An effector protein of Fusarium graminearum targets chloroplasts and suppresses cyclic photosynthetic electron flow

Abstract Chloroplasts are important photosynthetic organelles that regulate plant immunity, growth, and development. However, the role of fungal secretory proteins in linking the photosystem to the plant immune system remains largely unknown. Our systematic characterization of 17 chloroplast-targeting secreted proteins of Fusarium graminearum indicated that Fg03600 is an important virulence factor. Fg03600 translocation into plant cells and accumulation in chloroplasts depended on its chloroplast transit peptide. Fg03600 interacted with the wheat (Triticum aestivum L.) proton gradient regulation 5-like protein 1 (TaPGRL1), a part of the cyclic photosynthetic electron transport chain, and promoted TaPGRL1 homo-dimerization. Interestingly, TaPGRL1 also interacted with ferredoxin (TaFd), a chloroplast ferredoxin protein that transfers cyclic electrons to TaPGRL1. TaFd competed with Fg03600 for binding to the same region of TaPGRL1. Fg03600 expression in plants decreased cyclic electron flow (CEF) but increased the production of chloroplast-derived reactive oxygen species (ROS). Stably silenced TaPGRL1 impaired resistance to Fusarium head blight (FHB) and disrupted CEF. Overall, Fg03600 acts as a chloroplast-targeting effector to suppress plant CEF and increase photosynthesis-derived ROS for FHB development at the necrotrophic stage by promoting homo-dimeric TaPGRL1 or competing with TaFd for TaPGRL1 binding.