Stealth Pathogens: The Sooty Blotch and Flyspeck Fungal Complex

Sooty blotch and flyspeck (SBFS) fungi produce superficial, dark-colored colonies on fruits, stems, and leaves of many plant genera. These blemishes are economically damaging on fruit, primarily apple and pear, because they reduce the sale price of fresh fruit. Fungicide spray programs can control SBFS but are costly and impair human and environmental health; thus, less chemically intensive management strategies are needed. Although the scientific study of SBFS fungi began nearly 200 years ago, recent DNA-driven studies revealed an unexpectedly diverse complex: more than 100 species in 30 genera of Ascomycota and Basidiomycota. Analysis of evolutionary phylogenetics and phylogenomics indicates that the evolution of SBFS fungi from plant-penetrating ancestors to noninvasive ectophytic parasites was accompanied by a massive contraction of pathogenicity-related genes, including plant cell wall-degrading enzymes and effectors, and an expansion of cuticle-degradation genes. This article reviews progress in understanding SBFS taxonomy and ecology and improving disease management. We also highlight recent breakthroughs in reconstructing the evolutionary origins of these unusual plant pathogens and delineating adaptations to their ectophytic niche.