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Variation Inphytophthora Infestans Variation inPhytophthora infestans -sourcesan dimplications - Promotor: Prof.dr . R.F.Hoekstra , Hoogleraar ind e Genetica,i.h.b . depopulatie - en kwantitatieve genetica,Wageninge n Universiteit Copromotoren: Dr. ir. L.J.Turkenstee n Senior onderzoeker, Plant Research International Prof.dr . W.E.Fry , Plant Pathology Professor, Cornell University, Ithaca, NY,US A Promotiecommissie: Prof.dr . M.J.Jege r Huxley School of Imperial College,U K Dr. D.S. Shaw School of Biological Sciences, University of Wales,U K Prof.dr . ir. P.Sta m Wageningen Universiteit Prof.dr . ir. P.C.Strui k Wageningen Universiteit W HN(W^ . Wilbert Flier Variation inPhytophthora infestans -sourcesan dimplications - Proefschrift Terverkrijgin g vand egraa dva ndocto r op gezagva n derecto r magnificus vanWageninge n Universiteit, Prof,d r ir L.Speelman , in hetopenbaa r teverdedige n op dinsdag 5jun i 2001 desnamiddag so m 16.00 uur in deAul a ibtbddi CIP-DATA KONINKUJKEBIBLIOTHEEK , DENHAA G Flier,W.G. ,200 1 Variation inPhytophthora infestans, sourcesan d implications. PhDthesi sWageninge n University, Wageningen,th e Netherlands - With references - With summary inDutch . ISBN:9 0 580842 05 Subject headings: Potato late blight / Solatium tuberosum I genetic variation / pathogenicity / stability of disease resistance Typeset in 10/14pt Frutiger 45. Printed by Ponsen& Looyen BV,Wageninge n The research described in this thesis (September 1996 - December 2000) was conducted at Plant Research International, Wageningen, the Netherlands and at PICTIPAPA (Programa Internacional Cooperative del Tiz6n Tardio de la Papa), Metepec, Estado de Mexico, Mexico. A PLANT RESEARCH INTERNATIONAL Stellingen De effectiviteit van partiele resistentie in aardappelen tegenPhytophthora infestansword t negatief beinvloed door de toegenomen agressiviteit van isolaten en het optreden van rasx isolaa t interacties. dit proefschrift In tegenstelling tot seks bij mensen leidt seksuele reproductie bij Phytophthora infestansto t opwinding achteraf. dit proefschrift Ook duurzame resistenties hebben een uiterste houdbaarheidsdatum. In het licht van de huidige problemen met de Phytophthora-bestrijdlng kan men de biologische teelt van aardappelen beschouwen als een luxe probleem. 'Everyone isa reductionis t about subjectstha t they do not understand' Andrew Brown (1999). The Darwin Wars, Simon & Schuster, London,UK (p. 48) Integrale invoering van de 'mahana''-benadering in het projectmanagement kan een bedrage leveren aan het voorkomen van het zogenaamde 'burn-out syndroom'. ' vrijnaar Hector Lozoya-Saldaha, technisch directeurPICTIPAPA, Mexico. Wageningen Universiteit heeft samen met haar oude identiteit en brede vakkenpakket ook haar bestaansrechtverloren . Het verhogen van de minimum snelheid op rijkswegen tot 100 km/uur verhoogt deveilighei d vanweggebruikers . Voor mijn ouders;Ari e en Lijntje Abstract Flier,W.G. , 2001. Variation inPhytophthora infestans, sourcesan d implications.Ph D Thesis,Wageninge n University,th e Netherlands. The oomycete pseudofungus Phytophthora infestans (Mont.) de Bary, the causal organism of late blight, is considered to be one of the most devastating pathogens affecting potatoes and tomatoes worldwide. In Europe, the pathogen caused severe epidemics on potatoes after its introduction in 1845. Late blight management became much more troublesome after the introduction of another P. infestanspopulatio n of Mexican origin. The present population of P. infestans in the Netherlands and an increasing number of other Europeancountrie s consistso f bothA 1 andA 2 mating type isolates and sexual reproduction has been reported. The goals of this thesis were to study late blight epidemiology and population biology of the present P. infestans population. Therefore, sources and patterns of variation for pathogenicity in sexual P. infestans populations were studied and the impact of increased levelso f aggressiveness on the stability of partial resistance to late blight was investigated. Results showed that considerable levelso f variationfo r aggressiveness are maintained in regional populations of P. infestansi n the Netherlands and that oospores are readily produced in field crops and volunteer potato plants. Oospore production and viability proved to be highly dependent on combining abilities of parental strains and there are indications that oospores areabl et o survive in soilsfo r three to four years. Increasedaggressivenes s and cultivar-by-isolate interactions between partial resistant potato cultivars andP. infestans strains negatively affect the stabilityo f resistance. Population genetic studies in itscentr e of origin and diversity revealed differentiation within the Toluca Valley implying host specificity. From the results presented in this thesis, it isclea r that the introduction of a sexually reproducing population of P. infestans in the Netherlands has had a major impact on late blight epidemics and population biology of the late blight pathogen. Sexual reproduction has therefore led to a genetically more diverse population of P. infestans in the Netherlands that is marked by an increased adaptability to host and environment. Contents General introduction Section I 2 Variation intube r pathogenicity of Phytophthorainfestans i nth e Netherlands 9 3 Foliar aggressiveness of Phytophthorainfestans inthre e potato growing regions inth e Netherlands 21 Section II 4 Production,surviva l and infectivity of oospores of Phytophthorainfestans 33 5 Formation,productio n and viability of oosporeso f Phytophthorainfestans from potato andSolanum demissum inth e Toluca Valley,centra l Mexico 49 Section III 6 Differential interaction of Phytophthorainfestans on tubers of potato cultivars with different levelso f blight resistance 69 7 Stability of partial resistance in potato cultivars exposedt o aggressive strains of Phytophthorainfestans 87 Section IV 8 Influence of host and management on the population structure ofPhytophthora infestans within the Toluca Valley of central Mexico 109 9 Thepopulatio n structure of Phytophthorainfestans fro m the Toluca Valley in central Mexicosuggest s genetic differentiation between populations from cultivated potato 135 andwil d Solanum species 10 Phytophthoraipomoeae, a ne w homothallic speciescausin g leaf blight on Ipomoea longipedunculatai nth e Toluca Valley of central Mexico 151 11 Summarising discussion 169 Samenvattendediscussi e 177 References 185 Nawoord 199 Curriculum vitae 201 Listo f publications 203 1 General introduction Chapter 1 Thepotato lateblight pathogen Theoomycet e Phytophthora infestans (Mont.) de Bary(d e Bary, 1876), the causeo f late blight in potatoes and tomatoes, is considered to be among the most important pathogens of potato crops worldwide (Hooker, 1981). The pathogen is feared by farmers around the globe through its ability to destroy entire fields of potatoes and tomatoes in a few weeks time. The pathogen affects both foliage and stems, reducing the photosynthetic capacity of the crop and therefore leading to tuber yield reduction. Inaddition ,P. infestans can infect fruits andtubers ,whic h will add upt o the total losses in marketable yield. Phytophthorainfestans belong s to a select group of plant pathogens that have the dubious honour of being a direct cause of sociological and political changes in the recent history of mankind. It is thought that P. infestans originated and co-evolved on native wild tuber bearing Solanum species in the central highlands of Mexico (Reddick, 1939). Farmers in European d NorthAmeric a were unaware of itsexistenc e untilth efirs t reports of a mysterious disease of potatoes appeared in newspapers and scientific journals in Europe and northern North America. When late blight appeared in England in 1845, John Lindley (editor of the Gardener's Chronicle and Agricultural Gazette) wrote, "...the disease consists ina gradual decay of theleaves andstem, which become aputrid mass, and the tubers areaffected by degrees ina similar way. The first obvious signis the appearance on the edgeof the leafof ablack spot whichgradually spreads; the gangrene then attacks the haulms, and in a few days the latter are decayed, emitting apeculiar and rather offensive odour".Devastatin g late blight epidemics swept through European ddestroye d potato crops in Irelanddurin g 1845an d 1846,whic h left the Irish population in poverty andstarvation .Thi sblac k episode in Irish history catalysed the massemigratio n of people to North America and became known asth e Irish potato famine. More recently, severeP. infestans epidemics destroyed potato crops in Germany in 1917 during the First World War. Priority was given to supply the German army, which at that time wasengage d ina wa r of attrition inth e trenches of NorthernFrance . Back home in Germany, civilians starved and when news about the poor situation reached the Western front, it demoralized the German troops. The shortage of food in Germany during the winter of 1917-1918 became known as the"Steckrubenwinter" (Heddergott, 1957). It has been argued that the shortage in food greatly attributed to the internal instability of the German Empire in 1918 and thus accelerated the end of the GreatWa r (Schumann, 1991). Inou r days,cro p lossesdu et o late blight have beenestimate d to account for 10 to 15 percent of the total global annual potato production (Anonymous, 1996). The economic value of the crop lost plusth e costs of crop protection amount to 3 billionU S $ annually (Duncan, 1999). In the developed world, control of potato late
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