Submitted to: Fungal Genetics and Biology
Publication Type: Peer reviewed journal
Publication Acceptance Date: 3/8/2004
Publication Date: 4/1/2004
Citation: O Donnell, K., Ward, T.J., Geiser, D.M., Kistler, H.C., Aoki, T. 2004. Genealogical concordance between the mating type locus and seven other nuclear genes support formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genetics and Biology. 41:600-623. Interpretive Summary: The fungal disease of small grain cereals called Fusarium Head Blight (FHB) reached epidemic proportions within the United States during the past decade, resulting in losses close to 3 billion dollars to U.S. farmers due to price discounts and lower yields. FHB-infected grain is often contaminated with toxins and estrogens that pose a serious threat to human and animal health and food safety. FHB is a global problem with recent outbreaks also having occurred in Canada, China, Australia and South America. The present study was conducted to better understand the genetic diversity of the pathogen thought to be responsible for most of the FHB epidemics around the world, Fusarium graminearum. A global collection of this pathogen was typed genetically by collecting and analyzing DNA sequence data from 11 different genes. These analyses demonstrated that the FHB pathogen, F. graminearum, actually comprises nine genetically different species that are morphologically indistinguishable. Because of the importance of these pathogens to world agriculture, the genetic data was used as a basis for giving each species a unique name so as to facilitate communication among plant pathologists, plant breeders and quarantine officials. This same genetic data will be used for molecular diagnostics so that these pathogens can be subjected to active surveillance.
Technical Abstract: Genealogical concordance phylogenetic species recognition (GCPSR) is based on the fact that in the absence of significant gene flow genetic drift will eliminate shared neutral polymorphism over time, so that evolutionary lineages that have reached an advanced state of biological speciation should be recovered as reciprocally monophyletic groups in genealogies derived from orthologous loci. GCPSR was used in this study to examine species limits within the Fusarium graminearum clade (Fg clade) by conducting phylogenetic analyses on DNA sequences of the mating-type (MAT) locus, histone H3, and portions of six previously published nuclear genes. Parsimony analysis of the MAT locus (5930 aligned nucleotide characters), the combined non-MAT sequences (7708 bp), and the combined MAT and non-MAT data set (13,638 aligned bp) resolved the same nine biogeographically structured, phylogenetically distinct species within the morphospecies F. graminearum. In contrast to these nine species which possess a homothallic MAT locus structural organization consisting of contiguous MAT1-1 and MAT1-2 idiomorphs, the four putatively asexual species and the single heterothallic species studied possess a heterothallic MAT locus structural organization in that only one of the two idiomorphs are present within each strain. Comparative molecular evolutionary analyses indicate the evolution of all four MAT genes is dominated by strong purifying selection and show that MAT is functionally constrained, even in species for which a sexual state is unknown. The phylogeny supports a monophyletic and apomorphic origin of homothallism within this clade. Morphological analyses demonstrate that conidial characters are too homoplasious to be used for morphological species recognition. Given their importance to world agriculture, species rank is formally proposed for the eight unnamed cryptic species within the Fg clade using fixed nucleotide characters.