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

Abstract

Phytophthora infestans is a destructive plant pathogen best known for causing the disease that triggered the Irish potato famine and remains the most costly potato pathogen to manage worldwide. Identification of P. infestan's 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 of which are centers of diversity of Solanum host plants. To test these competing hypotheses, we conducted detailed phylogeographic and approximate Bayesian computation analyses, which are suitable approaches to unraveling complex demographic histories. Our analyses used microsatellite markers and sequences of four nuclear genes sampled from populations in the Andes, Mexico, and elsewhere. To infer the ancestral state, we included the closest known relatives Phytophthora phaseoli, Phytophthora mirabilis, and Phytophthora ipomoeae, as well as the interspecific hybrid Phytophthora andina. We did not find support for an Andean origin of P. infestans; rather, the sequence data suggest a Mexican origin. 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. Although centers of origin are well documented as centers of evolution and diversity for numerous crop plants, the number of plant pathogens with a known geographic origin are limited. This work has important implications for our understanding of the coevolution of hosts and pathogens, as well as the harnessing of plant disease resistance to manage late blight.biological invasion | coalescent analysis | oomycete | population genetics | stramenopile

Best Practices for Population Genetic Analyses

“…Observing sexual reproductive structures in nature will provide an expectation that the organism is sexual (Goss et al 2014;Milgroom 1996;Peever et al 2004). However, populations exhibiting a mixed mating system (e.g., involving both outcrossing and selfing) may purge the variation needed to infer a sexual mode of reproduction through inbreeding, resulting in a situation where it becomes difficult to detect if sexual reproduction occurs.…”

“…For example, a recent study included all Phytophthora clade 1c taxa to infer the origin and evolutionary history of the Irish famine pathogen Phytophthora infestans (Goss et al 2014). In the absence of a close relative the ancestral state of any locus cannot be inferred.…”

“…n loci were randomly sampled 1,000 times in order to create the distribution using poppr in R with simple sequence repeats data for populations of the potato late blight pathogen Phytophthora infestans (Goss et al 2014;Grünwald et al 2016a;Kamvar et al 2015a). …”

“…For many reasons, population genetics is a tremendously useful discipline with a long history of application to plant pathology. For example, one can establish where the likely center of origin of a plant pathogen is located, which in turn allows harnessing of plant resistance genes (Goss et al 2014;Grünwald and Flier 2005;Stukenbrock et al 2007;Vleeshouwers and Oliver 2014;Vleeshouwers et al 2011). Plant pathogens continue to emerge and reemerge and population genetic analyses can be used to infer genetic patterns (subdivision, bottlenecks, clonality, etc.…”

“…Yet other pathogens have been shown to emerge via hybridization or speciation (Geiser et al 1998;Giraud et al 2010;Goss et al 2011;Stukenbrock et al 2007). Population genetics can also be useful to provide inferences on the degree of sexual outcrossing by studying linkage among markers (Atallah et al 2010;Goss et al 2014;Milgroom 1996;Milgroom et al 2014). …”