Genomic Characterization of a South American Phytophthora Hybrid Mandates Reassessment of the Geographic Origins of Phytophthora infestans.

Michael D Martin,Andaine Seguin-Orlando,Mikkel Schubert,Jean B Ristaino,Nathan Wales,M Thomas P Gilbert,Filipe G Vieira,Simon Y W Ho

doi:10.1093/molbev/msv241

Abstract

As the oomycete pathogen causing potato late blight disease, Phytophthora infestans triggered the famous 19th-century Irish potato famine and remains the leading cause of global commercial potato crop destruction. But the geographic origin of the genotype that caused this devastating initial outbreak remains disputed, as does the New World center of origin of the species itself. Both Mexico and South America have been proposed, generating considerable controversy. Here, we readdress the pathogen’s origins using a genomic data set encompassing 71 globally sourced modern and historical samples of P. infestans and the hybrid species P. andina, a close relative known only from the Andean highlands. Previous studies have suggested that the nuclear DNA lineage behind the initial outbreaks in Europe in 1845 is now extinct. Analysis of P. andina’s phased haplotypes recovered eight haploid genome sequences, four of which represent a previously unknown basal lineage of P. infestans closely related to the famine-era lineage. Our analyses further reveal that clonal lineages of both P. andina and historical P. infestans diverged earlier than modern Mexican lineages, casting doubt on recent claims of a Mexican center of origin. Finally, we use haplotype phasing to demonstrate that basal branches of the clade comprising Mexican samples are occupied by clonal isolates collected from wild Solanum hosts, suggesting that modern Mexican P. infestans diversified on Solanum tuberosum after a host jump from a wild species and that the origins of P. infestans are more complex than was previously thought.

Highlights

Species in the oomycete genus Phytophthora are important pathogens on many plants in agricultural, forest and aquatic environs, and new species are being described at an accelerating pace (Hansen et al 2012; Guha Roy and Gru€nwald 2015)
P. infestans have previously been assigned to a distinct lineage called HERB-1, which persists in extant isolates of P. infestans from Mexico and Ecuador (Martin et al 2014)
The lineage persists in Ecuadorian isolates of P. andina EC3394 and P13803, both of which originate from S. betaceum hosts

Summary

Introduction

Species in the oomycete genus Phytophthora (plant destroyer) are important pathogens on many plants in agricultural, forest and aquatic environs, and new species are being described at an accelerating pace (Hansen et al 2012; Guha Roy and Gru€nwald 2015). The major locales of diversification of their primary hosts often have been identified, centers of origin of many Phytophthora species are unknown (Hansen et al 2012). Among Phytophthora species, P. infestans is perhaps the most widely known. Its reputation arises both from its destructive potential as a plant pathogen that was once responsible for great human loss, and to a particular ability to inspire scientific controversy, for example, in its early identification as the causal agent of a plant disease, as well as its highly disputed New World origin (Bourke 1991).

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Conclusion