Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium

Abstract

Filamentous fungi within the Fusarium graminearum species complex (Fg complex) are the primary etiological agents of Fusarium head blight (scab) of wheat and barley. Scab is an economically devastating plant disease that greatly limits grain yield and quality. In addition, scabby grain is often contaminated with trichothecene mycotoxins that act as virulence factors on some hosts, and pose a serious threat to animal health and food safety. Strain-specific differences in trichothecene metabolite profiles (chemotypes) are not well correlated with the Fg complex phylogeny based on genealogical concordance at six single-copy nuclear genes. To examine the basis for this discord between species and toxin evolution, a 19-kb region of the trichothecene gene cluster was sequenced in 39 strains chosen to represent the global genetic diversity of species in the Fg complex and four related species of Fusarium. Phylogenetic analyses demonstrated that polymorphism within these virulence-associated genes is transspecific and appears to have been maintained by balancing selection acting on chemotype differences that originated in the ancestor of this important group of plant pathogens. Chemotype-specific differences in selective constraint and evidence of adaptive evolution within trichothecene genes are also reported.

Multilocus sequence analysis of Fusarium pseudograminearum reveals a single phylogenetic species

“…In the Fg clade, phylogenetic lineages are linked to the geographic origin of isolates (O'Donnell et al 2000;O'Donnell et al 2004;Ward et al 2002), but this is not the case with F. pseudograminearum as seen in the current study. In the tree topology generated from the MLS data set, clades Fps 2 (Australia and USA), Fps 4 (New Zealand and Canada) and Fps 6 (Australia, Canada and South Africa) contained isolates from multiple regions.…”

“…Conversely, the former F. graminearum Group 2 has been subject to in depth study in recent times probably because of its close association with FHB worldwide. Cumulative sequencing and phylogenetic comparison of 11 nuclear genes has demonstrated that F. graminearum (hereafter referred to as the Fg clade) consists of nine distinct lineages (O'Donnell et al 2000;O'Donnell et al 2004;Ward et al 2002), each of which have been proposed for formal species status (O'Donnell et al 2004). The presence of nine phylogenetic species within the Fg clade, begs the question of whether a similar lineage development/speciation has occurred within its close relative, F. pseudograminearum.…”

“…This situation is the reverse of that observed in the closely related, and morphologically similar, Fg clade. In the Fg clade, GCPSR has been used to show congruence in phylogenetic signal over 11 genes (O'Donnell et al 2000;O'Donnell et al 2004;Ward et al 2002), and it has been formally proposed that the Fg clade be redefined into nine phylogenetic species (O'Donnell et al 2004).…”

Unveiling the biosynthetic puzzle of destruxins in Metarhizium species

“…Fusarium spp. express a CYP65 trichothecene C-15 hydroxylase (Tri11, 35% identity with DtxS2) involved in trichothecene biosynthesis (36). The Aspergillus parasiticus CYP65 VerB (33% identity with DtxS2) in the aflatoxin biosynthesis cluster is involved in desaturation of versicolorin B to versicolorin A (37).…”

Genetic and phenotypic diversity within the Fusarium graminearum species complex in Norway

“…Variation in trichothecene chemotypes may have important implications for toxicity (Forsell and Pestka 1985;Luongo et al 2008;Minervini et al 2004). In addition, chemotype differences have been maintained by selection and may have important consequences for pathogen fitness in different environments (Ward et al 2002). In Europe, 15-ADON is observed in South and Central European countries (Boutigny et al 2014;Jennings et al 2004;Talas et al 2011;Toth et al 2005), whereas in northwestern parts of Europe, 3-ADON has dominated (Fredlund et al 2013;Langseth et al 1999;Nielsen et al 2012;Yli-Mattila et al 2009).…”