The Fusarium graminearum Effector Protease FgTPP1 Suppresses Immune Responses and Facilitates Fusarium Head Blight Disease

Abstract

Most plant pathogens secrete effector proteins to circumvent host immune responses, thereby promoting pathogen virulence. One such pathogen is the fungus Fusarium graminearum, which causes Fusarium head blight (FHB) disease on wheat and barley. Transcriptomic analyses revealed that F. graminearum expresses many candidate effector proteins during early phases of the infection process, some of which are annotated as proteases. However, the contributions of these proteases to virulence remain poorly defined. Here, we characterize an F. graminearum endopeptidase, FgTPP1 (FGSG_11164), that is highly upregulated during wheat spikelet infection and is secreted from fungal cells. To elucidate the potential role of FgTPP1 in F. graminearum virulence, we generated FgTPP1 deletion mutants (∆Fgtpp1) and performed FHB infection assays. Deletion of FgTPP1 reduced the virulence of F. graminearum as assessed by spikelet bleaching. Infection with wild-type F. graminearum induced full bleaching in about 50% of the spikes at 10 to 11 days postinfection, whereas this fraction was reduced to between 18 and 27% when using ∆Fgtpp1 mutants. Transient expression of green fluorescent protein-tagged FgTPP1 revealed that FgTPP1 localizes, in part, to chloroplasts and attenuates chitin-mediated activation of mitogen-activated protein kinase signaling, reactive oxygen species production, and cell death induced by an autoactive disease resistance protein when expressed in planta. Notably, the FgTPP1 protein is conserved across the Ascomycota phylum, suggesting that it may be a core effector among ascomycete plant pathogens. These properties make FgTPP1 an ideal candidate for decoy substrate engineering, with the goal of engineering resistance to FHB.