Shifts in diversification rates and host jump frequencies shaped the diversity of host range among Sclerotiniaceae fungal plant pathogens

Abstract

The range of hosts that a parasite can infect in nature is a trait determined by its own evolutionary history and that of its potential hosts. However, knowledge on host range diversity and evolution at the family level is often lacking. Here, we investigate host range variation and diversification trends within the Sclerotiniaceae, a family of Ascomycete fungi. Using a phylogenetic framework, we associate diversification rates, the frequency of host jump events and host range variation during the evolution of this family. Variations in diversification rate during the evolution of the Sclerotiniaceae define three major macro‐evolutionary regimes with contrasted proportions of species infecting a broad range of hosts. Host–parasite cophylogenetic analyses pointed towards parasite radiation on distant hosts long after host speciation (host jump or duplication events) as the dominant mode of association with plants in the Sclerotiniaceae. The intermediate macro‐evolutionary regime showed a low diversification rate, high frequency of duplication events and the highest proportion of broad host range species. Our findings suggest that the emergence of broad host range fungal pathogens results largely from host jumps, as previously reported for oomycete parasites, probably combined with low speciation rates. These results have important implications for our understanding of fungal parasites evolution and are of particular relevance for the durable management of disease epidemics.

Quantitative interactions driveBotrytis cinereadisease outcome across the plant kingdom

“…Critically, the strains that display host preference appear to have lost virulence on the nonpreferred hosts rather than gained enhanced virulence on the preferred host. This could be favoured by host jumps at high frequency and low speciation rate (Navaud et al, 2018).…”

Small RNAs from the plant pathogenic fungus Sclerotinia sclerotiorum highlight host candidate genes associated with quantitative disease resistance

“…Since sRNAs from plant pathogenic fungi are likely to suppress host genes functioning in disease resistance, we hypothesized that the prediction of plant genes targeted by fungal sRNAs could be combined with a GWAS to aid identification of plant genes relevant to QDR. Like B. cinerea, S. sclerotiorum is a plant pathogen belonging to the Sclerotiniaceae family of Ascomycete fungi, which is able to infect hundreds of plant species (Kabbage et al, 2015;Navaud et al, 2018). Sclerotinia sclerotiorum is widely dispersed throughout the world and poses a significant threat to agricultural production (Derbyshire and Denton-Giles, 2016).…”

Selective sweeps in populations of the broad host range plant pathogenic fungusSclerotinia sclerotiorum

“…When a favourable allele increases in frequency due to positive 47 genome sequence of S. sclerotiorum was recently sequenced to completion using PacBio 76 technology and has been annotated using extensive RNA sequencing data and manual 77 curation (23). This species is a host generalist that infects more than 600 species of plant 78 (24). It has been globally disseminated and is present in numerous environments where it 79 causes significant yield losses in economically important crops (25).…”