Effector biology during biotrophic invasion of plant cells

Chaudhari, Prateek; Ahmed, Bulbul; Joly, David L; Germain, Hugo

Pathogens are known to target host vesicular trafficking, a key element of plant defense. 30 In H. arabidopsidis, 26% of examined effectors have been found to localize to membranes, the majority of them (18%) associating with the endoplasmic reticulum. 63 Arabidopsis cells hosting H. arabidopsidis haustoria develop bulging vesicular structures compared with non-infected cells, 30 the occurrence of such vesicles being attributed to presence of the pathogen. It is possible that the formation of these vesicles is driven by a particular effector or effectors to upset vesicular movement and disrupt any organized defense response. They may also be pathogen-driven and provide the extra-phospholipid bilayer required at the plasma membrane to accommodate fastexpanding haustoria. Regardless, support for the fact that these are vacuolar structures comes from the observations of very similar structures in cotyledons of transgenic Arabidopsis γ-TIP-GFP plants. 64 Other types of membrane structures have been shown to differentially localize around haustoria formed by H. arabidopsidis and P. infestans. 60 HaRxL17 localizes to the EHM during infection by H. arabidopsidis. However, in the absence of the pathogen, it localizes to the tonoplast where its ability to enhance plant susceptibility is possibly linked with a task in plant cell membrane trafficking. 30 Since tonoplast is located close to the EHM along with the effector HaRxL17 in the event of infection, the effector may be interfering with plant cell membrane trafficking, and interestingly, this also suggests a role for tonoplast in EHM formation. However, no single effector has been reported to cause the bulb-like vesicular structures observed in the presence of growing pathogens, 29 and it is not clear whether it is a plant defense response or an effector-driven process. Surprisingly, our understanding of the detailed mechanism of vacuolar biogenesis is still limited, justifying the need to push the investigation further into such peculiar vesicular structures. It is difficult to elucidate possible pathways being targeted by pathogens to hinder vesicular trafficking and eventually give rise to these bulb-like structures. In A. thaliana, a point mutation in the deubiquitinating enzyme AMSH3 renders cells incapable of forming central lytic vacuoles. In addition, amsh3 mutant cells accumulate autophagosomes and incorrectly sort their vacuolar protein cargo. 65 Vacuoles are important in various plant defense mechanisms, and two vacuole-mediated mechanisms have been postulated to affect programmed cell death. 66 In one of them, vacuolar-processing enzymes mediate vacuolar membrane disruption, thus releasing vacuolar content into the cell cytoplasm (demonstrated for viral infection). 67 In the second proposed mechanism, vacuole fusion with the plasma membrane enables the extracellular release of vacuolar content (demonstrated in bacterial infection). 68 Interestingly and coincidentally, phenotypic similarity between vesicular structures from amsh3 mutants and cells hosting haustoria can be noticed. 60, 65 This concurring vesicular signature suggests that pathogens could be targeting AMSH3 (or similar components) to alter the vesicular pathway.