First historical genome of a crop bacterial pathogen from herbarium specimen: Insights into citrus canker emergence.

Over the past decade, ancient genomics has been used in the study of various pathogens. In this context, herbarium specimens provide a precious source of dated and preserved DNA material, enabling a better understanding of plant disease emergences and pathogen evolutionary history. We report here the first historical genome of a crop bacterial pathogen, Xanthomonas citri pv. citri (Xci), obtained from an infected herbarium specimen dating back to 1937. Comparing the 1937 genome within a large set of modern genomes, we reconstructed their phylogenetic relationships and estimated evolutionary parameters using Bayesian tip-calibration inferences. The arrival of Xci in the South West Indian Ocean islands was dated to the 19th century, probably linked to human migrations following slavery abolishment. We also assessed the metagenomic community of the herbarium specimen, showed its authenticity using DNA damage patterns, and investigated its genomic features including functional SNPs and gene content, with a focus on virulence factors.

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.

On Social and Political Effects of Plant Pest and Disease Epidemics.

Selected historical pest and disease outbreaks in the Old World are discussed in view of their social and political consequences. Large-scale epidemics always caused social unrest, and often hunger, pestilence, and death. When coming on top of deeply rooted and widely spread social unrest such epidemics contributed to political change. Examples are the revolts following epidemics in 1789 and 1846. Epidemics, regardless of causal and target organisms, have elements in common. The notion of a common concept grew into a firmly established discipline: epidemiology.

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.

Biology and management of sugarcane yellow leaf virus: an historical overview.

Sugarcane yellow leaf virus (SCYLV) is one of the most widespread viruses causing disease in sugarcane worldwide. The virus has been responsible for drastic economic losses in most sugarcane-growing regions and remains a major concern for sugarcane breeders. Infection with SCYLV results in intense yellowing of the midrib, which extends to the leaf blade, followed by tissue necrosis from the leaf tip towards the leaf base. Such symptomatic leaves are usually characterized by increased respiration, reduced photosynthesis, a change in the ratio of hexose to sucrose, and an increase in starch content. SCYLV infection affects carbon assimilation and metabolism in sugarcane, resulting in stunted plants in severe cases. SCYLV is mainly propagated by planting cuttings from infected stalks. Phylogenetic analysis has confirmed the worldwide distribution of at least eight SCYLV genotypes (BRA, CHN1, CHN3, CUB, HAW, IND, PER, and REU). Evidence of recombination has been found in the SCYLV genome, which contains potential recombination signals in ORF1/2 and ORF5. This shows that recombination plays an important role in the evolution of SCYLV.

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 spread of tomato yellow leaf curl virus from the Middle East to the world.

The ongoing global spread of Tomato yellow leaf curl virus (TYLCV; Genus Begomovirus, Family Geminiviridae) represents a serious looming threat to tomato production in all temperate parts of the world. Whereas determining where and when TYLCV movements have occurred could help curtail its spread and prevent future movements of related viruses, determining the consequences of past TYLCV movements could reveal the ecological and economic risks associated with similar viral invasions. Towards this end we applied Bayesian phylogeographic inference and recombination analyses to available TYLCV sequences (including those of 15 new Iranian full TYLCV genomes) and reconstructed a plausible history of TYLCV's diversification and movements throughout the world. In agreement with historical accounts, our results suggest that the first TYLCVs most probably arose somewhere in the Middle East between the 1930s and 1950s (with 95% highest probability density intervals 1905-1972) and that the global spread of TYLCV only began in the 1980s after the evolution of the TYLCV-Mld and -IL strains. Despite the global distribution of TYLCV we found no convincing evidence anywhere other than the Middle East and the Western Mediterranean of epidemiologically relevant TYLCV variants arising through recombination. Although the region around Iran is both the center of present day TYLCV diversity and the site of the most intensive ongoing TYLCV evolution, the evidence indicates that the region is epidemiologically isolated, which suggests that novel TYLCV variants found there are probably not direct global threats. We instead identify the Mediterranean basin as the main launch-pad of global TYLCV movements.

A discovery 70 years in the making: characterization of the Rose rosette virus.

Rose rosette was first described in the early 1940s and it has emerged as one of the most devastating diseases of roses. Although it has been 70 years since the disease description, the rosette agent is yet to be characterized. In this communication, we identify and characterize the putative causal agent of the disease, a negative-sense RNA virus and new member of the genus Emaravirus. The virus was detected in 84/84 rose rosette-affected plants collected from the eastern half of the USA, but not in any of 30 symptomless plants tested. The strong correlation between virus and disease is a good indication that the virus, provisionally named Rose rosette virus, is the causal agent of the disease. Diversity studies using two virus proteins, p3 and p4, demonstrated that the virus has low diversity between isolates as they share nucleotide identities ranging from 97 to 99%.

Port wine landscape: railroads, phylloxera, and agricultural science.

It is easy to understand why regions that produce very fine goods such as port wine tend to conceal technological and scientific inputs and praise the uniqueness of the terroir. This paper suggests that, during the last decades of the nineteenth century, viticulture in the Douro region of Portugal was as much a product of soil, local farming traditions, and individual entrepreneurship as it was of modern state science and national politics for agricultural improvement. the unprecedented public projects of building a railroad and fighting phylloxera permanently changed the land of port wine. Moreover, those engineering practices of rationalization, simplification, and standardization that were inscribed on Douro's landscape proved essential for the Portuguese experience of modernization and nation-building.

A history of virus diseases of plants: from the beginning to 1950.

The history of plant virology has given much space to viruses, especially to Tobacco mosaic virus, but very little space to virus diseases. Still, viruses were clearly characterised only more than fifty years after the first observations and descriptions of diseases appearing infected with ineffable agents and, until the 1950s, most of the plant virologists spent a lot of time to study the disease as the preliminary but absolutely necessity in order to identify the virus. The first virus diseases to be investigated were the "tobacco mosaic" in Europe and "rice stunt" in Far East Asia, and both represented useful models for performing a great number of similar researches. The study of virus diseases made necessary the employment of several strategies, and the introduction of new techniques of research. The simple observation of external symptoms, not too selective and requiring broad experience, was followed by histological and cytological analyses which, in the period herein considered, were carried out by light microscopic methodologies. These analyses helped the research of the physiological causes of symptom formation, which, unfortunately, did not always profit from the interest of plant physiologists and biochemists. This schematic series of efforts was not always followed, since research often proceeded in an erratic way, according to the interest or the possibility of single virologists. However, the comprehensive view emerging from the historical analysis of results (for example, from the first textbook of this discipline) allows us to outline that logical sequence of events we have mentioned above. Obviously, the diffusion of viruses in field was one of most investigated line of research, as well as the individuation of the losses produced by virus diseases. From these fields of research (epidemiology and control), it was possible to enter the war to the most pathogenetic viruses by obtaining the first positive successes: this war became more and more pressing and is still current by the use of a very high technology. The work performed during seventy years at first by beginner virologists and afterwards by mature virologists, amounts to a splendid page of history of virology: This page has been written by hundreds and hundreds researchers, most of them quite neglected by the new generation of plant virologists. This history also represents a grateful homage to those researchers.

Creating an agricultural world order: regional plant protection problems and international phytopathology, 1878-1939.

Beginning in 1878 with the International Phylloxera Convention of Berne, international conventions have sought to relieve national agricultural industries from two specific burdens. First, by defining phytosanitary practices to be enforced by national plant protection services, these conventions attempted to prevent the introduction of plant diseases and pests into national territories from which they were previously absent. Second, by standardizing these practices - especially through the design of a unique certificate of inspection - the conventions attempted to eliminate barriers such as quarantines affection international agricultural trade. The succession of phytopathological conventions seemed to epitomize the coalescence of an international community against agricultural pests. What actually coalesced was bio-geopolitics wherein plant pathologists and economic entomologists from North America and the British Empire questioned the so-called internationality of the environmental and economic specificities of continental European agriculture, embodied in "international" conventions. Although an international phenomenon, the dissemination of agricultural pests provided opportunities for cooperation on a strictly regional albeit transnational basis that pitted bio-geopolitical spaces against each other. This article retraces the formation of these spaces by analyzing the deliberations of committees and congresses that gathered to define an international agricultural order based on the means to prevent the spread of plant diseases and pests.

Richard Bradley: a unified, living agent theory of the cause of infectious diseases of plants, animals, and humans in the first decades of the 18th century.

During the years 1714 to 1721, Richard Bradley, who was later to become the first Professor of Botany at Cambridge University, proposed a unified, unique, living agent theory of the cause of infectious diseases of plants and animals and the plague of humans. Bradley's agents included microscopic organisms, revealed by the studies of Robert Hooke and Antony van Leeuwenhoek. His theory derived from his experimental studies of plants and their diseases and from microscopic observation of animalcules in different naturally occurring and artificial environments. He concluded that there was a microscopic world of "insects" that lived and reproduced under the appropriate conditions, and that infectious diseases of plants were caused by such "insects." Since there are structural and functional similarities between plants and animals, Bradley concluded that microscopic organisms caused human and animal infectious diseases as well. However, his living agent cause of infectious diseases was not accepted by the contemporary scientific society.

Noel T. Keen--pioneer leader in molecular plant pathology.

Noel T. Keen (1940-2002) made pioneering contributions to molecular plant pathology during a period when the study of disease mechanisms was transformed by the new tools of molecular genetics. His primary contributions involved race-specific elicitors of plant defenses and bacterial pectic enzymes. In collaboration with Brian J. Staskawicz and Frances Jurnak, respectively, Noel cloned the first avirulence gene and determined that pectate lyase C possessed a novel structural motif, known as the parallel beta-helix. Noel received his B.S. and M.S. from Iowa State University in Ames and his Ph.D. from the Department of Plant Pathology at the University of Wisconsin in Madison in 1968. He joined the faculty of the Department of Plant Pathology at the University of California at Riverside the same year and remained there his entire career. He served as Chair of the department from 1983 to 1989 and in 1997 assumed the William and Sue Johnson Endowed Chair in Molecular Plant Pathology. He became a Fellow of the American Phytopathological Society in 1991, a Fellow of the American Association for the Advancement of Science in 1996, a Fellow of the American Academy of Microbiology in 1997, and a member of the National Academy of Sciences in 1997. He was serving as President of the American Phytopathological Society (2001-2002) at the time of his death.

Tell me again what it is that you do.

My job at Pullman, Washington, starting in 1965, was to control the root diseases of wheat and barley, focusing first on fusarium root and crown rot, then including take-all and pythium and rhizoctonia root rots. In the absence of viable alternatives, the agronomic approaches used were implemented through design of cereal-based cropping systems. Starting in the late 1970s, the mission focused further on cereal-intensive direct-seed (no-till) cropping systems. A team effort demonstrated the role of indigenous antibiotic-producing fluorescent pseudomonads in the widespread decline of take-all in response to monoculture wheat (or barley-wheat sequences). Today, the suppression of take-all by these beneficial rhizobacteria is the centerpiece of an integrated system that augments take-all decline while limiting pythium and rhizoctonia root rots and fusarium root and crown rot in direct-seed systems. In such systems, "crop rotation" takes the form of different sequences of winter and spring wheat, barley and triticale varieties, and market classes, all susceptible to all four root diseases.

Breaking sod or breaking even? Flax on the northern Great Plains and Prairies, 1889-1930.

A new thirst for paint and color in cities made extensive flax production profitable in the northern Great Plains and Prairies and contributed to the cultivation of the most fragile grassland ecosystems. The production of flax seed for linseed oil became an early spin-off of the Prairie wheat economy but, unlike wheat, flax vanished from old land after one or two rotations and reappeared in districts with the most new breaking. Officials explained the migrant crop as preparing native grasslands for cultivation or exhausting soil in old land, but farmers brought flax to their new breaking for other reasons. Producers would only put flax on any land when a range of economic and environmental conditions were in place. It was never sown without promise of adequately high prices or in the absence of affordable seed and other inputs. When price allowed, it usually appeared on new breaking because it could be planted later and transported further without upsetting the balance of other activities and without farmers learning many new techniques. Scientists discovered that diseased soil drove flax off old land, not soil exhaustion. Circumventing the disease was possible but costly, and farmers simply replaced flax with the next most lucrative commodity.

Colonial foresters versus agriculturalists: the debate over climate change and cocoa production in the Gold Coast.

This article draws attention to the unfolding debate concerning forest cover loss, climatic change, and declining cocoa production in the Gold Coast (colonial Ghana) during the early twentieth century. It argues that, although desiccationist theory was prevalent, its acceptance among colonial authorities in the Gold Coast was far from hegemonic. There were important dissenting colonial voices, particularly among agriculturalists, who argued that declining cocoa yields were due to plant diseases, most notably cocoa swollen shoot disease. It was based on the latter's non-environmental model of disease transmission, rather than the premises of desiccation science, that the government's postwar "cutting out campaign" of cocoa was predicated. Nevertheless, the foresters' correlation of the deterioration of cocoa areas with fears of desiccation was not without its effects on state practice, providing the rationale for an accelerated program of forest reservations in the 1930s.

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.