Update on Secretory Pathways in Plant Immune Responses Secretory Pathways in Plant Immune Responses

Innate immune receptors in plants detect the presence of microbial pathogens and trigger defense responses to terminate or restrict pathogen growth. The molecular mechanisms of receptor-mediated nonself recognition and subsequent intracellular signaling pathways have received much attention in the past. Less is known about the cellular mechanisms that contribute to the execution of immune responses. Recent studies revealed the existence of a secretory machinery that becomes engaged in the execution of extracellular immune responses. At least two vesicleassociated and SNARE protein-mediated exocytosis pathways appear to drive focal and/or nondirectional secretion of antimicrobial cocktails comprising proteins, small molecules, and cell wall building blocks into the apoplastic space. Both pathways have additional functions in plant development and might have been coopted for immune responses. Bacteria and fungi appear to have evolved counterdefense molecules that intercept the secretion machinery by blocking vesicle formation from intracellular membranes. Independently from this, plant plasma membrane ATP-binding cassette-type (ABC) transporters act in parallel defense pathways and serve as efflux pumps for the targeted delivery of antimicrobials and/or agents promoting chemical cross-linking of plant cell wall polymers. All multicellular eukaryotic organisms are exposed to the danger of microbial pathogens. Unlike animals, plants lack specialized and mobile immune cells to engulf and dismantle microbial intruders. Plants resist microbial attack using elaborate nonself surveillance systems consisting of a repertoire of cell surface and intracellular immune sensors. These receptors detect the presence of parasites and trigger powerful immune responses (for review, see Jones and Dangl, 2006). Microbial parasites have evolved diverse strategies to enter hosts for nutrient retrieval and multiplication. It is conceivable that plants have invented execution mechanisms for immune responses that are fine tuned to microbial entry routes. For example, most microbial pathogens such as bacteria and fungi first come into contact with plant epidermal cells (Fig. 1). In contrast to many bacterial pathogens of vertebrates that multiply inside host cells, the majority of plant pathogenic bacteria remain in the intercellular space (apoplast) after entering the interior of plant organs through natural openings such as stomata (Fig. 1). Similarly, some fungal parasites such as Cladosporium fulvum infect plant leaves by growth of fungal hyphae in the apoplastic space (Thomma et al., 2005). Thus, plants must have evolved defense mechanisms to terminate extracellular colonization attempts. Even for parasitic fungi that enter host cells through direct penetration of the plant cell wall, pathogenesis is often terminated prior to invasive growth at the host cell periphery (Johnson et al. 1982; Hoogkamp et al., 1998), indicating the existence of apoplastic defense. The exterior of plant cells such as the cell wall or leaf cuticle can be considered as preformed physical barriers to invasive pathogens. Indeed, cell wallpenetrating fungal species in general secrete hydrolytic enzymes to degrade the cuticles and cell walls of plant cells and frequently form specialized pad-like infection structures, called appressoria, to initiate entry into plant cells (Kolattukudy, 1985; Mendgen and Deising, 1993; Knogge, 1996). In many cases plant cells respond to such entry attempts by de novo cell wall biosynthesis and by local deposition of the newly synthesized cell wall material, including the (1/3)-bD-glucan callose, into the paramural space between the cell wall and the plasma membrane (Aist, 1976; Belanger et al., 2002). This localized thickening is called a papilla and is thought to represent an inducible reinforcement of the cell wall against pathogen entry. However, callose-rich papillae are also found at contact sites between plant cells and bacteria that do not penetrate plant cell walls (Bestwick et al., 1995), thereby pointing to additional more complex roles in plant defense. One remarkable feature of pathogen-induced papillae is their spatial confinement to microbial contact sites (typically representing a small circular area at the periphery of a single plant cell), suggesting directional delivery of cell wall precursors and/or cell wallsynthesizing enzymes to incipient infection sites. Focal redistribution of the actin cytoskeleton and the congregation of cellular organelles such as the nucleus, Golgi, the endoplasmic reticulum (ER), peroxisomes, and vesicle-like structures beneath microbial contact sites suggest that papilla formation may represent one 1 This work was supported by funds from the Max Planck Society and the Deutsche Forschungsgemeinschaft (SFB670 and SPP1212). * Corresponding author; e-mail [email protected]. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Paul Schulze-Lefert ([email protected]). www.plantphysiol.org/cgi/doi/10.1104/pp.108.121566