Mating system and speciation of the citrus brown spot pathogen, Alternaria alternata

Jane E. Stewart

High levels of genotypic diversity have been found in several putatively asexual fungi, including as many as 15,000 phytopathogenic fungi. How this level of diversity has arisen and is maintained in putatively asexual species is not well understood, and raises questions about the reproductive mode, mechanisms of recombination, and speciation in asexual fungi. The majority of Alternaria species are considered exclusively asexual in their reproductive mode, however, high levels of genotypic diversity found in some populations suggests that meiotic or mitotic recombination mechanisms may be common. Understanding the molecular evolution of mating type genes, their ability to recombine, evolutionary history, and potential speciation of a plant-pathogenic fungus may allow insight into processes of adaptation to new hosts or environments and the evolution of virulence. The objective of this study was to infer the molecular evolution of the mating type genes (MAT1) in Alternaria species using nucleotide diversity, nonsynonymous vs. synonymous substitution (dn/ds) ratios and codon usage statistics, to critically examine the mating system of the citrus brown spot pathogen, A. alternata, using sequence data from physically unlinked loci for linkage disequilibrium and recombination analyses, and to use the coalescent to study the evolutionary histories and estimate species boundaries of a worldwide population of the citrus brown spot pathogen. Codon-site models demonstrated that MAT1 is under purifying selection and significant differences in codon usage were observed between the two mating idiomorphs, MAT1-1-1 and MAT1-2-1. Using gametic disequilibrium tests to examine the mating system strongly supported a clonal reproductive system of A. alternata. However, signatures of recombination events were evident and could be localized to isolates of opposite mating type in three populations. Using a sample representing the worldwide diversity of citrus brown spot pathogen, A. alternata, a complex evolutionary history with signals of lineage sorting and recombination was observed. One lineage, citrus 2, was diverged from the remaining three lineages with strong phylogenetic support in all loci. Divergence of the citrus 2 lineage from the others was estimated between 1- 12 my before present, predating the migration of citrus from SE Asia. Two species were identified using concatenation and GCPSR, but only a single species was detected using BEST and MDC.

Mating system and speciation of the citrus brown spot pathogen, Alternaria alternata

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