Reconstructing genome evolution in historic samples of the Irish potato famine pathogen.
ABSTRACT: Responsible for the Irish potato famine of 1845-49, the oomycete pathogen Phytophthora infestans caused persistent, devastating outbreaks of potato late blight across Europe in the 19th century. Despite continued interest in the history and spread of the pathogen, the genome of the famine-era strain remains entirely unknown. Here we characterize temporal genomic changes in introduced P. infestans. We shotgun sequence five 19th-century European strains from archival herbarium samples--including the oldest known European specimen, collected in 1845 from the first reported source of introduction. We then compare their genomes to those of extant isolates. We report multiple distinct genotypes in historical Europe and a suite of infection-related genes different from modern strains. At virulence-related loci, several now-ubiquitous genotypes were absent from the historical gene pool. At least one of these genotypes encodes a virulent phenotype in modern strains, which helps explain the 20th century's episodic replacements of European P. infestans lineages.
Project description: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.
Project description:Phytophthora infestans, the cause of potato late blight, is infamous for having triggered the Irish Great Famine in the 1840s. Until the late 1970s, P. infestans diversity outside of its Mexican center of origin was low, and one scenario held that a single strain, US-1, had dominated the global population for 150 years; this was later challenged based on DNA analysis of historical herbarium specimens. We have compared the genomes of 11 herbarium and 15 modern strains. We conclude that the 19th century epidemic was caused by a unique genotype, HERB-1, that persisted for over 50 years. HERB-1 is distinct from all examined modern strains, but it is a close relative of US-1, which replaced it outside of Mexico in the 20th century. We propose that HERB-1 and US-1 emerged from a metapopulation that was established in the early 1800s outside of the species' center of diversity. DOI:http://dx.doi.org/10.7554/eLife.00731.001.
Project description:Phytophthora infestans (Mont.) de Bary, the causal agent of potato late blight, was responsible for the Irish potato famine of the 1840s. Initial disease outbreaks occurred in the US in 1843, two years prior to European outbreaks. We examined the evolutionary relationships and source of the 19th-century outbreaks using herbarium specimens of P. infestans from historic (1846-1970) and more recent isolates (1992-2014) of the pathogen. The same unique SSR multilocus genotype, named here as FAM-1, caused widespread outbreaks in both US and Europe. The FAM-1 lineage shared allelic diversity and grouped with the oldest specimens collected in Colombia and Central America. The FAM-1 lineage of P. infestans formed a genetic group that was distinct from more recent aggressive lineages found in the US. The US-1 lineage formed a second, mid-20th century group. Recent modern US lineages and the oldest Mexican lineages formed a genetic group with recent Mexican lineages, suggesting a Mexican origin of recent US lineages. A survey of mitochondrial haplotypes in a larger set of global herbarium specimens documented the more frequent occurrence of the HERB-1 (type Ia) mitochondrial haplotype in archival collections from 1866-75 and 1906-1915 and the rise of the Ib mitochondrial lineage (US-1) between 1946-1955. The FAM-1 SSR lineage survived for almost 100 years in the US, was geographically widespread, and was displaced first in the mid-20th century by the US-1 lineage and then by distinct new aggressive lineages that migrated from Mexico.
Project description:Phytophthora infestans, the causal agent of potato late blight, triggered the devastating Great Irish Famine that lasted from 1845 to 1852. Today, it is still the greatest threat to the potato yield. Ethylicin is a broad-spectrum biomimetic-fungicide. However, its application in the control of Phytophthora infestans is still unknown. In this study, we investigated the effects of ethylicin on Phytophthora infestans. We found that ethylicin inhibited the mycelial growth, sporulation capacity, spore germination and virulence of Phytophthora infestans. Furthermore, the integrated analysis of proteomics and metabolomics indicates that ethylicin may inhibit peptide or protein biosynthesis by suppressing both the ribosomal function and amino acid metabolism, causing an inhibitory effect on Phytophthora infestans. These observations indicate that ethylicin may be an anti-oomycete agent that can be used to control Phytophthora infestans.
Project description:Phytophthora infestans (P. infestans) is the causal agent of potato late blight, which caused the devastating Irish Potato Famine during 1845-1852. Until now, potato late blight is still the most serious threat to potato growth and has caused significant economic losses worldwide. Melatonin can induce plant innate immunity against pathogen infection, but the direct effects of melatonin on plant pathogens are poorly understood. In this study, we investigated the direct effects of melatonin on P. infestans. Exogenous melatonin significantly attenuated the potato late blight by inhibiting mycelial growth, changing cell ultrastructure, and reducing stress tolerance of P. infestans. Notably, synergistic anti-fungal effects of melatonin with fungicides on P. infestans suggest that melatonin could reduce the dose levels and enhance the efficacy of fungicide against potato late blight. A transcriptome analysis was carried out to mine downstream genes whose expression levels were affected by melatonin. The analysis of the transcriptome suggests that 66 differentially expressed genes involved in amino acid metabolic processes were significantly affected by melatonin. Moreover, the differentially expressed genes associated with stress tolerance, fungicide resistance, and virulence were also affected. These findings contribute to a new understanding of the direct functions of the melatonin on P. infestans and provide a potential ecofriendly biocontrol approach using a melatonin-based paradigm and application to prevent potato late blight.
Project description:Potato virus Y (PVY) causes disease in potatoes and other solanaceous crops. The appearance of its necrogenic strains in the 1980s made it the most economically important virus of potatoes. We report the isolation and genomic sequences of 32 Peruvian isolates of PVY which, together with 428 published PVY genomic sequences, gave an alignment of 460 sequences. Of these 190 (41%) were non-recombinant, and 162 of these provided a dated phylogeny, that corresponds well with the likely history of PVY, and show that PVY originated in South America which is where potatoes were first domesticated. The most basal divergences of the PVY population produced the N and C: O phylogroups; the origin of the N phylogroup is clearly Andean, but that of the O and C phylogroups is unknown, although they may have been first to establish in European crops. The current PVY population originated around 156 CE. PVY was probably first taken from South America to Europe in the 16th century in tubers. Most of the present PVY diversity emerged in the second half of the 19th century, after the Phytophthora infestans epidemics of the mid-19th century destroyed the European crop and stimulated potato breeding. Imported breeding lines were shared, and there was no quarantine. The early O population was joined later by N phylogroup isolates and their recombinants generated the R1 and R2 populations of damaging necrogenic strains. Our dating study has confirmed that human activity has dominated the phylodynamics of PVY for the last two millennia.
Project description:The application of DNA sequencing technology to the study of ancient DNA has enabled the reconstruction of past epidemics from genomes of historically important plant-associated microbes. Recently, the genome sequences of the potato late blight pathogen Phytophthora infestans were analyzed from 19th century herbarium specimens. These herbarium samples originated from infected potatoes collected during and after the Irish potato famine. Herbaria have therefore great potential to help elucidate past epidemics of crops, date the emergence of pathogens, and inform about past pathogen population dynamics. DNA preservation in herbarium samples was unexpectedly good, raising the possibility of a whole new research area in plant and microbial genomics. However, the recovered DNA can be extremely fragmented resulting in specific challenges in reconstructing genome sequences. Here we review some of the challenges in computational analyses of ancient DNA from herbarium samples. We also applied the recently developed linkage method to haplotype reconstruction of diploid or polyploid genomes from fragmented ancient DNA.
Project description:Food and diet were class markers in nineteenth-century Ireland, which became evident as nearly one million people, primarily the poor and destitute, died as a consequence of the notorious Great Famine of 1845–1852. Famine took hold after a blight (Phytophthora infestans) destroyed the only means of subsistence—the potato crop—for a significant proportion of the population. This study seeks to elucidate the variability of diet in mid-nineteenth-century Ireland through microparticle and proteomic analysis of human dental calculus samples (n = 42) from victims of the Famine. The sample derives from remains of people who died between August 1847 and March 1851 while receiving poor relief as inmates in the union workhouse in the city of Kilkenny (52°39’N, -7°15’W). The results corroborate the historical accounts of food provisions before and during the Famine, with evidence of corn (maize), potato and cereal starch granules from the microparticle analysis and milk proteins from the proteomic analysis. Unexpectedly, there is also evidence of egg proteins—a food source generally reserved only for export and the better-off social classes—which highlights the variability of the Famine experience for those who died. Through historical contextualisation, this study shows how the notoriously monotonous potato diet of the nineteenth-century Irish poor was supplemented by other foodstuffs on an opportunistic basis. While the Great Irish Famine was one of the worst subsistence crises in history, it was foremost a social disaster induced by the lack of access to food and not the lack of food availability.
Project description: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 (beta-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.
Project description:Pest and pathogen losses jeopardise global food security and ever since the 19(th) century Irish famine, potato late blight has exemplified this threat. The causal oomycete pathogen, Phytophthora infestans, undergoes major population shifts in agricultural systems via the successive emergence and migration of asexual lineages. The phenotypic and genotypic bases of these selective sweeps are largely unknown but management strategies need to adapt to reflect the changing pathogen population. Here, we used molecular markers to document the emergence of a lineage, termed 13_A2, in the European P. infestans population, and its rapid displacement of other lineages to exceed 75% of the pathogen population across Great Britain in less than three years. We show that isolates of the 13_A2 lineage are among the most aggressive on cultivated potatoes, outcompete other aggressive lineages in the field, and overcome previously effective forms of plant host resistance. Genome analyses of a 13_A2 isolate revealed extensive genetic and expression polymorphisms particularly in effector genes. Copy number variations, gene gains and losses, amino-acid replacements and changes in expression patterns of disease effector genes within the 13_A2 isolate likely contribute to enhanced virulence and aggressiveness to drive this population displacement. Importantly, 13_A2 isolates carry intact and in planta induced Avrblb1, Avrblb2 and Avrvnt1 effector genes that trigger resistance in potato lines carrying the corresponding R immune receptor genes Rpi-blb1, Rpi-blb2, and Rpi-vnt1.1. These findings point towards a strategy for deploying genetic resistance to mitigate the impact of the 13_A2 lineage and illustrate how pathogen population monitoring, combined with genome analysis, informs the management of devastating disease epidemics.