Modeling quantitative interactions: the disease outcome of generalist fungal pathogen across the plant kingdom

Botrytis cinerea is a fungal pathogen that causes necrotic disease on more than a thousand known hosts widely spread across the plant kingdom. How B. cinerea interacts with such extensive host diversity remains largely unknown. To address this question, we generated an infectivity matrix of 98 strains of B. cinerea on 90 genotypes representing eight host plants. This experimental infectivity matrix revealed that the disease outcome is largely explained by variations in either the host resistance or pathogen virulence. However, the specific interactions between host and pathogen account for 16% of the disease outcome. Furthermore, the disease outcomes cluster among genotypes of a species but are independent of the relatedness between hosts. When analyzing the host specificity and virulence of B. cinerea, generalist strains are predominant. In this fungal necrotroph, specialization may happen by a loss in virulence on most hosts rather than an increase of virulence on a specific host. To uncover the genetic architecture of Botrytis, a genome-wide association study (GWAS) was performed and revealed 124 genes associated with host specificity and virulence. The genetic architecture of these traits is distinct, polygenic and widespread across B. cinerea genome. The complexity of the disease outcome is best explained by the additivity of small effect genes that adjust the infection to diverse hosts.