This guest post is by Detlef Weigel (@WeigelWorld) and Hernán A. Burbano on their arXived paper [with coauthors] Yoshida et al. The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. arXived here and in press at eLife [to appear here].
This paper is the result of a great collaboration between a lab that specializes in ancient DNA (that of Johannes Krause from the University of Tübingen), an expert in pathogen systematics (the group of Marco Thines from the Senckenberg Museum and Goethe University in Frankfurt), two pathogen genomics labs (those of Sophien Kamoun from the Sainsbury Laboratory in Norwich and Frank Martin from the USDA in California), and our evolutionary genomics group at the Max Planck Institute in Tübingen (Hernán A. Burbano and Detlef Weigel).
Phytophthora infestans made history when it destroyed large parts of the European potato crop, beginning in 1845. Potato has its origin in the Andes, in the Southeast of modern Peru and Northwest of Bolivia, while the center of diversity of P. infestans is several thousand kilometers further north, in Mexico’s Toluca Valley. There, other Phytophthora species live on a broad range of host plants. At some point in its history, evolutionary events associated with repeat-driven genome expansion [1,2] endowed P. infestans with the genetic arsenal required to infect potato. The pathogen was introduced to Europe in 1845 via infected potato tuber from the United States, where potato blight had made its first appearance in 1843. In the ensuing European blight epidemic, Ireland was hit especially hard, because the virtual absence of independent farmers and a restrictive customs policy conspired with the disease caused by P. infestans, potato blight, to have disproportionately devastating effects. The Great Famine that struck Ireland was a decisive event in both European and American history. One million Irish died of starvation, and at least another million left the country – most of them to the USA.
This part of P. infestans history has been clear, but the relationship of the strain(s) that caused the nineteenth century epidemic to modern strains has been controversial. Before a range of genetically quite distinct P. infestans strains made their debut throughout the world some 40 years ago, the global population outside Mexico was dominated by a single strain, called US-1. Because of its prevalence, US-1 was long thought to have been the cause of the fatal outbreak in the nineteenth century. From the analysis of a single SNP in the mitochondrial genome, it was, however, concluded in 2001 that the nineteenth century strains were more closely related to the modern strains that prevail today .
In our new paper, we resolve this paradoxical view: While the historical pathogen strain, which we call HERB-1, indeed differs at this one position from US-1, which has a derived allele, HERB-1 is far more closely related to US-1 than to other modern strains. Molecular clock analyses show that both strains probably separated from each other only a few years before the major European outbreak. HERB-1 seems to have dominated the global population without many genetic changes, and only in the twentieth century, after new potato varieties were introduced, was HERB-1 replaced by US-1 as the most successful P. infestans strain. We do not know for sure why HERB-1 was replaced, but we noted that the modern strains tend to be polyploid, while HERB-1 was diploid. We speculate that the increased genetic diversity in polyploid lineages were important for the success of US-1 (and other modern strains).
Our conclusions are based on Illumina sequencing of 11 herbarium samples of infected potato and tomato leaves collected in Ireland, the UK, Continental Europe and North America and preserved in the herbaria of the Botanical State Collection Munich and the Kew Gardens in London. Both herbaria placed a great deal of confidence in our abilities and were very generous in providing the dried plants. The degree of DNA preservation in the herbarium samples was impressive, much higher than in other examples of ancient DNA, and the majority of recovered DNA was from the host plant, with some samples having in addition over 20% pathogen DNA. In contrast to recent studies of historic human pathogens, no target DNA enrichment was required. We compared the historic samples with modern strains from Europe, Africa and North and South America as well as two closely related Phytophthora species. Due to the 150-year long period over which the individual samples had been collected, we were able to estimate with great confidence when the various P. infestans strains had emerged during evolutionary time. Here, too, we found connections with historic events: the first contact between Europeans and Americans in Mexico falls exactly into the time window in which the genetic diversity of P. infestans experienced a remarkable increase. Presumably, the social upheaval following the arrival of the Europeans somehow led to a spread of the pathogen at the beginning of the sixteenth century, which in turn accelerated its evolution.
The historical HERB-1 type is so far not known from modern collections, but we now have many diagnostic markers with which we can type the hundreds of modern isolates to determine whether perhaps there is somewhere a reservoir of HERB-1. In addition, our work highlights that herbaria constitute a rich, so far untapped source for investigating real-time evolution.
Detlef Weigel, firstname.lastname@example.org
Hernán A. Burbano, email@example.com
Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
1. Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393-398.
2. Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D, et al. (2010) Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330: 1540-1543.
3. Ristaino JB, Groves CT, Parra GR (2001) PCR amplification of the Irish potato famine pathogen from historic specimens. Nature 411: 695-697.