Transient fusion and selective secretion of vesicle proteins inPhytophthora nicotianaezoospores

Abstract

Secretion of pathogen proteins is crucial for the establishment of disease in animals and plants. Typically, early interactions between host and pathogen trigger regulated secretion of pathogenicity factors that function in pathogen adhesion and host penetration. During the onset of plant infection by spores of the Oomycete, Phytophthora nicotianae, proteins are secreted from three types of cortical vesicles. Following induction of spore encystment, two vesicle types undergo full fusion, releasing their entire contents onto the cell surface. However, the third vesicle type, so-called large peripheral vesicles, selectively secretes a small Sushi domain-containing protein, PnCcp, while retaining a large glycoprotein, PnLpv, before moving away from the plasma membrane. Selective secretion of PnCcp is associated with its compartmentalization within the vesicle periphery. Pharmacological inhibition of dynamin function, purportedly in vesicle fission, by dynasore treatment provides evidence that selective secretion of PnCcp requires transient fusion of the large peripheral vesicles. This is the first report of selective protein secretion via transient fusion outside mammalian cells. Selective secretion is likely to be an important aspect of plant infection by this destructive pathogen.

Phytophthora cinnamomi

“…There are single Ccp genes in both P. parasitica and P. cinnamomi genomes (Table 2). Ccp proteins are stored in an outer shell surrounding an inner core of Lpv glycoproteins within large peripheral vesicles Zhang et al, 2013). Remarkably, during encystment, the small Ccp proteins are secreted, whereas the 500-600-kDa Lpv proteins are retained, an example of selective protein secretion.…”

Specialized attachment structure of the fish pathogenic oomycete Saprolegnia parasitica

“…In the plant pathogen Phytophthora signals such as Ca 2+ uptake or mechanical stimulation have been reported to be responsible to induce full and transient fusion of selective secretion of vesicle proteins (which likely to be an important aspect of host infection [ 13 ]. In this study, we investigated the effect of both chemical and mechanical stimuli on the length and number of bundles.…”

“…A variety of specialized structures such as those aiding ingresses of the fungal pathogen into its host, or adsorption of nutrients (appressoria, hyphodamia, haustoria, etc.) are triggered by the presence of certain ions [ 13 , 16 , 58 , 59 ]. Furthermore, the dynamic nature of the bundles was evidenced by the fact that their length is also affected by the nature of the surface.…”

“…e ., secondary zoospores [ 2 – 4 ] that form secondary cysts that attach to their host prior the infection [ 5 – 8 ]. The ability of the oomycetes to invade a wide range of hosts such as fungi, algae, plants, invertebrates, or vertebrates, indicates that they might have adaptable mechanisms for substrate and host colonization [ 9 – 13 ]. Recent genome and secretome studies have shown that these mechanisms involve diverse molecules including translocated host-targeting proteins [ 14 ], degrading enzymes, such as glycosyl-hydrolases and proteases [ 15 ], or adhesive biopolymers [ 16 , 17 ].…”

Organize, Don’t Agonize: Strategic Success of Phytophthora Species

“…The pathogen cells attach firmly to the outside of the potential host leading to cell entrance and further enhances the development of disease structures, which is a requirement for penetration [30]. While working on P. nicotianae, Zhang et al [49] identified a conserved protein containing short consensus repeats (10 kDa) with a beta-sandwich like arrangement called the Sushi domain. This domain lands onto the plant's surface from other zoospore vesicles by "kiss and run" exocytosis mechanism leading to cell-cell adhesion.…”