CELLULAR AND MOLECULAR MECHANISMS UNDERLYING INCOMPATIBLE AND COMPATIBLE INTERACTIONS BETWEEN HOST ARABIDOPSIS AND POWDERY MILDEWS

The powdery mildew disease, caused by fungal species in the Erysiphales, have great agriculture and economic importance. Plants evolved three types of responses upon the mildew attack: penetration resistance, post-invasion resistance and susceptibility. Penetration resistance is achieved mainly through the formation of papillae underneath pathogen-attempted entry sites as a reinforcement of the cell wall. The depositions of callose, lignin and defense-associated protein PEN1 into papillae play important roles in penetration resistance. However, cellular mechanisms underlying the transport of these components to the apoplastic papillae are not clear. In this study I show that Arabidopsis form actin patches under invasion sites as one of the earliest cellular responses upon fungal attack. The formation of actin patches is regulated by actin-related protein (ARP)2/3 complex and its upstream activators, WAVE/SCAR regulatory complex (W/SRC). Furthermore, mutation of ARP2/3 complex subunit impairs the endocytosis of PEN1 and reduces the deposition of PEN1 into papillae. My data indicate that W/SRC-ARP2/3 pathway regulates the reorganization of the actin cytoskeleton during plant-fungi interactions and contributes to the penetration resistance. Using pharmacological, cellular and genetic approaches, I demonstrate that the temporal-spatial aggregation of monolignol biosynthesis enzyme towards penetration sites contributes to the papillary lignification and penetration resistance. The papillary lignification is a cell-autonomous process and is regulated by actin cytoskeleton and myosins. My results reveal that the lignification process in defense responses is distinct from the developmental lignification process in plants. After successful entering plant cells, compatible powdery mildews form haustoria for nutrients uptake and the haustoria are tightly enveloped by a highly modified extrahaustorial membrane (EHM). Little is known about the EHM biogenesis and identity. My results demonstrate that among the two plasma membrane phosphoinositides in Arabidopsis, PI(4,5)P2 is dynamically up-regulated at powdery mildew infection sites and recruited to the EHM, whereas PI4P is absent at the EHM. Furthermore, depleting PI(4,5)P2 in pip5k1 pip5k2 mutants inhibits fungal pathogen development, which does not due to the increased defense responses. My results reveal that plant filamentous phytopathogens recruit host PI(4,5)P2 to the EHM as a susceptibility factor for plant disease