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.
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.
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.
As the oomycete pathogen causing potato late blight disease, Phytophthora infestans triggered the famous 19(th)-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 dataset 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 S. tuberosum after a host jump from a wild species and that the origins of P. infestans are more complex than was previously thought.
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.
Nematodes play a key role in soil processes with alterations in the nematode community structure having the potential to considerably influence ecosystem functioning. As a result fluctuations in nematode diversity and/or community structure can be gauged as a ‘barometer’ of a soil’s functional biodiversity. However, a deficit exists in regards to baseline knowledge and on the impact of specific GM crops on soil nematode populations and in particular in regard to the impact of GM potatoes on the diversity of nematode populations in the rhizosphere. The goal of this project was to begin to address this knowledge gap in regards to a GM potato line, cisgenically engineered for resistance to Phytophthora infestans (responsible organism of the Irish potato famine causing late blight disease). For this, a 3 year (2013, 2014, 2015) field experimental study was completed, containing two conventional genotypes (cvs. Desiree and Sarpo Mira) and a cisgenic genotype (cv. Desiree + Rpi-vnt1). Each potato genotype was treated with different disease management strategies (weekly chemical applications and corresponding no spray control). Hence affording the opportunity to investigate the temporal impact of potato genotype, disease management strategy (and their interaction) on the potato rhizosphere nematode community.
Various wild species germplasm has been used in European potato breeding since the first introduction of potato (Solanum tuberosum L.) to Europe. As the plant cytoplasmic genome including chloroplast and mitochondrial genomes is transmitted only through the maternal parent, cytoplasmic markers are useful tools in breeding programs to determine cytoplasmic genome types and to trace maternal ancestors. The potato cytoplasmic genome can be distinguished into six distinct types (M, P, A, W, T, and D). Male sterility was found in genotypes with S. demissum-derived D-type cytoplasm and S. stoloniferum-derived W/γ-type cytoplasm. These wild species were frequently used to incorporate superior pathogen resistance genes. As a result, the percentage of these two types is increasing unintentionally in the European germplasm pool. Other than cytoplasmic male sterility, little is known about effects of the cytoplasmic genome on complex agronomic traits in potato.
Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), is a serious global pest of potato, Solanum tuberosum L. Management of L. decemlineata has relied heavily on insecticides, but repeated evolution of insecticide resistance has motivated the exploration and development of alternative strategies, such as plant resistance. The recent development of two diploid potato families derived from crosses between cultivated and wild potato species (S. chacoense and S. berthaultii) has provided a unique opportunity to reexamine plant traits for resistance breeding. In this 2-yr study, we surveyed select F2 clones for the induction of L. decemlineata mortality and a reduction in defoliation in no-choice feeding assays when challenged with adults and larvae from three sites in Wisconsin. We tested for an association with glandular trichome density and foliar levels of the glycoalkaloids chaconine and solanine. Several potato clones demonstrated resistance in specific feeding assays, but none excelled consistently across experiments. Mortality and defoliation generally differed significantly among L. decemlineata populations, which could be indicative of heritable variation in beetle responses to plant defenses or variation in the physiological status of the beetle populations tested. Contrary to expectations, higher trichome density increased mortality or decreased defoliation in only a few cases, and levels of mortality and defoliation were unrelated to foliar glycoalkaloid content, warranting further investigation of the defense mechanisms of resistant clones. In addition to identifying several potential L. decemlineata resistance sources, this study underscores the need to include multiple insect populations in surveys of plant resistance to this diverse pest.
The potato cyst nematode (PCN), Globodera pallida, is a globally regulated and quarantine potato pest. It was detected for the first time in the U.S. in the state of Idaho in 2006. A spatial analysis was performed to: (i) understand the spatial arrangement of PCN infested fields in southern Idaho using spatial point pattern analysis; and (ii) evaluate the potential threat of PCN for entry to new areas using spatial interpolation techniques. Data point locations, cyst numbers and egg viability values for each infested field were collected by USDA-APHIS during 2006-2014. Results showed the presence of spatially clustered PCN infested fields (P = 0.003). We determined that the spread of PCN grew in diameter from the original center of infestation toward the southwest as an ellipsoidal-shaped cluster. Based on the aggregated spatial pattern of distribution and the low extent level of PCN infested fields in southern Idaho, we determined that PCN spread followed a contagion effect scenario, where nearby infested fields contributed to the infestation of new fields, probably through soil contaminated agricultural equipment or tubers. We determined that the recent PCN presence in southern Idaho is unlikely to be associated with new PCN entry from outside the state of Idaho. The relative aggregation of PCN infested fields, the low number of cysts recovered, and the low values in egg viability facilitate quarantine activities and confine this pest to a small area, which, in 2017, is estimated to be 1,233 hectares. The tools and methods provided in this study should facilitate comprehensive approaches to improve PCN control and eradication programs as well as to raise public awareness about this economically important potato pest.
Resistance genes (R-genes) from wild potato species confer protection against disease and can be introduced into cultivated potato varieties using breeding or biotechnology. The R-gene, Rpi-vnt1, which encodes the VNT1 protein, protects against late blight, caused by Phytophthora infestans. Heterologous expression and purification of active VNT1 in quantities sufficient for regulatory biosafety studies was problematic, making it impractical to generate hazard characterization data. As a case study for R-proteins, a weight-of-evidence, tiered approach was used to evaluate the safety of VNT1. The hazard potential of VNT1 was identified from relevant safety information including history of safe use, bioinformatics, mode of action, expression levels, and dietary intake. From the assessment it was concluded that Tier II hazard characterization was not needed. R-proteins homologous to VNT1 and identified in edible crops, have a history of safe consumption. VNT1 does not share sequence identity with known allergens. Expression levels of R-proteins are generally low, and VNT1 was not detected in potato varieties expressing the Rpi-vnt1 gene. With minimal hazard and negligible exposure, the risks associated with consumption of R-proteins in late blight protected potatoes are exceedingly low. R-proteins introduced into potatoes to confer late blight protection are safe for consumption.