Inside-out – from endosomes to extracellular vesicles in fungal RNA transport

Membrane-coupled RNA transport is an emerging theme in fungal biology. Researchers from Heinrich Heine University Düsseldorf review  the RNA cargo and mechanistic details of transport via two inter-related sets of organelles: endosomes and extracellular vesicles for intra- and intercellular RNA transfer. Simultaneous transport and translation of messenger RNAs (mRNAs) on the surface of shuttling endosomes is a conserved process pertinent to highly polarised eukaryotic cells, such as hyphae or neurons. The researchers detail the endosomal mRNA transport machinery components and mRNA targets of the core RNA-binding protein Rrm4. Extracellular vesicles (EVs) are newly garnering interest as mediators of intercellular communication, especially between pathogenic fungi and their hosts. Landmark studies in plant-fungus interactions indicate EVs as a means of delivering various cargos, most notably small RNAs (sRNAs), for cross-kingdom RNA interference. Recent advances and implications of the nascent field of fungal EVs are discussed and potential links between endosomal and EV-mediated RNA transport are proposed.

Cross-kingdom RNAi at the fungus-plant interface mediated by extracellular vesicles (EVs)

During infection, both the fungus and the plant deploy small RNAs (sRNAs) to silence target genes in the interaction partner, as virulence and defence strategies, respectively. Silencing of fungal pathogen genes by plant host sRNAs is termed host-induced gene silencing (HIGS) and vice versa, pathogen-induced gene silencing (PIGS) is brought about by fungal sRNAs in plants. EVs are one of the ways in which sRNAs are transferred between interacting organisms. EVs can be derived from multivesicular endosomes (MVEs) or from budding at the plasma membrane. Endosomes bud inwards during maturation to form intraluminal vesicles, incorporating contents from the cytosol, notably sRNAs and proteins. RNA-binding proteins are thought to be key determinants of RNA loading into EVs. Intraluminal vesicles are released as exosomes upon fusion of the MVE with the plasma membrane. How precisely EVs cross the cell walls and deliver their contents to the recipient cell are currently undetermined.