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Worldwide Migrations, Host Shifts and Reemergence Of CHAPTER 10 WORLDWIDE MIGRATIONS, HOST SHIFTS, AND REEMERGENCE OF PHYTOPHTHORA INFESTANS, THE PLANT DESTROYER JEAN BEAGLE RISTAINO INTRODUCTION potato tubers and tomato fruit and is still wreaking havoc more than 160 years after Phytophthora species are oomycete plant the Irish famine (Fry, 2008; Hu et al., 2012). pathogens that are responsible for devas­ Late blight is the most important biotic tating diseases on a wide range of food and constraint to potato production worldwide ornamental crops, natural vegetation, and and is major threat to food security, par­ forest trees worldwide (Erwin and Ribeiro, ticularly in the developing world where use 1996). Indeed the name Phytophthora is of fungicides is often uneconomical (Ander­ derived from the Greek phytó, "plant," and son et al., 2004; Pennisi, 2010). Worldwide phthorá, "destruction"; thus, members of losses due to late blight on potato and this genus are often referred to as "the tomato exceed $7 billion annually (Haver- plant destroyer." They represent an emerg­ kort et al., 2008). Evolution of strains ing food security threat, in large part due varying in sensitivity to fungicides and to increases in plant movement via interna­ novel pathotypes of P. infestans continue to tional trade (Brasier, 2008). Phytophthora challenge the sustainable production of infestans, the causal agent of late blight, potatoes. The pathogen has also reemerged exemplifies this threat; it was the first as a significant disease threat to the organic species in the genus described and left a tomato industry in the United States where path of devastation on potato in its wake in synthetic chemicals are not used (Stone, the United States, Ireland, and Europe in 2009). In 2009, late blight epidemics of the 19th century (Berkeley, 1846; Bourke, potato and tomato in the eastern United 1964; deBary, 1876). Movement of infected States were the worst in recent history due potato tubers led to the potato famine epi­ to widespread inoculum distribution and demics of the 19th century that resulted in weather conducive for disease (Hu et al., widespread human hunger, disease, and, 2012; Moskin, 2009). ultimately, death of two million people in This chapter provides an overview of the Ireland. The pathogen causes a destructive emergence of potato late blight in the 19th foliar blight of potato and also infects century and the evolutionary position, life Evolution of Virulence in Eukaryotic Microbes, First Edition. Edited by L. David Sibley. Barbara J. Howlett, and Joseph Heitman. © 2012 Wiley-Blackwell. Published 2012 by John Wiley & Sons, Inc. 192 EMERGENCE OF LATE BLIGHT IN THE UNITED STATES AND EUROPE 193 history, and the population biology of P. the lower Rhineland, Switzerland, and to infestans. Worldwide migrations of the southern England. In 1845, on the 16th of pathogen and the role of host shifts in the August, it was seen in the Isle of Wight and evolution of species in the genus are also on the 23rd of August in the South of discussed. England. The potato blight made its way into Ireland by the 7th of September, 1845, and later in the year to Scotland (Bourke, EMERGENCE OF LATE BLIGHT IN 1964). THE UNITED STATES AND EUROPE The farmers and learned men and women of the time immediately started The potato blight struck with a vengeance to speculate as to the cause of the "evil" in the United States in 1843 before it that was now widely affecting potatoes appeared on the European continent and grown everywhere. James Teschemacher, in the British Isles. The potato crop in the a member of Boston's Natural History United States was a good one in 1842, but Society, associated a minute fungus with the situation changed in 1843. One account the lesions on the potato plant (Teschem­ documented in the Annual Report of the acher, 1844). There was by no means a Commissioner of Patents in the United consensus on the subject of the cause of States stated that the "potato yield was the potato blight, which was attributed nearly 50 percent less owing to a rot which to the weather, insects, the wrath of God, seized them before the time for taking and the minute "fungus." Speculation began them out of the ground" (Ellsworth, 1843). about the cause of the disease and lively A second report in the same document discussions ensued in the Gardeners Chron­ stated "The potato crop has been attacked. icle in the United Kingdom: "That minute The cause is generally attributed to the and rapidly propagating fungi have been peculiarity of the weather" (Ellsworth, observed on the affected potato plants, 1843). The late blight epidemic began in there is no reason to doubt. But when we 1843 in the United States in a five-state know, from other facts, that such appear on area starting from the ports of New York plants after they are dead or diseased, and and Philadelphia (Bourke, 1964; Ellsworth, not when they are alive and healthy, we are 1843). The first appearance of the disease justified in affirming that we are yet igno­ near the two port cities of Philadelphia and rant of the cause of the malady in question" New York suggested an introduction via (MacKenzie, 1845). Others wrote, "It is imported tubers. Potatoes and bat guano, certain that a fungus appears in the leaves, which were used as fertilizer, were being stems, and tubers of the plants which have shipped at that time from Peru in South been attacked, but it is uncertain how far America into many ports in both the United the fungus is the cause or the consequence States and Europe to improve the stock of of the disease - how far it is to be consid­ seed potatoes that had declined from ered as a parasite upon the living potato, or Fusarium dry rot. These potatoes probably as a mere devourer of its dying parts" provided the source of inoculum for the (Johnson, 1845). first disease outbreaks. The pathogen was described and named In Europe, late blight was first noticed by C. Montagne in France and in the United on the coast of Belgium in the Courtrai Kingdom by the Reverend M. J. Berkeley area in June of 1845 (Bourke, 1964). By in 1846 as Botrytis infestans (Berkeley, mid-July, late blight had moved southward 1846; Montagne, 1845). Morren had into Flanders and parts of the Netherlands observed the disease in Belgium in 1844 and France. By August, it had spread into and called it Botrytis devastatrix and 194 WORLDWIDE MIGRATIONS, HOST SHIFTS, AND REEMERGENCE OF P. INFESTANS (b) Figure 10.1 (a) M. J. Berkeley, the British mycologist who described the pathogen Botrytis infestans (later named as Phytophthoru infestans) on potato in 1846; (b) sporangia and sporangiophores of P. infestans drawn on a famine-era archival specimen label by David Moore, Glasnevin, Ireland, that was sent to Berkeley for confirma­ tion; (c) herbarium specimen with leaf lesion caused by P. infestans collected by Krieger in Germany in 1888. See color insert. presented a paper to the Royal Society of the life cycle of the pathogen and based on Lille (Morren, 1844). Libert had also called sporangial development and sporangio- the pathogen B. devastatrix (alternate spell­ phore characteristics and changed its name ing vastatrix or devastrix) Lib. 1845, but from Peronospora to P. infestans (deBary, Berkeley chose to use the species name B. 1876). infestans. In 1847 and 1852, Unger and Caspary, respectively, considered it in the genus Peronospora (Unger, 1847). deBary EVOLUTIONARY POSITION AND initially accepted this opinion (Cline et al., PHYLOGENETIC RELATIONSHIPS 2008; deBary, 1863). OF PHYTOPHTHORA SPP. Miles J. Berkeley (Fig. 10.1a) and later deBary resolved the debate by document­ The genus Phytophthora now encompasses ing that the "fungus-like" organism P. infes­ more than 100 species that are classified tans was the cause and not the consequence within the diploid, algae-like Oomycetes in of the disease. David Moore of Ireland the Kingdom Stramenopila (Adl et al., drew pictures of the sporangiophores and 2005; Bauldauf, 2003; Gunderson et al., sporangia of the pathogen and sent speci­ 1987). The number of Phytophthora species mens to Berkeley, who named the patho­ described has increased rapidly due to gen B. infestans (Fig. 10.1b). The work on intensive monitoring of plants and water­ late blight by Berkeley predated work by ways in the past 10 years for Phytophthora Louis Pasteur on the germ theory and ramorum, the cause of sudden oak death clearly documented that a microbe could (Cline et al., 2008; Rizzo et al., 2002). cause disease (Berkeley, 1846) and was a Oomycetes were once grouped with true major contribution to both the develop­ fungi (ascomycetes and basidiomycetes) ment of the science of plant pathology and since they share a filamentous habit of the germ theory. In 1876, deBary elucidated growth by mycelium and obtain nutrition LIFE HISTORY OF THE PATHOGEN 195 by absorption. However, oomycetes differ LIFE HISTORY OF THE PATHOGEN from true fungi in many ways and are now placed in a separate kingdom in a distinct P. infestans is a hemibiotrophic pathogen branch in the eukaryotic tree of life and are that infects host tissue and after a few days more closely related to brown algae and produces symptoms. One reason why late diatoms than true fungi (Adl et al., 2005). blight is such a destructive disease is due to Based upon sequences of ribosomal the explosive, polycyclic nature of asexual genes and the introns associated with them sporulation that can occur on plant tissue (internal transcribed spacer [ITS] regions), (Fig. 10.2a). 10 clades in the genus Phytophthora were The pathogen produces black water- described (Cooke et al., 2000). Subse­ soaked lesions on potato leaf tissue that quently, multilocus sequencing more clearly produce asexual sporangia (Fig.
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