Plant infection by the necrotrophic fungusBotrytisrequires actin-dependent generation of high invasive turgor pressure

Abstract

AbstractThe devastating pathogenBotrytis cinereainfects a broad spectrum of host plants, causing great socio-economic losses. The necrotrophic fungus rapidly kills plant cells, nourishing their walls and cellular contents. To this end, necrotrophs secretes a cocktail of cell wall degrading enzymes, phytotoxic proteins and metabolites. Additionally, many fungi produce specialized invasion organs that generate high invasive pressures to force their way into the plant cell. However, for most necrotrophs, includingBotrytis, the biomechanics of penetration and its contribution to virulence are poorly understood. Here we use a combination of quantitative micromechanical imaging and CRISPR-Cas guided mutagenesis to show thatBotrytisuses substantial invasive pressure, in combination with strong surface adherence, for penetration. We found that the fungus establishes a unique mechanical geometry of penetration that develops over time during penetration events, and which is actin cytoskeleton dependent. Furthermore, interference of force generation by blocking actin polymerization was found to decreaseBotrytisvirulence, indicating that also for necrotrophs, mechanical pressure is important in host colonization. Our results demonstrate for the first time mechanistically how a necrotrophic fungus such asBotrytisemploys this “brute force” approach, in addition to the secretion of lytic proteins and phytotoxic metabolites, to overcome plant host resistance.