Multi-omics approaches to explore phenotypic and genetic diversity in the brown rot fungal pathogens Monilinia fructicola, Monilinia laxa and Monilinia fructigena

Monilinia fructicola, Monilinia fructigena and Monilinia laxa are the main causal agents of brown rot and blossom blight, among the most important diseases on pome and stone fruits, worldwide responsible for heavy losses both in the field and in postharvest. Following the introduction of M. fructicola into Europe in 2001, the pathogen spread widely and rapidly, and became prevalent over the endogenous species M. laxa and M. fructigena. To improve knowledge on the biology, evolutionary history, and diversity of these important pathogens, high-quality reference genomes and transcriptomes of M. fructicola strain Mfrc123, M. fructigena strain Mfrg269 and M. laxa strain Mlax316 were de novo assembled and compared. In particular we explored: (i) phylogenomic and synthenic relationships between the Monilinia genomes and those of the closely related species within Sclerotiniaceae, Botrytis cinerea and Sclerotinia sclerotiorum; (ii) the abundance and evolutionary dynamics of transposable element; (iii) the genetic basis of mating type and the genome-wide occurrence and extent of Repeat-Induced Point (RIP) mutations; and (iv) common and species-specific effectors, carbohydrate-active enzymes and secondary metabolite gene clusters with some differences that might explain host plants and organ preferences distinguishing the three Monilinia species. Moreover, a metagenomic approach was used to investigate the mycovirome of M. fructicola in a worldwide collection of isolates from different hosts and revealed a great abundance and variety of mycoviruses infecting the fungus. A total of 32 positive-sense single-stranded (ss)RNA viruses and a new putative ssDNA mycovirus were identified and characterized.