Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab

Abstract

During the past decade, the plant disease called scab or Fusarium head blight of wheat and barley has reached epidemic proportions in North America and elsewhere in the world. Scab is an economically devastating plant disease, not only because it causes significant reduction in seed yields and quality, but also because infested seeds are often contaminated with trichothecene and estrogenic mycotoxins that pose a serious threat to animal health and food safety. To test whether the primary etiological agent of scab, the fungus Fusarium graminearum, is panmictic throughout its range, allelic genealogies were constructed from six single-copy nuclear genes from strains selected to represent the global genetic diversity of this pathogen. Excluding one hybrid strain, all six genealogies recovered the same seven biogeographically structured lineages, suggesting that they represent phylogenetically distinct species among which gene flow has been very limited during their evolutionary history. Parsimony analysis of the combined data set comprising 7,120 aligned nucleotide characters resolved most relationships among the seven lineages of the F. graminearum clade and related fusaria included in the study. Phylogenetic evidence is also presented for introgressive hybridization and intragenic recombination among lineages of the F. graminearum clade in nature.

Figure 1

One maximum parsimony phylogram from each of the six genes sequenced. CI, consistency index; RI, retention index; RC, rescaled consistency index. Numbers by nodes represent bootstrap support ≥50% from 1,000 replications. The seven biogeographically structured lineages of the F. graminearum clade are color-coded by origin as shown in Fig. 3. The arrow on each phylogram indicates the position of the hybrid strain 28721, which is resolved cladistically within either Asian (yellow code) or African (blue code) lineages. The 3-O-acetyltransferase (i.e., TRI101) allele of 28721 is an Asian–African hybrid (see Fig. 2).

Figure 2

Evidence for intragenic recombination within TRI101 in strain 28721. Phylogenetically informative sites are shown within the three adjacent genes and are color-coded according to the legend in Fig. 3. Based on DNA sequence analysis, the recombination breakpoint maps between nucleotide positions 703 and 1,092 (22).

Figure 3

One of eight most-parsimonious phylograms inferred from the combined data set for the seven color-coded lineages (numbered 1–7) of the F. graminearum clade (supported by bold node) and related B trichothecene-producing fusaria. The color-coded key indicates putative geographic origin of the seven lineages as defined in Table 1. Sequences of F. pseudograminearum, formerly known as F. graminearum Group 1 (18), were used to root the tree by the outgroup method. Decay indices are indicated below nodes; bootstrap intervals from 1,000 replicates are indicated above nodes. Numbers in parentheses above four nodes represent bootstrap support after excluding the hybrid strain 28721.