An Andean origin of Phytophthora infestans inferred from mitochondrial and nuclear gene genealogies

Abstract

Phytophthora infestans (Mont.) de Bary caused the 19th century Irish Potato Famine. We assessed the genealogical history of P. infestans using sequences from portions of two nuclear genes (␤-tubulin and Ras) and several mitochondrial loci P3, (rpl14, rpl5, tRNA) and P4 (Cox1) from 94 isolates from South, Central, and North America, as well as Ireland. Summary statistics, migration analyses and the genealogy of current populations of P. infestans for both nuclear and mitochondrial loci are consistent with an ''out of South America'' origin for P. infestans. Mexican populations of P. infestans from the putative center of origin in Toluca Mexico harbored less nucleotide and haplotype diversity than Andean populations. Coalescent-based genealogies of all loci were congruent and demonstrate the existence of two lineages leading to present day haplotypes of P. infestans on potatoes. The oldest lineage associated with isolates from the section Anarrhichomenun including Solanum tetrapetalum from Ecuador was identified as Phytophthora andina and evolved from a common ancestor of P. infestans. Nuclear and mitochondrial haplotypes found in Toluca Mexico were derived from only one of the two lineages, whereas haplotypes from Andean populations in Peru and Ecuador were derived from both lineages. Haplotypes found in populations from the U.S. and Ireland was derived from both ancestral lineages that occur in South America suggesting a common ancestry among these populations. The geographic distribution of mutations on the rooted gene genealogies demonstrate that the oldest mutations in P. infestans originated in South America and are consistent with a South American origin.late blight ͉ oomycetes ͉ phylogeography ͉ Solanum tuberosum ͉ stamenopiles

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

“…A competing hypothesis argues that the center of origin of the potato, the South American Andes, is the center of origin of P. infestans (5). This hypothesis recently gained prominence after an analysis demonstrated ancestral variation in Andean lineages of P. infestans (5). Other evidence supporting this hypothesis includes infection of native Solanum hosts and an Andean distribution for Phytophthora andina, a phylogenetic relative of P. infestans (6).…”

“…To determine ancestral state, we added sequences from the sister taxa P. andina, P. mirabilis, P. ipomoeae, and Phytophthora phaseoli, all of which belong to Phytophthora clade 1c (30,31). Finally, we aimed to reconcile the biology of P. infestans in Mexico with the findings of Gómez-Alpizar et al (5) Table S1). We found 30 multilocus simple sequence repeat (SSR) genotypes in the Andes sample and 43 in the Mexico sample.…”

“…Support for the alternate hypothesis that P. infestans originated in the Andes is based on a coalescent analysis conducted by Gómez-Alpizar et al (5). This analysis used the nuclear RAS locus and the mitochondrial P3 and P4 regions to infer rooted gene genealogies that showed ancestral lineages rooted in the Andes.…”

“…In the 1980s, a single asexual lineage named US-1, possibly derived from the same metapopulation as HERB-1 (1), dominated global populations, whereas a genetically diverse and sexual population of P. infestans in central Mexico led to formulation of the hypothesis identifying Mexico as this pathogen's center of origin (3,4). A competing hypothesis argues that the center of origin of the potato, the South American Andes, is the center of origin of P. infestans (5). This hypothesis recently gained prominence after an analysis demonstrated ancestral variation in Andean lineages of P. infestans (5).…”

Fifty years of oomycetes—from consolidation to evolutionary and genomic exploration

“…Until the 1980's, only a single clonal lineage of the A1 mating type was present outside Mexico or the Andes (Goodwin et al 1994), the centre of origin being still debated (Grunwald and Flier 2005;Gomez-Alpizar et al 2007), and after that the A2 mating type was introduced to both Europe and North America. This caused P. infestans to re-emerge as a very serious threat to potato cultivation by increasing its aggressiveness towards the host, reducing fungicide efficacy, facilitating its survival in soil or debris and broadening its host range to include tomato Fry and Goodwin 1997;Gavino et al 2000;Lee et al 1999).…”