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Home , Phytophthora infestans

CHAPTER 10

WORLDWIDE MIGRATIONS, SHIFTS, AND REEMERGENCE OF INFESTANS, THE PLANT DESTROYER

JEAN BEAGLE RISTAINO

INTRODUCTION tubers and fruit and is still wreaking havoc more than 160 years after Phytophthora species are plant the Irish (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 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 where path of devastation on potato in its wake in synthetic chemicals are not used (Stone, the United States, Ireland, and 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 -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 . 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 : "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 (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 , 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 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 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 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 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 and since they share a filamentous habit of the germ theory. In 1876, deBary elucidated growth by 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 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. 10.2a). elucidated phylogenetic relationships Tuber infections lead to a purplish brown among a larger group of Phytophthora discoloration of the tissue and eventually species (Blair et al., 2008; Kroon et al., 2004; the tuber rots (Fig. 10.2b). The pathogen Martin and Tooley, 2003). P. infestans is a causes brown lesions on the stems, petioles, member of the Ic clade of Phytophthora and leaves of tomatoes (Fig. 10.2c). (Blair et al., 2008; Cooke et al., 2000). Other Brown zonate lesions occur on the fruit species in this clade include the more dis­ (Fig. 10.2d). tantly related Phytophthora phaseoli and Sporangia (Fig. 10.2e) can be dispersed Phytophthora mirabilis, Phytophthora ipo- by wind and at local and national moeae, and Phytophthora andina (Flier scales (hundreds of meters) and entire et al, 2002; Galindo and Hohl, 1985; Oliva fields can be destroyed in a few days. Late et al., 2010). blight is truly a community disease, and

Figure 10.2 Symptoms of late blight caused by P. infestans on (a) potato leaf, (b) tuber, (c) tomato stem, (d) tomato fruit, (e) plants in a field, and (f) a tomato transplant, (e) Asexual sporangia borne on compound sporangiophores; (f) sexual oospore produced by fusion of anisogamous gametangia (male antheridium and female oogonia) of opposite mating types (Al and A2). See color insert. 196 WORLDWIDE MIGRATIONS, HOST SHIFTS, AND REEMERGENCE OF P. INFESTANS

inoculum in fields left untreated can spread chlorophyll-related plant hormone phytol to neighboring fields due to aerial dispersal (Ojika et al., 2011). This exciting discovery of sporangia. The pathogen has caused may lead to novel methods to stop sexual major losses mostly by the unintentional reproduction in the pathogen. spread on infected plant materials such as Oospores were reported first in , potato tubers or tomato transplants that but the pathogen now also reproduces sex­ are transported over large areas, as is illus­ ually in the Netherlands, , and trated by the widespread epidemics of 2009 (Andersson et al., 2009; Drenth on tomato in the United States (Hu et al., et al., 1994; Gavino et al., 2000). Oospores 2012). The pathogen typically survives from are not common in the United States and to season as mycelium in infected sexual reproduction is rare. The oospore is potato tubers, volunteer potato plants, or a thick-walled survival structure and can infected culled potatoes that contribute persist in at low temperatures for to epidemic development on subsequent several years but does not survive well at crops. higher temperatures (Fay and Fry, 1997; P. infestans is heterothallic and requires Maytoun et al., 2000). two opposite mating types, Al and A2, for sexual reproduction and formation of the nonmotile sexual oospore (Fig. 10.2f) POPULATION BIOLOGY: MIGRATION (Gallegly and Galindo, 1958). Oogonia THEORIES OF P. INFESTANS IN THE develop when Al and A2 mating type iso­ 19TH CENTURY lates are paired. Hormonal heterothallism is involved in the formation of gametangia P. infestans has four mitochondrial haplo- with one thallus producing a hormone types (la, lb, Ha, and lib) (Avila-Adame that stimulates gametangia formation of et al., 2006). The mitochondrial the opposite mating type (Ko, 1988). Each of all the extant haplotypes have been thallus is bisexual and can act as either sequenced (Avila-Adame et al., 2006; male or female and induces either oogonia Carter et al., 1990; Lang and Forget, 1993). or antheridia formation in the opposite Phylogenetic and coalescent analysis mating type (Judelson, 1997). Studies of the revealed that although the type I and II inheritance of mating type show that the haplotypes share a common ancestor, they Al types have a heterozygous locus (Aa), form two distinct lineages that evolve inde­ while A2 types are homozygous recessive pendently. Type II haplotypes diverge (aa) (Fabritius and Judelson, 1997; Judelson earlier than type I haplotypes. The type II et al., 1995).The position of the mating type lineages did not evolve from type I lineages, locus on a genetic linkage map (Van der as previously suggested (Gavino and Fry, Lee et al., 2004) and in genomic clones 2002). Our data support the hypothesis that (Randall et al., 2003) has been identified all the extant mitochondrial lineages of P. and in several strains has been linked to infestans evolved from a common ancestor genetic abnormalities such as balanced in since the most ancient lethality and translocations (Judelson, mutations in the four lineages occur there 1996a,b). The Al mating-type hormone (Gomez et al., 2007). MH-1 a has been purified and reported to The center of origin and diversity of be a diterpene (Harutyunyan et al., 2008; the late blight pathogen is proposed to Qi et al., 2005). A second structurally be in Mexico (Fry and Goodwin, 1997; similar mating hormone, MH-2 a, has Goodwin et al., 1994b; Reddick, 1939). recently been purified, and both hormones This hypothesis is based on the fact that are proposed to be derived from the in Mexico, (i) both mating types occur; WHAT mtDNA HAPLOTYPE CAUSED THE FAMINE AND WHERE DID IT COME FROM? 197

(ii) host resistance genes are present in of the pathogen from Mexico after the wild Solatium populations; and (iii) patho­ 1970s (Goodwin et al., 1994a), but no defin­ gen populations are highly diverse for itive evidence for migrations of P. infestans neutral DNA markers and pathotypes. Iso­ during the interval between 1840 and 1970. lates of P. infestans of the A2 mating type The fact that the putative "old" US-1 and oospores in infected plant material lineage (lb mtDNA) has not been widely were first discovered in central Mexico in reported in Mexico, does not support the 1956 (Fry et al, 1992; Gallegly and Galindo, theory that Mexico provided the source 1958; Goodwin et al., 1994a). Prior to 1980, inoculum for the late blight epidemics of both the Al and A2 mating types were the . reported only in Mexico, while the Al The Mexican "bottleneck" theory of mating type was reported elsewhere in the Goodwin and colleagues was challenged by world (Fry, 2008; Fry and Goodwin, 1997; several authors (Abad and Abad, 1997; Gallegly and Galindo, 1958). This situation Andrivon, 1996; Ristaino, 1998; Tooley changed in the 1980s when the A2 mating et al., 1989). A second "hybrid" migration type was observed in Switzerland (Hohl theory was proposed, suggesting that and Iselin, 1984). Mexico may represent the center of origin Mexico has also been proposed to have of the disease but that inoculum that caused provided the source inoculum for the late the 19th century potato famine epidemics blight epidemics of the 1840s (Fry and originated in Peru (Andrivon, 1996; Bourke, Goodwin, 1997; Goodwin et al., 1994b). 1964). This theory was based on both his­ Genetic analysis of modern worldwide torical data and an evaluation of the pub­ populations of P. infestans demonstrated lished population genetic data at the time. that they were dominated by a single clonal A third theory suggests that the Peruvian lineage known as the US-1 "old" represents both the center of origin (mtDNA haplotype lb) in the mid 20th of the disease and the source of inoculum century (Fry, 2008; Goodwin et al., 1994b). for 19th century epidemics. Evidence to Mexican populations are highly diverse for support this theory has been provided by genotypic and phenotypic markers and both historical data about disease occur­ thus, Mexico clearly represents a present- rence (Abad and Abad, 1997; Berkeley, day center of diversity of the pathogen. 1846) and population genetic data (Gomez However, since Mexican populations are et al., 2007). highly diverse, the pathogen population is proposed to have undergone a genetic bot­ tleneck in the 1840s during the first migra­ WHAT mtDNA HAPLOTYPE CAUSED tion event, thus greatly reducing genetic THE FAMINE AND WHERE DID IT diversity, in order to explain the dominance COME FROM? of a single "old" clonal genotype (US-1 genotype) in modern worldwide popula­ Nineteenth and early twentieth century tions prior to the 1980s (Fry and Goodwin, scientists collected and preserved potato 1997; Goodwin et al., 1994b). Domesticated and tomato leaves infected with P. infes­ potatoes were not grown for export in tans, and specimens exist from the Irish Mexico in the 1840s and tuber blight was potato famine (Fig. 10.1b,c). Historical not common. It was suggested that the specimens have been analyzed to answer pathogen may have been accidentally questions about the evolution and popu­ introduced by a plant collector (Goodwin lation biology of the pathogen (Ristaino, et al., 1994b). These authors have provided 1998, 2002, 2006; Ristaino et al., 2001; well-documented evidence for migrations May and Ristaino, 2004). The polymerase 198 WORLDWIDE MIGRATIONS, HOST SHIFTS, AND REEMERGENCE OF P. INFESTANS

TABLE 10.1 Identity of the Mitochondrial DNA Lineage of P. infestans in Archival Herbarium Specimens Collected Worldwide Year Number of Geographic Region Collected Specimens mtDNA Haplotype" Central and South America 1889-1969 18 la lb—Bolivia (1944), Ecuador (1967) lib—Nicaragua (1956) 1855-1958 88 la lb (1931 and later—potato, tomato, Solatium sarrachoides) Northern Europe 1866-1905 11 la Western Europe 1845-1982 52 la Eastern Europe 1892-1978 7 la United Kingdom 1845-1974 52 la China 1935-1982 10 la lb (1952—potato, 1956—tomato) lb (1982—Solarium lyratum) Southeast Asia and Australia 1901-1987 13 All la except: (Japan, Philippines India, lb India (1968,1974—potato) Nepal, Peninsular lb Thailand, (1981—tomato) Malaysia, Thailand) ' Based on PCR methods of Griffith and Shaw (1998).

chain reaction (PCR) has been used to Interestingly, both the la and lib haplo­ amplify minute amounts of DNA from types were found in potato leaves from leaves infected with P. infestans from his­ specimens collected in 1954 and 1956 in toric epidemics. Nicaragua (Table 10.1). These data chal­ The mtDNA haplotypes present in spec­ lenge the hypothesis that a single clonal imens collected during the Irish potato lineage of P. infestans existed outside of famine and later in the 19th and early 20th Mexico since two mtDNA haplotypes were century were identified (May and Ristaino, present in samples from Nicaragua. Thus, 2004; Ristaino et al., 2001). First, a 100-bp late blight populations in the mid 20th fragment of DNA from ITS region 2 spe­ century in Central America did not consist cific for P. infestans was amplified from of a single clonal lineage and pathogen 90% of the leaves tested, confirming infec­ diversity was greater than previously tion by P. infestans (Trout et al., 1997; believed. Ristaino, 1998, 2001). Primers were then designed that amplify short segments of mtDNA around variable restriction sites WHEN DID THE mtDNA HAPLOTYPE that separate the four mtDNA haplotypes lb MIGRATE FROM SOUTH (Griffith and Shaw, 1998) and the DNA was AMERICA? sequenced. Surprisingly, 86% of lesions from leaves collected during historic epi­ The lb haplotype of P. infestans was found demics were caused by the mtDNA haplo­ in several plant samples from herbaria type la (May and Ristaino, 2004), not lb including a sample from Bolivia (1944) and (Goodwin et al., 1994b), as previously Ecuador (1967) in the mid-20th century believed. (Table 10.1) (May and Ristaino, 2004). We HISTORIC MIGRATIONS: "OUT-OF-SOUTH AMERICA" MIGRATION HYPOTHESIS 199 recently examined mtDNA haplotypes of from portions of two nuclear genes (¿3- several hundred samples of P. infestans tubulin and ras) and several mitochondrial from infected potato and tomato leaves loci P3 (rpll4, rpl5, tRNA) and P4 (Coxl) from herbaria collected from the United from 94 "modern" isolates from South States between 1855 and 1953. In all cases, America, Central America, North America, haplotype la was predominant and found and Ireland in order to test an out-of-South before the haplotype lb was detected (May America migration hypothesis (Gomez and Ristaino, 2004; Ristaino and Lassiter, et al., 2007). Summary statistics, migration unpublished data). The la haplotype of P. analyses, and the genealogy of populations infestans was also found earlier in China of P. infestans for both nuclear (ras ) than other mtDNA haplotypes (Ristaino and mitochondrial loci are consistent with and Hu, 2009). In contrast, the earliest an out-of-South America origin for P. infes­ record of haplotype lb in China was in 1952 tans rather than an "out-of-Mexico" origin. on potato in 1954 and in 1956 on tomato Mexican populations of P. infestans from (Beijing). The haplotype lb still occurs in the putative center of origin in Toluca the Beijing area on tomato (Guo et al., Valley of Mexico harbored less nucleotide 2010). Modern Chinese populations contain and haplotype diversities than Andean all four haplotypes, suggesting more recent populations. Coalescent-based genealogies introductions of Ha and lib haplotypes of mitochondrial and nuclear loci were con­ (Guo et al., 2010). In other areas in Asia, gruent and demonstrate the existence of the earliest documentation of haplotype la two lineages leading to present-day haplo­ was in Japan in 1901. The haplotype la was types of P. infestans on potatoes. Mitochon­ also found in India (1913), the Philippines drial haplotypes found in Toluca, Mexico, (1910), and Russia and Australia (1917). In were from the type I haplotype lineage, contrast, haplotype lb was only found in whereas those from Peru and Ecuador three samples in India on potato (1968 and were derived from both type I and type II 1974) and in Thailand on tomato (1981). All lineages (Fig. 10.3). Mitochondrial and the rest of the herbarium plant samples nuclear haplotypes in populations from from other Southeast Asian countries and both the United States and Ireland were regions were infected with haplotype la derived from both ancestral lineages that (Table 10.1).Thus, our data suggest that the occur in South America, suggesting a haplotype lb was dispersed in early to mid- common ancestry among these popula­ 20th century migrations into the United tions. The oldest mitochondrial lineage was States, China, and Southeast Asia, whereas associated with isolates from the botanical earliest introductions during the famine- section Anarrhichomenum including Sola- era epidemic in the United States and num tetrapetalum from Ecuador (Gomez Europe, no doubt on imported potato et al., 2007). This lineage (EC-2 Ic) shares tubers, were the la haplotype (May and a common ancestor with P. infestans and Ristaino, 2004; Ristaino and Hu, 2009). has been named P. andina (Gomez et al., 2008; Kroon et al., 2004; Olivia et al, 2010). The geographic distribution of mutations HISTORIC MIGRATIONS: on the rooted coalescent tree for both "OUT-OF-SOUTH AMERICA" nuclear and mitochondrial loci demon­ MIGRATION HYPOTHESIS strates that the oldest mutations in P. infes­ tans originated in South America; this is We have assessed the genealogical history consistent with an Andean origin (Gomez of P. infestans using multilocus sequences et al., 2007). 200 WORLDWIDE MIGRATIONS, HOST SHIFTS, AND REEMERGENCE OF P. INFESTANS

19 SA

20 SA

21 NSA

8 SA

24 NSA

7 NSA 25 NSA

6 NSA

26 SA 5 NSA

27 NSA

28 NSA

, 30 SA 23 NSA 16 NSA 15 NSA

13 NSA

10 SA

22 NSA 4 NSA

H6 H2 H3 H4 H5 H8 H1 H7 H9

3 24 1 1 3 2 23 1 Count

3 7 20 1 South American 17 3 Non-South American 3 Bolivia 5 Brazil 5 Peru 7 Ecuador Costa Rica Mexico United States Ireland

A2 A1/A2 A1 A2 A1/A2 A1/A2 A1/A2 A1/A2 A1 Mating type le la/1b la la la la Ma Mb lia Carter's mtDNA haplotype Type I Type II HOST SHIFTS AND JUMPS 201

Figure 10.3 The rooted coalescent-based gene genealogy showing the distribution of mutations for South American (SA: Peru, Ecuador, Bolivia, Brazil) and non-South American (NSA: Costa Rica, Mexico, United States, Ireland) populations for the mitochondrial (P3 + P4) loci of Phytophthora infestons generated using GENET- REE. The timescale is in coalescent units of effective population size and the direction of divergence is from the top (past-oldest) to the bottom (present-youngest). Numbers below the tree from top to bottom designate each distinct haplotype (H) and its count (i.e., the number of occurrences of the haplotype in the sample, where. = 0), the count of each haplotype in each population, the mating type of the isolates, and the mtDNA haplotype according to Carter et al. (1990). Image reproduced with permission from the Proceedings of the National Academy of Sciences of the United States of America from Gomez et al. (2007).

HOST SHIFTS AND JUMPS cally in Ecuador with P. andina. P. andina can infect other non-tuber-bearing species P. infestans can infect other of Solanum, Solanum muricatum, and species and has shifted hosts on numerous Solanum betaceum, indicating that P. andina occasions to exploit new niches. After its has an expanded host range compared to P. first introduction into Ireland, it was infestans. P. mirabilis was first considered reported by Moore in Dublin in 1846 on the closest known relative of P. infestans Anthocercis illicfolia, a solanaceous shrub (Galindo and Hohl, 1985). However, phylo- that had been imported from Australia into genetic analysis of P. andina from Ecuador the Botanic Gardens at Glasnevin (Fig. suggests that P. andina (EC-2 Ic lineage) is 10.1b). The pathogen was also reported in also closely related to P. infestans (Adler petunia in the United Kingdom by M. C. et al, 2004; Blair et al., 2008; Gomez et al., Cooke in 1856. The haplotype lb of P. infes­ 2008; Kroon et al., 2004; Oliva et al., 2010), tans was identified on Solanum lyratum, a and this lineage shares a common ancestor weed host that occurs commonly alongside with P. infestans in the Andean region potato fields in China in 1982 (Table 10.1). (Gomez et al., 2007). The occurrence of the lb haplotype on a Whether P. andina evolved as a hybrid weed host in China, coincident with the of P. infestans and P. mirabilis (Gomez et time of first use of the metalaxyl al., 2008) or some other very close relative in the country, suggests that this host shift of P. mirabilis is still uncertain (Goss et al., may have enabled this fungicide-sensitive 2011; Lassiter et al., 2010). The ras intron 1 strain to survive by avoiding the fungicide sequence suggests that P. andina may have that had been sprayed in fields. Weeds such arisen from a hybridization possibly as Solanum nigrum, Solanum dulcamara, between P. infestans and P. mirabilis and Solanum sisymbriifolium are also hosts (Gomez et al., 2008). However, P. mirabilis of P. infestans and may act as a refuge and has not been found in Ecuador where P. overwintering host for the pathogen in the andina occurs. P. mirabilis was first reported absence of a potato or tomato crop in the in Mexico (Galindo and Hohl, 1985), so field (Flier et al., 2003). further exploration for P. mirabilis in the P. infestans occurs sympatrically in Andean region is warranted. P. infestans Mexico with P. mirabilis a pathogen that and P. mirabilis can hybridize in the labora­ infects Mirabilis jalapa and P. ipomoeae tory and produce viable progeny (Goodwin a pathogen that infects Ipomoea longipe- and Fry, 1994). M. jalapa has not been dunculata (morning glory). The evolution widely surveyed for P. mirabilis in South in the Ic clade has involved host jumps to America, although the host evolved in these unrelated plant species (Raffaele Peru and its common name is the flower of et al., 2010). P. infestans occurs sympatri­ Peru. We are currently using nuclear gene 202 WORLDWIDE MIGRATIONS, HOST SHIFTS, AND REEMERGENCE OF P. INFESTANS

genealogies and Bayesian statistics to in plant material (tubers or transplants) clarify the evolutionary relationships of the have made local and long-distance spread Ic clade species (Lassiter et al., 2010). One common. The polycyclic nature of the life interpretation of the data is that the Andean cycle enables the pathogen to produce region is the center of evolutionary origin copious amounts of in a short time for all the species in the Ic clade since P. period on aerial parts of plants, and these andina and P. infestans coexist there and spores can move rapidly (within days) the oldest mutations in the P. andina EC-2 through untreated fields. Pathogen popula­ Ic lineage are of South American origin. tions became resistant to the phenylamide Further surveys are needed to test the pos­ fungicides shortly after their introduction. sibility of the occurrence of P. mirabilis and The widespread of highly sus­ P. ipomoeae in the Andean region. ceptible potato cultivars in the United The patterns of sequence variation States has made them vulnerable to disease. involved in host jumps in several Ic clades P. infestans also can infect a wide range species of Phytophthora including P. pha- of other solanaceous plants. The plasticity seoli, P. ipomoeae, and P. mirabilis have of the as revealed by genome been compared to P. infestans by rese- sequencing and the diversity of pathogen quencing genomes of the sister species in effectors that can overcome host R (resis­ the Ic clade (Raffaele et al., 2010). Patterns tance) genes make host resistance a moving of gene-sparse, repeat-rich regions in the target at best and make the search for more genomes of the sister species were found, durable host resistance a more viable goal as reported in the P. infestans genome then single-gene resistance (Haas et al., (Haas et al., 2009; Raffaele et al., 2010). 2009; Kamoun and Smart, 2005). These repeat-rich regions contained many Populations of P. infestans in the United effector genes that showed evidence of States have consisted of a series of mostly positive selection, uneven rates of evolu­ asexual clonal and 19 genotypes tion, and enrichment of genes induced in have been reported previously in regional planta during preinfection and infection, populations (Fraser et al., 1999; Fry et al., suggesting host adaptation has led to the 1992; Gavino et al., 2000; Goodwin et al., evolution of species in the clade. Unfortu­ 1994a, 1998;Wangsomboondee et al., 2002). nately, these authors (Raffaele et al., 2010) We recently identified five new multilocus did not analyze the genome of P. andina genotypes in the eastern United States due to difficulties in reassembly of the (US-20 to US-24) (Hu et al., 2012). The genome, which contained many loci with presence of sexually reproducing popula­ heterozygous sites, a situation suggestive of tions in several European countries has P. andina being a hybrid (Brasier et al., been documented by restriction fragment 1999; Gomez et al., 2008; Goss et al., 2011; length polymorphism (RFLP) markers Kroon et al., 2004; Lassiter et al., 2010). and later by microsatellite markers (Cooke et al., 2007; Drenth et al., 1994; Knapova and Gisi, 2002; Lees et al., 2006; Zwankhui- WHY IS LATE BLIGHT A zen et al., 1998, 2000). REEMERGING DISEASE? In 2009, a widespread strain, US-22 (Hu et al., 2012), identified by multilocus geno- Late blight has reemerged as a significant typing, spread in the northeast of the threat to production for both tomato and United States on tomato transplants and potato. The varied dispersal mechanisms of rapidly infected potatoes. There was a com­ the pathogen including the ability to move plete loss of the tomato crop in many states both as airborne inoculum (sporangia) and and an increase in fungicide use on pota- REFERENCES 203 toes to curb epidemic spread. A combina­ help document the pathogen-host arms tion of weather conducive for disease and race and lead to strategies to slow the widespread inoculum distribution exacer­ development of new pathotypes of P. bated the epidemic. Strain US-22 was very in fes tans. widespread (12 states) on tomato and potato, and this genotype accounted for about 60% of all the isolates genotyped in CONCLUSIONS 2009 in the United States. Organic tomato growers were devastated by the disease Further field and laboratory studies are since few options for control besides under way exploiting the P. infestans copper-based sprays are available in these genome sequence to develop rapid geno- production systems. At least 400 farms typing methods and to monitor further were affected by the disease in New changes in the structure of both selectively England (Moskin, 2009). The lack of neutral and evolving traits of the popula­ deployment of resistant varieties of both tions of the pathogen in North America. A potato and tomato in the United States has national portal (http://www.USAblight.org) exacerbated the situation. On the basis of has been developed to track disease occur­ sequence analysis of the ras gene, US-22, rences, send disease alerts, provide a venue US-23, and US-24 appear to have been for submitting samples for diagnosis and derived from a common ancestor (Hu et al., genotyping, publish pathogen multilocus 2012). genotypes, and provide management infor­ The US-8 genotype, which is still mation to growers developed by the exten­ common on potatoes in the United States, sion and research community on late blight. is mefenoxam resistant. Isolates of the Over 160 years after the , late widespread US-22 genotype and several blight continues to challenge the sustain­ other clonal lineages (US-23 and US-24) able production of potato worldwide. are largely sensitive to mefenoxam. How­ ever, this information was not known REFERENCES until after the widespread epidemics in the United States in 2009 since fungicide Abad ZG, Abad JA. 1997. 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