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Title: The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes

Author
item GOSS, ERICA - University Of Florida
item TABIMA, JAVIER - Oregon State University
item COOKE, DAVID - The James Hutton Institute
item RESTREPO, SILVIA - Universidad De Los Andes
item FRY, WILLIAM - Cornell University
item FORBES, GREGORY - International Potato Center
item FIELAND, VALERIE - Oregon State University
item CARDENAS, MARTHA - Universidad De Los Andes
item MYERS, KEVIN - Cornell University
item Grunwald, Niklaus - Nik

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/6/2014
Publication Date: 6/17/2014
Citation: Goss, E.M., Tabima, J.F., Cooke, D., Restrepo, S., Fry, W.E., Forbes, G.A., Fieland, V.J., Cardenas, M., Myers, K.L., Grunwald, N.J. 2014. The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. Proceedings of the National Academy of Sciences. 111(24):8791-8796.

Interpretive Summary: The potato late blight pathogen was introduced to Europe in the 1840s and caused devastating loss of a staple crop, resulting in the Irish potato famine and subsequent diaspora. Research on this disease has engendered much debate, which, in recent years, has focused on whether the geographic origin of the pathogen is South America or central Mexico. Different lines of evidence support each hypothesis. We sequenced four nuclear genes in representative samples from Mexico and the South American Andes. Our analysis provides strong support for a center of origin in Mexico and reconciles previous findings of ancestry in the Andes. This is a rare example of a pathogen with a known origin that is secondary to its current major host.

Technical Abstract: Phytophthora infestans is a destructive plant pathogen best known for causing the disease that triggered the Irish potato famine and continues to be the most costly potato pathogen to manage worldwide. Identification of its elusive center of origin is critical to understanding the mechanisms of repeated global emergence of this pathogen. There are two competing theories placing the origin in either South America or in central Mexico. Both regions are centers of diversity of Solanum host plants. To test these competing hypotheses, we conducted detailed phylogeographic and approximate Bayesian computation analyses, which are approaches suitable to unraveling complex demographic histories. The analyses used microsatellite marker and sequences of four nuclear genes sampled from populations in the Andes, Mexico, and elsewhere. To infer the ancestral state, we newly included the closest known relatives P. phaseoli, P. mirabilis, P. ipomoeae, as well as the interspecific hybrid P. andina. We obtained decisive support for a central Mexican origin of P. infestans that is congruent with its natural history. Our findings support the hypothesis that populations found in the Andes are descendants of the Mexican populations and reconcile previous findings of ancestral variation in the Andes. While centers of origin are well documented as centers of evolution and diversity for numerous crop plants, P. infestans is a rare example of a plant pathogen with a known geographic origin. This work has important implications for our understanding of the coevolution of hosts and pathogens, and harnessing of plant disease resistance to manage late blight.