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, 99 (14), 9278-83

Ancestral Polymorphism and Adaptive Evolution in the Trichothecene Mycotoxin Gene Cluster of Phytopathogenic Fusarium

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Ancestral Polymorphism and Adaptive Evolution in the Trichothecene Mycotoxin Gene Cluster of Phytopathogenic Fusarium

Todd J Ward et al. Proc Natl Acad Sci U S A.

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.

Figures

Figure 1
Figure 1
Organization of the trichothecene gene cluster in Fusarium. The genes sequenced include a 15-O-acetyltransferase (TRI3), two P450 oxygenases (TRI4 and TRI11), a transcription factor (TRI6), trichodiene synthase (TRI5), a regulatory gene (TRI10), a trichothecene efflux pump (TRI12), and a predicted protein of unknown function (TRI9) (9, 18).
Figure 2
Figure 2
One of four most parsimonious phylograms (differing only in the position of the Fg4 and Fg3 clades) inferred from a combined analysis of six noncluster genes, and one of three most parsimonious phylograms (differing only in the relationships within Fg2) inferred from a combined analysis of eight TRI-cluster genes. Colored blocks indicate the trichothecene chemotype of each strain, and colored branches reflect parsimony-based reconstructions of trichothecene chemotype evolution. In-group strains are identified by their Agricultural Research Service Culture Collection (NRRL) number followed by an abbreviation in parentheses indicating species: Fg complex (Fg 1–8), F. lunulosporum (lu), F. cerealis (ce), F. culmorum (cu), and F. pseudograminearum (p). F. sporotrichioides is abbreviated as Fs. The frequency (%) with which a given branch was recovered in 2,000 bootstrap replications is shown above all branches recovered in more than 70% of bootstrap replicates.
Figure 3
Figure 3
Strict consensus cladograms derived from maximum parsimony (MP) analyses of individual TRI-cluster genes. Individual analyses of TRI9 were not performed because this gene contained only seven parsimony-informative characters (PIC). Colored blocks indicate the trichothecene chemotype of each strain. Individual strains are labeled as indicated in Fig. 2. The frequency (%) with which a given branch was recovered in 2,000 bootstrap replications is shown above all branches recovered in more than 70% of bootstrap replicates.

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