HOW INFECTION SHAPED HISTORY: LESSONS FROM THE IRISH FAMINE.

Human history has been profoundly affected by infection throughout the millennia. In most cases, the impact has been a direct consequence of infection in humans. However, in the 1840s, a plant infection - potato blight, caused by the fungus Phytopthera infestans - showed us how an environmental catastrophe in a vulnerable community can profoundly affect human history. Before the visitation of potato blight, the population of Ireland was the most rapidly growing in Europe in the early 1840s. Yet between 1845 and 1850, Ireland's population fell by over one-third - with 3 million people disappearing from the island - half through death and half through emigration. This directly led to a subsequent diaspora of almost 80 million people, many destined for residence in the Americas. The diaspora carried enormous consequences for the social, economic, and political development of the US. Today, lessons from the Irish famine remain poignant and relevant. Social science maps the dimensions of a disaster dependent on the size of its impact and the relative vulnerability of the society which experiences the disaster. Ireland's vulnerability was in terms of its overall poverty and its dependence on the potato as a subsistence crop. However, a critical factor in the disaster was the political structure in which it occurred - where governance was unwilling and unable to respond to the needs of the population.

Viroids as Companions of a Professional Career.

Since the early 1970s when "virus-like" agents were considered as the cause of two diseases (potato spindle tuber and citrus exocortis), their study and further characterization have been linked to the development and use of molecular biology tools. Sucrose density gradient centrifugation and polyacrylamide gel electrophoresis (PAGE) played a critical role in the pioneering studies of PSTVd and citrus exocortis viroid (CEVd). This was later modified by using other PAGEs (sequential PAGE, return PAGE, two-dimensional PAGE), and/or different staining methods (ethidium bromide, silver nitrate, etc.). Since then, disease-causing agents suspected to be viroids were usually subjected to a number of tests to define their: (i) Molecular nature (RNA or DNA; single stranded or double stranded; circular or linear RNA); (ii) molecular weight; (iii) secondary and tertiary structure. Further biological assays are also essential to establish the relationship of a viroid with plant disease and to fulfill Koch's postulates.

Five Reasons to Consider Phytophthora infestans a Reemerging Pathogen.

Phytophthora infestans has been a named pathogen for well over 150 years and yet it continues to "emerge", with thousands of articles published each year on it and the late blight disease that it causes. This review explores five attributes of this oomycete pathogen that maintain this constant attention. First, the historical tragedy associated with this disease (Irish potato famine) causes many people to be fascinated with the pathogen. Current technology now enables investigators to answer some questions of historical significance. Second, the devastation caused by the pathogen continues to appear in surprising new locations or with surprising new intensity. Third, populations of P. infestans worldwide are in flux, with changes that have major implications to disease management. Fourth, the genomics revolution has enabled investigators to make tremendous progress in terms of understanding the molecular biology (especially the pathogenicity) of P. infestans. Fifth, there remain many compelling unanswered questions.

The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes.

Phytophthora infestans is a destructive plant pathogen best known for causing the disease that triggered the Irish potato famine and remains the most costly potato pathogen to manage worldwide. Identification of P. infestan's elusive center of origin is critical to understanding the mechanisms of repeated global emergence of this pathogen. There are two competing theories, placing the origin in either South America or in central Mexico, both of which are centers of diversity of Solanum host plants. To test these competing hypotheses, we conducted detailed phylogeographic and approximate Bayesian computation analyses, which are suitable approaches to unraveling complex demographic histories. Our analyses used microsatellite markers and sequences of four nuclear genes sampled from populations in the Andes, Mexico, and elsewhere. To infer the ancestral state, we included the closest known relatives Phytophthora phaseoli, Phytophthora mirabilis, and Phytophthora ipomoeae, as well as the interspecific hybrid Phytophthora andina. We did not find support for an Andean origin of P. infestans; rather, the sequence data suggest a Mexican origin. Our findings support the hypothesis that populations found in the Andes are descendants of the Mexican populations and reconcile previous findings of ancestral variation in the Andes. Although centers of origin are well documented as centers of evolution and diversity for numerous crop plants, the number of plant pathogens with a known geographic origin are limited. This work has important implications for our understanding of the coevolution of hosts and pathogens, as well as the harnessing of plant disease resistance to manage late blight.

Persistence of the mitochondrial lineage responsible for the Irish potato famine in extant new world phytophthora infestans.

The plant pathogen Phytophthora infestans emerged in Europe in 1845, triggering the Irish potato famine and massive European potato crop losses that continued until effective fungicides were widely employed in the 20th century. Today the pathogen is ubiquitous, with more aggressive and virulent strains surfacing in recent decades. Recently, complete P. infestans mitogenome sequences from 19th-century herbarium specimens were shown to belong to a unique lineage (HERB-1) predicted to be rare or extinct in modern times. We report 44 additional P. infestans mitogenomes: four from 19th-century Europe, three from 1950s UK, and 37 from modern populations across the New World. We use phylogenetic analyses to identify the HERB-1 lineage in modern populations from both Mexico and South America, and to demonstrate distinct mitochondrial haplotypes were present in 19th-century Europe, with this lineage initially diversifying 75 years before the first reports of potato late blight.

Reconstructing genome evolution in historic samples of the Irish potato famine pathogen.

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.

Spontaneous generation and disease causation: Anton de Bary's experiments with Phytophthora infestans and late blight of potato.

Anton de Bary is best known for his elucidation of the life cycle of Phytopthora infestans, the causal organism of late blight of potato and the crop losses that caused famine in nineteenth-century Europe. But while practitioner histories often claim this accomplishment as a founding moment of modern plant pathology, closer examination of de Bary's experiments and his published work suggest that his primary motiviation for pursing this research was based in developmental biology, not agriculture. De Bary shied away from making any recommendations for agricultural practice, and instead focused nearly exclusively on spontaneous generation and fungal development - both concepts promoted through prize questions posted by the Académie des Sciences in the 1850s and 1860s. De Bary's submission to the Académie's 1859 Alhumbert prize question illustrates his own contributions to debates about spontaneous generation and demonstrates the practical applications of seemingly philosophical questions - such as the origin of life.

Potato agriculture, late blight science, and the molecularization of plant pathology.

By the mid-1980s nucleic-acid based methods were penetrating the farthest reaches of biological science, triggering rivalries among practitioners, altering relationships among subfields, and transforming the research front. This article delivers a "bottom up" analysis of that transformation at work in one important area of biological science, plant pathology, by tracing the "molecularization" of efforts to understand and control one notorious plant disease -- the late blight of potatoes. It mobilizes the research literature of late blight science as a tool through which to trace the changing typography of the research front from 1983 to 2003. During these years molecularization intensified the traditional fragmentation of the late blight research community, even as it dramatically integrated study of the causal organism into broader areas of biology. In these decades the pathogen responsible for late blight, the oomycete "Phytophthora infestans," was discovered to be undergoing massive, frightening, and still largely unexplained genetic diversification -- a circumstance that lends the episode examined here an urgency that reinforces its historiographical significance as a case-study in the molecularization of the biological sciences.

Being at the right place, at the right time, for the right reasons--plant pathology.

This article relates some personal history and influences leading to becoming a plant pathologist. Next a summary of my research experiences on rice and barley diseases and the effect of regulatory changes on efforts to manage rice diseases in California. I conclude with an invitation to consider the opportunities and obligations of plant pathologists to return to the field and for individual introspection regarding attitudes and behavior toward colleagues and factors affecting our profession.

Identity of the mtDNA haplotype(s) of Phytophthora infestans in historical specimens from the Irish potato famine.

The mtDNA haplotypes of the plant pathogen Phytophthora infestans present in dried potato and tomato leaves from herbarium specimens collected during the Irish potato famine and later in the 19th and early 20th century were identified. A 100 bp fragment of ribosomal DNA (rDNA) specific for P. infestans was amplified from 90% of the specimens (n = 186), confirming infection by P. infestans. Primers were designed that distinguish the extant mtDNA haplotypes. 86% percent of the herbarium specimens from historic epidemics were infected with the Ia mtDNA haplotype. Two mid-20th century potato leaves from Ecuador (1967) and Bolivia (1944) were infected with the Ib mtDNA haplotype of the pathogen. Both the Ia and IIb haplotypes were found in specimens collected in Nicaragua in the 1950s. The data suggest that the Ia haplotype of P. infestans was responsible for the historic epidemics during the 19th century in the UK, Europe, and the USA. The Ib mtDNA haplotype of the pathogen was dispersed later in the early 20th century from Bolivia and Ecuador. Multiple haplotypes were present outside Mexico in the 1940s-60s, indicating that pathogen diversity was greater than previously believed.

Tracking historic migrations of the Irish potato famine pathogen, Phytophthora infestans.

The plant pathogen Phytophthora infestans causes late blight, a devastating disease on potato that led to the Irish potato famine during 1845-1847. The disease is considered a reemerging problem and still causes major epidemics on both potato and tomato crops worldwide. Theories on the origin of the disease based on an examination of the genetic diversity and structure of P. infestans populations and use of historic specimens to understand modern day epidemics are discussed.

PCR amplification of the Irish potato famine pathogen from historic specimens.

Late blight, caused by the oomycete plant pathogen Phytophthora infestans, is a devastating disease of potato and was responsible for epidemics that led to the Irish potato famine in 1845 (refs 1,2,3,4,5). Before the 1980s, worldwide populations of P. infestans were dominated by a single clonal lineage, the US-1 genotype or Ib mitochondrial DNA (mtDNA) haplotype, and sexual reproduction was not documented outside Mexico, the centre of diversity of the pathogen. Here we describe the amplification and sequencing of 100-base-pair fragments of DNA from the internal transcribed spacer region 2 from 28 historic herbarium samples including Irish and British samples collected between 1845 and 1847, confirming the identity of the pathogen. We amplified a variable region of mtDNA that is present in modern Ib haplotypes of P. infestans, but absent in the other known modern haplotypes (Ia, IIa and IIb). Lesions in samples tested were not caused by the Ib haplotype of P. infestans, and so theories that assume that the Ib haplotype is the ancestral strain need to be re-evaluated. Our data emphasize the importance of using historic specimens when making inferences about historic populations.

History of therapy of plant viral diseases.

Sixty years of therapy of virus-infected plants have been examined by analyzing the development of therapeutic techniques which have been successful, i.e. thermotherapy, chemotherapy and meristem tip culture. The reasons that gave rise to the practice of combining techniques have also been investigated. The results have only slightly improved our knowledge of virus biology, but have made possible the micropropagation of marketable virus-free germoplasm.