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Rapid Global Spread of Two Aggressive Strains of a Wheat Rust Fungus

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Rapid Global Spread of Two Aggressive Strains of a Wheat Rust Fungus Molecular Ecology (2008) doi: 10.1111/j.1365-294X.2008.03886.x RapidBlackwell Publishing Ltd global spread of two aggressive strains of a wheat rust fungus MOGENS S. HOVMØLLER,* AMOR H. YAHYAOUI,† EUGENE A. MILUS‡ and ANNEMARIE F. JUSTESEN* *Department of Integrated Pest Management, Faculty of Agricultural Sciences, University of Aarhus, Flakkebjerg, 4200 Slagelse, Denmark, †International Center for Agricultural Development in the Dry Areas, PO Box 5466, Aleppo, Syria, ‡Department of Plant Pathology, University of Arkansas, Fayetteville, AR 72701, USA Abstract Rust fungi can overcome the effect of host resistance genes rapidly, and spores can disperse long distance by wind. Here we demonstrate a foreign incursion of similar strains of the wheat yellow rust fungus, Puccinia striiformis f. sp. tritici, in North America, Australia and Europe in less than 3 years. One strain defined by identity at 15 virulence loci and 130 amplified fragment length polymorphism (AFLP) fragments was exclusive to North America (present since 2000) and Australia (since 2002). Another strain of the same virulence phenotype, but differing in two AFLP fragments, was exclusive to Europe (present since 2000–2001) as well as Western and Central Asia and the Red Sea Area (first appearance unknown). This may be the most rapid spread of an important crop pathogen on the global scale. The limited divergence between the two strains and their derivatives, and the temporal–spatial occurrence pattern confirmed a recent spread. The data gave evidence for additional intercontinental dispersal events in the past, that is, many isolates sampled before 2000 in Europe, North America and Australia had similar AFLP fingerprints, and isolates from South Africa, which showed no divergence in AFLP, differed by only two fragments from particular isolates from Central Asia, West Asia and South Europe, respectively. Previous research has demonstrated that isolates of the two new strains produced up to two to three times more spores per day than strains found in USA and Europe before 2000, sug- gesting that increased aggressiveness at this level may accelerate global spread of crop pathogens. Keywords: clonal evolution, long-distance dispersal, phylogeography, Puccinia striiformis, stripe rust, yellow rust Received 8 April 2008; revision received 26 June 2008; accepted 30 June 2008 in regions where the climate is seasonally unfavourable Introduction (Brown & Hovmøller 2002). For obligate biotrophic fungi, The pace at which microbes spread to new niches is a which are completely dependent on living host tissue critical determinant of the emergence or re-emergence of for reproduction, the production of huge numbers of infectious diseases in humans, animals and plants (Anderson wind-dispersed spores is essential for spread and survival et al. 2004; Hui 2006), affecting health (Binder et al. 1999) (Brown et al. 2002). and food security (Strange & Scott 2005). Crop pathogens are In this study, we have focused on the recent spread and spread long distance mainly by human activity resulting evolution of a cereal rust fungus, Puccinia striiformis f. sp. from trade and travel or by wind-dispersed spores, tritici, which is a dikaryotic basidiomycete causing yellow allowing the pathogens to colonize new areas or re-establish rust (stripe rust) on wheat. Unlike other wheat rusts, yellow rust is not known to complete a sexual reproductive cycle Correspondence: Mogens Støvring Hovmøller, Fax: +45 8999 3501; as no alternative host has been identified (Stubbs 1985) E-mail: [email protected] and no recombination under natural conditions has been © 2008 The Authors Journal compilation © 2008 Blackwell Publishing Ltd 2 M. S. HOVMØLLER ET AL. reported (Hovmøller et al. 2002; Enjalbert et al. 2005). Puccinia The combined effect of this sampling strategy and a rigorous striiformis f. sp. tritici has highly specialized host preferences phenotype assessment based on both virulence and AFLP and follows the pattern of a gene-for-gene relationship markers provided a unique opportunity to test the role of (Flor 1971). Thus, the pathogen can be grouped into virulence long-distance dispersal of an important crop pathogen. phenotypes, defined by its compatibility with host The phylogeographical pattern of pathogen evolution plants possessing different resistance genes (Brown 2003). provided the basis for a discussion of the sequence of Although virulence represents the lack of recognition events and dispersal mechanisms. between pathogen and host, the term ‘virulence phenotype‘ is used throughout this study to designate the combined Materials and methods phenotypic state of the virulence/avirulence loci considered. Genetic variability at the DNA level is often low in Sampling P. striiformis f. sp. tritici at national and regional scales as compared to the diversity for virulence phenotype (Steele Most Puccinia striiformis f. sp. tritici isolates (Table 1) were et al. 2001; Hovmøller et al. 2002; Enjalbert et al. 2005). obtained by the authors from local field trials and Therefore, population studies of this pathogen are often commercial fields as single lesions on detached wheat based on techniques with a high power of discrimination, leaves and kept on 0.5% water agar containing 35 p.p.m. like amplified fragment length polymorphism (AFLP; benzimidazole until multiplication on wheat cultivar Justesen et al. 2002), despite the dominant nature of AFLP ‘Cartago’. Additional isolates were supplied by C. Wellings fragments (Vos et al. 1995). (Australia), X. Chen (Western USA), Z. Pretorius (South Recent epidemics of yellow rust have appeared in new Africa), C. de Vallavieille-Pope, R. Bayles and L. Boyd areas, for example, warm areas in eastern USA (Chen 2005; (Europe), R. Singh (Mexico) and E. Duveiller (Nepal). Except Milus et al. 2006). In 1996, the disease emerged for the for isolates sampled in Australia, they were multiplied first time in South Africa (Boshoff et al. 2002) and in 2002, under quarantine facilities at the Faculty of Agricultural yellow rust first appeared in Western Australia (Wellings Sciences, University of Aarhus, Denmark. et al. 2003). Isolates sampled from eastern USA since 2000 had unusual virulence phenotypes for the region (Chen Determination of virulence phenotypes 2005; Markell & Milus 2008), similar to the virulence phenotype of most isolates from Western Australia (Wellings Isolates were assayed for virulence phenotype using a set 2007). A similar phenotype was reported for the first time of 30 wheat yellow rust differential cultivars and lines in Central and northern Europe in 2000–2001 (Flath & according to Hovmøller & Justesen (2007a). The virulence Barthels 2002; Hovmøller & Justesen 2007a). Nearly all phenotype of Australian isolates were derived from isolates from eastern USA sampled since 2000 were closely Wellings (2007) and a common scoring by C. Wellings, related, based on AFLP fingerprints, and clearly different Plant Breeding Institute, University of Sydney and the from representative isolates collected all over USA before Correspondence of this paper. The virulence phenotype 2000 (Markell & Milus 2008). Isolates representing this of each isolate is available via Table S1, Supplementary new population showed a significant increase in aggres- material. siveness, that is, the ability to cause severe disease more quickly, especially at high temperature, compared to AFLP fingerprinting isolates collected before 2000 (Milus et al. 2006; Milus et al. 2008). A subset of 151 isolates representing all of the diversity In this study, we investigated P. striiformis f. sp. tritici with respect to virulence phenotype, region and sampling diversity at the global scale and tested a hypothesis of year was DNA fingerprinted by AFLP in Denmark. Spores recent intercontinental spread of wheat yellow rust as (10–20 mg) of each isolate were mixed with equal amounts opposed to local evolution of similar virulence phenotypes. of acid-washed sand and ground with two steel balls Representative subsets of past and present isolates from (5 mm in diameter) in a Geno/Grinder 2000 at 1500 Europe, North America and Australia were selected strokes/min for 3 × 30 s followed by DNA extraction according to origin and virulence phenotype. These samples (Justesen et al. 2002). The AFLP procedure was carried out represented the majority of diversity in virulence pheno- as described previously (Hovmøller & Justesen 2007b). All type in the fungus since the mid-1970s in these regions. isolates were analysed with nine primer combinations, Additional random samples were collected from areas which were selected in a preliminary screening to be the in Central, West and South Asia, the Arabian Peninsula most informative and to give fingerprints of high quality: and northeast Africa (Red Sea Area), representing diverse P11(AA)/M13(AG), P12(AC)/M26(TT), P16(CC)/M14(AT), ecological niches in terms of agricultural practices, host P19(GA)/M24(TC), P19(GA)/M25(TG), P20(GC)/M11(AA), characteristics, precipitation and temperature regimes. P22(GT)/M15(CA), P22(GT)/M22(GT), and P26(TT)/ © 2008 The Authors Journal compilation © 2008 Blackwell Publishing Ltd GLOBAL SPREAD OF AGGRESSIVE WHEAT YELLOW RUST 3 Table 1 Collections and sources of Puccinia striiformis f. sp. tritici isolates Country Region Sampling period No. of isolates Sample reference Denmark North Europe (EU) 1993–2005 595 ⎫ ⎥ Eritrea ⎫ 2002–2005 111 ⎬ Red Sea Area (RS) ⎥ Yemen⎭ 2003, 2005 15 ⎥ Kazakhstan 2003 7 ⎬ Authors ⎫ ⎥ Kyrgistan⎬ Central Asia
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