Abstract

The plant pathogen that caused the Irish potato famine, Phytophthora infestans, continues to reemerge globally. These modern epidemics are caused by clonally reproducing lineages. In contrast, a sexual mode of reproduction is observed at its center of origin in Mexico. We conducted a comparative genomic analysis of 47 high-coverage genomes to infer changes in genic copy number. We included samples from sexual populations at the center of origin as well as several dominant clonal lineages sampled worldwide. We conclude that sexual populations at the center of origin are diploid, as was the lineage that caused the famine, while modern clonal lineages showed increased copy number (3×). Copy number variation (CNV) was found genome-wide and did not to adhere to the two-speed genome hypothesis. Although previously reported, tetraploidy was not found in any of the genomes evaluated. We propose a model of dominant clone emergence supported by the epidemiological record (e.g., EU_13_A2, US-11, US-23) whereby a higher copy number provides fitness, leading to replacement of prior clonal lineages.IMPORTANCE The plant pathogen implicated in the Irish potato famine, Phytophthora infestans, continues to reemerge globally. Understanding changes in the genome during emergence can provide insights useful for managing this pathogen. Previous work has relied on studying individuals from the United States, South America, Europe, and China reporting that these can occur as diploids, triploids, or tetraploids and are clonal. We studied variation in sexual populations at the pathogen's center of origin, in Mexico, where it has been reported to reproduce sexually as well as within clonally reproducing, dominant clones from the United States and Europe. Our results newly show that sexual populations at the center of origin are diploid, whereas populations elsewhere are more variable and show genome-wide variation in gene copy number. We propose a model of evolution whereby new pathogen clones emerge predominantly by increasing the gene copy number genome-wide.

Highlights

  • The plant pathogen that caused the Irish potato famine, Phytophthora infestans, continues to reemerge globally

  • Our findings provide a new perspective on how plasticity in ploidy, copy number, and presence/absence polymorphisms contribute to the emergence of the Irish potato famine pathogen and other Phytophthora pathogens

  • We explored if the variation in ploidy apparent in P. infestans is observed in other heterothallic Phytophthora taxa

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Summary

Introduction

The plant pathogen that caused the Irish potato famine, Phytophthora infestans, continues to reemerge globally These modern epidemics are caused by clonally reproducing lineages. The Irish famine pathogen, Phytophthora infestans (Mont.) de Bary, notorious for destroying the potato crop in Ireland in the 19th century, continues to reemerge globally as one of the world’s costliest plant pathogens [1] This pathogen causes late blight on potato worldwide and is considered the most economically important pathogen of this crop. The global population structure of P. infestans is characterized as having a sexually reproducing population in Mexico as well as reemerging clonal epidemics in the United States and most of the rest of the world (except northern Europe), consisting of distinct clonal lineages that displace older clonal lineages

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