Population structure and migration of the Tobacco Blue Mold Pathogen, Peronospora tabacina, into North America and Europe

Tobacco blue mold, caused by Peronospora tabacina, is an oomycete plant pathogen that causes yearly epidemics in tobacco (Nicotiana tabacum) in the United States and Europe. The genetic structure of P. tabacina was examined to understand genetic diversity, population structure and patterns of migration. Two nuclear loci, Igs2 and Ypt1, and one mitochondrial locus, cox2, were amplified, cloned and sequenced from fifty-four isolates of P. tabacina from the United States, Central America-Caribbean-Mexico (CCAM), Europe and the Middle East (EULE). Cloned sequences from the three genes showed high genetic variability across all populations. Nucleotide diversity and the population mean mutation parameter per site (Watterson's theta) were higher in EULE and CCAM and lower in U.S. populations. Neutrality tests were significant and the equilibrium model of neutral evolution was rejected, indicating an excess of recent mutations or rare alleles. Hudson's S-nn tests were performed to examine population subdivision and gene flow among populations. An isolation-with-migration analysis (IM) supported the hypothesis of long-distance migration of P. tabacina from the Caribbean region, Florida and Texas into other states in the United States. Within the European populations, the model documented migration from North Central Europe into western Europe and Lebanon, and migration from western Europe into Lebanon. The migration patterns observed support historical observations about the first disease introductions and movement in Europe. The models developed are applicable to other aerial dispersed emerging pathogens and document that high-evolutionary-risk plant pathogens can move over long distances to cause disease due to their large effective population size, population expansion and dispersal.