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 critical diseases on pome and stone fruits, responsible for heavy losses both in the field and in postharvest. Following the introduction of M. fructicola into Europe, the plant pathogen spread widely and rapidly and became prevalent over the endogenous species M. laxa and M. fructigena. To improve knowledge of biology, evolutionary history, and diversity of these important plant pathogens, high-quality reference genomes and transcriptomes of M. fructicola Mfrc123, M. fructigena Mfrg269 and M. laxa Mlax316 were de novo assembled and compared. The study was focused on several key areas: (i) phylogenomic and synthenic relationships between the Monilinia genomes and those of the closely related species Botrytis cinerea and Sclerotinia sclerotiorum; (ii) the abundance and evolutionary dynamics of transposable elements; (iii) the genetic basis of mating type and the genome-wide occurrence and extent of Repeat-Induced Point (RIP) mutations; (iv) common and species- specific effectors, carbohydrate-active enzymes and secondary metabolite gene clusters; and v) gene expression profiling under different cultural conditions. The results highlighted several 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, which revealed a great abundance and diversity 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.