Quantification of colletotrichum fioriniae in orchards and deciduous forests indicates it is primarily a leaf endophyte

Colletotrichum fioriniae of the C. acutatum species complex is an important hemibiotrophic pathogen of vegetables and fruits in temperate regions worldwide. In apple, it is one of the primary species responsible for bitter rot disease. Understanding the disease cycle is complicated because many broadleaf plants can be hosts of C. fioriniae. By detecting and quantifying rain-splashed C. acutatum species complex conidia in more than 500 samples from heavily bitter-rot-infected apple orchards and nearby forested woodlots over two summers, we show that conidial quantities were higher in the woodlots than in the orchards. Testing of more than 1,000 surface-disinfected leaves of apple and 24 different forest plant species showed that overall C. fioriniae was an abundant leaf endophyte, with high variation in leaf colonization area. Endophytic isolates from leaves were pathogenic on apples, and multilocus sequence analysis showed 100% identity between most isolates from leaves and diseased fruits. Apple leaves endophytically infected with C. fioriniae were present in a conventionally managed orchard and abundant in an untreated orchard. These lines of evidence, in the context of previously published research, lead us to hypothesize that the main ecological role of C. fioriniae is that of a leaf endophyte, which we present as a generalized C. fioriniae infection cycle that provides an updated framework for its integrated management in agricultural systems.