Tracking of Diversity and Evolution in the Brown Rot Fungi Monilinia fructicola, Monilinia fructigena, and Monilinia laxa.

Francesco Faretra,Celeste Raguseo,Stefania Pollastro,Rita Milvia De Miccolis Angelini,Lucia Landi,Gianfranco Romanazzi

doi:10.3389/fmicb.2022.854852

Abstract

Monilinia species are among the most devastating fungi worldwide as they cause brown rot and blossom blight on fruit trees. To understand the molecular bases of their pathogenic lifestyles, we compared the newly assembled genomes of single strains of Monilinia fructicola, M. fructigena and M. laxa, with those of Botrytis cinerea and Sclerotinia sclerotiorum, as the closest species within Sclerotiniaceae. Phylogenomic analysis of orthologous proteins and syntenic investigation suggest that M. laxa is closer to M. fructigena than M. fructicola, and is closest to the other investigated Sclerotiniaceae species. This indicates that M. laxa was the earliest result of the speciation process. Distinct evolutionary profiles were observed for transposable elements (TEs). M. fructicola and M. laxa showed older bursts of TE insertions, which were affected (mainly in M. fructicola) by repeat-induced point (RIP) mutation gene silencing mechanisms. These suggested frequent occurrence of the sexual process in M. fructicola. More recent TE expansion linked with low RIP action was observed in M. fructigena, with very little in S. sclerotiorum and B. cinerea. The detection of active non-syntenic TEs is indicative of horizontal gene transfer and has resulted in alterations in specific gene functions. Analysis of candidate effectors, biosynthetic gene clusters for secondary metabolites and carbohydrate-active enzymes, indicated that Monilinia genus has multiple virulence mechanisms to infect host plants, including toxins, cell-death elicitor, putative virulence factors and cell-wall-degrading enzymes. Some species-specific pathogenic factors might explain differences in terms of host plant and organ preferences between M. fructigena and the other two Monilinia species.

Highlights

Phylogenetic investigations suggest that M. laxa and M. fructigena are close to each other, while M. fructicola is more distant from them, they all derive from a common ancestor
The three Monilinia species are closely related to B. cinerea and S. sclerotiorum, within the family Sclerotiniaceae, and grouped in the “sclerotinioid” clade within Helotiales
Synteny results indicated that M. laxa is the closest to the other Sclerotiniaceae species investigated, which suggests that M. laxa was the earliest differentiated through the speciation process

Summary

Introduction

Ruhland) Honey are the main causal agents of brown rot and blossom blight on fruit trees. They are Ascomycetes fungi that are included in the family Sclerotiniaceae, order Helotiales, and they are responsible for one of the most important and common diseases on stone and pome. Comparative Genomics of Monilinia Species fruit in the field, as well as postharvest, causing heavy yield losses and reducing shelf-life (Petróczy et al, 2012; Martini and Mari, 2014). Monilinia laxa was the prevalent species in California (United States) in the first half of the 20th century (Hewitt and Leach, 1939), and was first identified as the causal agent of brown rot on stone fruit in Europe (Byrde and Willets, 1977). M. laxa is a quarantine pathogen in China and in some parts of North America (Martini and Mari, 2014)

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