Extracellular vesicles including exosomes in cross kingdom regulation: a viewpoint from plant-fungal interactions.

Abstract

Throughout evolution, plants and pathogenic fungi have been in a constant battle where fungi have developed new mechanisms to infect plants while plants have co-evolved to combat the infection. The early stages of plant-pathogen interactions occur in the intercellular spaces of the plant tissue and thus involve a myriad of secreted factors. Traditionally, all proteins released into the extracellular space were thought to be transported via the ER-Golgi dependent classical secretory pathway. However, non-classical secretion of proteins/RNA through extracellular vesicles (EVs) has recently been reported to contribute to the milieu of extracellular molecules that mediate plant-fungal interactions (Rodrigues et al., 2007; Meyer et al., 2009). EVs can be broadly classified into exosomes and ectosomes (Keerthikumar et al., 2015). Exosomes are secreted microvesicles (30–150 nm in diameter) of endocytic origin that are released by multiple cell types and are conserved across various species (Lotvall et al., 2014; Gangoda et al., 2015). In contrast, ectosomes or shedding microvesicles are larger (100–1000 nm in diameter) and bud off directly from the plasma membrane (Keerthikumar et al., 2015). For clarity, we will collectively refer to both types of membranous vesicles as EVs in this article. Recent studies on mammalian systems have highlighted the role of EVs in cell-cell communication and the intercellular transport of cargo (proteins, nucleic acids, and carbohydrates) (Batista et al., 2011; Cossetti et al., 2014). Whilst the role of EVs in plant-fungal interactions is still poorly defined, this non-canonical secretory pathway has been proposed as an alternative route for the secretion of virulence and defense molecules by fungi and plants, respectively (Robatzek, 2007; Rodrigues et al., 2011). The basic requirement for successful host colonization is the establishment of a parasitic relationship between the fungal pathogen and the host. This requires the induction of specific defense mechanisms in the fungus for protection against the plant innate immune system (Hayes et al., 2013). Evasion or suppression of the plant defense response is thought to be regulated by virulence factors that are secreted from the fungus and act at the plasma membrane or in the cytoplasm of the plant cell (Rodrigues et al., 2008a). Interestingly, recent studies allude to the EV-mediated transport of virulence factors from the fungus into the host cell as a more efficacious delivery mechanism than simple diffusion (Rodrigues et al., 2008a; Silverman and Reiner, 2011). Similarly, in plants, when the integrity of the cell wall is threatened by a fungal pathogen, a response is mediated, at least in part, by multivesicular bodies (MVBs) (An et al., 2006b). In mammalian cells, it is well documented that fusion of MVBs with the plasma membrane results in the secretion of exosomes (Boukouris and Mathivanan, 2015; Gangoda et al., 2015). Though the production of MVBs may not always result in the secretion of EVs, the observation that plants produce MVBs in response to a fungal infection leads to the speculation that EVs may play a critical role in plant-fungal interactions. Here, we will discuss the current knowledge on EVs in the context of human-fungal interactions and their potential roles in plant-fungal interactions.