Plant Extracellular Vesicles with Complex Molecular Cargo: A Cross-Kingdom Conduit for MicroRNA-Directed RNA Silencing

Plants secrete a heterogenous population of membrane-enclosed extracellular vesicles that harbour an incredible diversity of molecular cargo. It is the complexity of the molecular cargo encapsulated by plant extracellular vesicles (PEVs) which facilitates the fundamental role PEVs play in mediating communication and signalling. PEV molecular cargo is composed of a diverse mixture of lipids, metabolites, proteins, and nucleic acids. Among the nucleic acids, the microRNA (miRNA) class of small regulatory RNA can be viewed as one of the most biologically relevant. Plant miRNAs regulate the expression of genes essential for all aspects of development as well as to control the gene expression changes required to drive the adaptive and defensive responses of plants to environmental stress and pathogen attack. Furthermore, recent research has shown that specific miRNA cohorts are selectively packaged into PEVs as part of the molecular-level response of a plant to its growth environment. For example, PEVs are loaded with a specific miRNA population for their targeted delivery to sites of pathogen infection in the host plant, or for cross-kingdom delivery of host-plant-encoded miRNAs to the pathogen itself. Here we outline PEV physical properties, compare PEV biogenesis pathways, detail the composition of PEV molecular cargo, and go on to provide detailed commentary on the role of PEV-delivered miRNAs in plant development, environmental stress adaptation, and pathogen defence. We conclude this article with a proposal for the potential future use of PEVs and their miRNA cargo in agriculture and aquaculture.