGS, transcriptional gene silencing; tRFs, red stem loop tRFs shown in root nodule.