At knifepoint: Appressoria-dependent turgor pressure of filamentous plant pathogens

Filamentous pathogens need to overcome plant barriers for successful infection. To this end, special structures, most commonly appressoria, are used for penetration. In differentiated appressoria, the generation of high turgor pressure is mandatory to breach plant cell wall and cuticle. However, quantitative description of turgor pressure and resulting invasive forces are only described for a handful of plant pathogens. Recent advances in methodology allowed determination of surprisingly high pressures and corresponding forces in oomycetes and a necrotrophic fungus. Here, we describe turgor generation in appressoria as essential function for host penetration. We summarize the known experimentally determined turgor pressure as well as invasive forces and discuss their universal role in plant pathogen infection.To establish a successful host interaction, pathogens have to adhere to and penetrate preformed plant barriers such as cuticle, cell wall and plasma membrane [1,2]. By developing specialized infection structures, such as appressoria and penetration hyphae, fungi and oomycetes have evolved sophisticated strategies to (mechanistically) overcome these barriers. The formation of infection structures after spore germination is triggered by physical and chemical signals of the plant surface, such as hardness of the surface, its topography, hydrophobicity and chemical cues such as nutrients, cutin monomers or ethylene [3,4]. Processing of these signals involves several signaling pathways, including G proteins, cyclic AMP (cAMP), the target of rapamycin (TOR) pathway, calcium/calmodulin-mediated pathways, and mitogen-activated protein (MAP) kinases [5, 6, 7]. In Magnaporthe oryzae, the MAP kinase Pmk1 is a master regulator of infection-related development, including appressoria function. Recently, a phosphoproteomics approach confirmed the particular importance of PMK1 by identifying 32 direct substrates, and additionally demonstrated a high degree of homology in the phosphorylation landscape of fungi [8]. In most cases, invasion starts with either simple appressoria or compound appressoria (e.g. infection cushions), followed by penetration and infection hyphae or haustoria, depending on the fungus [1,9,10]. Various types of appressoria are the most common early infection structures of filamentous plant pathogens. Initially, the hyphal tip of the emerging germ tube is attaching to the plant surface, sensing the physical and chemical cues required to trigger appressorium formation [1]. At the future site of penetration, the forming appressorium attaches to the plant surface by either entering through stomata, a strategy rust fungi employ [11], or directly breaching through the cuticle and cell wall. In the latter case turgor pressure is generated, reaching up to 80 bar [12]. In this review, we focus on turgor formation in appressoria as essential function for host penetration in fungi and oomycetes. In addition, we discuss the role of secreted enzymes during penetration.

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