Journal
PLANT CELL
Volume 33, Issue 9, Pages 3151-3175Publisher
OXFORD UNIV PRESS INC
DOI: 10.1093/plcell/koab170
Keywords
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Funding
- Natural Sciences and Engineering Research Council of Canada
- Canadian Foundation for Innovation
- National Aeronautics and Space Administration (NASA) [80NSSC18K1462]
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The actin cytoskeleton plays a critical role in regulating cellular activities in plant-microbe interactions and immunity. The assembly and turnover of actin filaments at pathogen interaction sites are regulated by the ARP2/3 complex and W/SRC. Phosphatidylinositol-4,5-bisphosphate accumulation at fungal penetration sites modulates actin patch formation.
The actin cytoskeleton regulates an array of diverse cellular activities that support the establishment of plant-microbe interactions and plays a critical role in the execution of plant immunity. However, molecular and cellular mechanisms regulating the assembly and rearrangement of actin filaments (AFs) at plant-pathogen interaction sites remain largely elusive. Here, using live-cell imaging, we show that one of the earliest cellular responses in Arabidopsis thaliana upon powdery mildew attack is the formation of patch-like AF structures beneath fungal invasion sites. The AFs constituting actin patches undergo rapid turnover, which is regulated by the actin-related protein (ARP)2/3 complex and its activator, the WAVE/SCAR regulatory complex (W/SRC). The focal accumulation of phosphatidylinositol-4,5-bisphosphate at fungal penetration sites appears to be a crucial upstream modulator of the W/SRC-ARP2/3 pathway-mediated actin patch formation. Knockout of W/SRC-ARP2/3 pathway subunits partially compromised penetration resistance with impaired endocytic recycling of the defense-associated t-SNARE protein PEN1 and its deposition into apoplastic papillae. Simultaneously knocking out ARP3 and knocking down the Class I formin (AtFH1) abolished actin patch formation, severely impaired the deposition of cell wall appositions, and promoted powdery mildew entry into host cells. Our results demonstrate that the ARP2/3 complex and formins, two actin-nucleating systems, act cooperatively and contribute to Arabidopsis penetration resistance to fungal invasion.
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