Phylogenomics of Plant-Associated Botryosphaeriaceae Species

Abstract

The Botryosphaeriaceae is a fungal family that includes many destructive vascular pathogens of woody plants (e.g., Botryosphaeria dieback of grape, Panicle blight of pistachio). Species in the genera Botryosphaeria, Diplodia, Dothiorella, Lasiodiplodia, Neofusicoccum, and Neoscytalidium attack a range of horticultural crops, but they vary in virulence and their abilities to infect their hosts via different infection courts (flowers, green shoots, woody twigs). Isolates of seventeen species, originating from symptomatic apricot, grape, pistachio, and walnut were tested for pathogenicity on grapevine wood after 4 months of incubation in potted plants in the greenhouse. Results revealed significant variation in virulence in terms of the length of the internal wood lesions caused by these seventeen species. Phylogenomic comparisons of the seventeen species of wood-colonizing fungi revealed clade-specific expansion of gene families representing putative virulence factors involved in toxin production and mobilization, wood degradation, and nutrient uptake. Statistical analyses of the evolution of the size of gene families revealed expansions of secondary metabolism and transporter gene families in Lasiodiplodia and of secreted cell wall degrading enzymes (CAZymes) in Botryosphaeria and Neofusicoccum genomes. In contrast, Diplodia, Dothiorella, and Neoscytalidium generally showed a contraction in the number of members of these gene families. Overall, species with expansions of gene families, such as secreted CAZymes, secondary metabolism, and transporters, were the most virulent (i.e., were associated with the largest lesions), based on our pathogenicity tests and published reports. This study represents the first comparative phylogenomic investigation into the evolution of possible virulence factors from diverse, cosmopolitan members of the Botryosphaeriaceae.

Comparative Genomics Reveals Evolutionary Traits, Mating Strategies, and Pathogenicity-Related Genes Variation of Botryosphaeriaceae

“…Currently, genomics technology has been widely used to study many pathogenic fungi of plants, and greatly promoted the understanding of their evolution and pathogenic mechanisms ( Islam et al, 2012 ; Blanco-Ulate et al, 2013 ; van der Nest et al, 2014 ; Nagel et al, 2018 ; Félix et al, 2019 ; Landi et al, 2020 ; Meile et al, 2020 ). For example, gene family expansion associated with virulence factors in wood-colonizing pathogenic fungi in the Botryosphaeriaceae was revealed via phylogenomic comparisons ( Garcia et al, 2021 ); the comparative genome analyses of latent plant pathogens in the Botryosphaeriaceae were conducted to define their genomes ( Nagel et al, 2021 ). In addition, a large-scale comparative genomic analysis can better reveal the physiological characteristics and evolutionary history of fungi ( Guttman et al, 2014 ; Haridas et al, 2020 ; Miyauchi et al, 2020 ).…”

Diversity of Neofusicoccum parvum for the Production of the Phytotoxic Metabolites (-)-Terremutin and (R)-Mellein

“…We also identified polymorphisms in genes involved in (-)-terremutin and ( R )-mellein biosynthesis among these four isolates. Such high level of genetic variations within a species could be a consequence of the evolution and adaptation of N. parvum to its biotic environment as already suggested [ 69 ]. The phylogenetic tree constructed with Np-UCR-NP2, Np-UCD-646-So, Np-Bt67 and Np-B sequences clearly showed that Np-B/Np-UCD-646-So and Np-Bt67/Np-UCR-NP2 clustered as separate clades ( Figure S3 ).…”

A New Disease for Europe of Ficus microcarpa Caused by Botryosphaeriaceae Species

“…Many factors can be involved in the ability of some Botryosphaeriaceae species to jump from one host to another, meaning that they are more virulent than other species. Among these, a recent study [ 46 ] revealed how some groups of taxa, such as Botryosphaeria , Lasiodiplodia , and Neofusicoccum , show an expansion of certain clades of gene families involved in the pathogenesis. Specifically, in the Botryosphaeria and Neofusicoccum genomes, an expansion of secreted cell-wall-degrading enzymes (CAZymes) was observed [ 46 ].…”

“…Among these, a recent study [ 46 ] revealed how some groups of taxa, such as Botryosphaeria , Lasiodiplodia , and Neofusicoccum , show an expansion of certain clades of gene families involved in the pathogenesis. Specifically, in the Botryosphaeria and Neofusicoccum genomes, an expansion of secreted cell-wall-degrading enzymes (CAZymes) was observed [ 46 ]. It is no surprise that the species identified in this study also occurred on other taxonomically distant hosts in Sicily.…”