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<I>Phytophthora Alni</I> University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers in Plant Pathology Plant Pathology Department 2-2013 Strong Genetic Differentiation Between North American and European Populations of Phytophthora alni subsp. uniformis Jaime Aguayo Université de Lorraine Gerard C. Adams University of Nebraska-Lincoln, [email protected] Fabien Halkett Université de Lorraine Mursel Catal Akdeniz University Claude Husson Université de Lorraine See next page for additional authors Follow this and additional works at: http://digitalcommons.unl.edu/plantpathpapers Part of the Other Plant Sciences Commons, Plant Biology Commons, and the Plant Pathology Commons Aguayo, Jaime; Adams, Gerard C.; Halkett, Fabien; Catal, Mursel; Husson, Claude; Nagy, Zoltán Á.; Hansen, Everett M.; Marçais, Benoît; and Frey, Pascal, "Strong Genetic Differentiation Between North American and European Populations of Phytophthora alni subsp. uniformis" (2013). Papers in Plant Pathology. 286. http://digitalcommons.unl.edu/plantpathpapers/286 This Article is brought to you for free and open access by the Plant Pathology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Plant Pathology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Jaime Aguayo, Gerard C. Adams, Fabien Halkett, Mursel Catal, Claude Husson, Zoltán Á. Nagy, Everett M. Hansen, Benoît Marçais, and Pascal Frey This article is available at DigitalCommons@University of Nebraska - Lincoln: http://digitalcommons.unl.edu/plantpathpapers/286 Population Biology Strong Genetic Differentiation Between North American and European Populations of Phytophthora alni subsp. uniformis Jaime Aguayo, Gerard C. Adams, Fabien Halkett, Mursel Catal, Claude Husson, Zoltán Á. Nagy, Everett M. Hansen, Benoît Marçais, and Pascal Frey First, third, fifth, eighth, and ninth authors: INRA, UMR1136, INRA, Université de Lorraine, Interactions Arbres-Micro-organismes, IFR110 EFABA, Centre INRA de Nancy, 54280 Champenoux, France; second author: Department of Plant Pathology, University of Nebraska, Lincoln; fourth author: Department of Plant Protection, Akdeniz University, Antalya, Turkey; sixth author: Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Hungary; and seventh author: Department of Botany and Plant Pathology, Oregon State University, Corvallis. Accepted for publication 15 October 2012. ABSTRACT Aguayo, J., Adams, G. C., Halkett, F., Catal, M., Husson, C., Nagy, Z. Á., mating system of P. alni subsp. uniformis. Five new polymorphic micro- Hansen, E. M., Marçais, B., and Frey, P. 2013. Strong genetic differen- satellite markers were used to contrast both geographical populations. tiation between North American and European populations of Phytoph- The study comprised 71 isolates of P. alni subsp. uniformis collected thora alni subsp. uniformis. Phytopathology 103:190-199. from eight European countries and 10 locations in North America. Our results revealed strong differences between continental populations (Fst = Alder decline caused by Phytophthora alni has been one of the most 0.88; Rst = 0.74), with no evidence for gene flow. European isolates important diseases of natural ecosystems in Europe during the last 20 showed extremely low genetic diversity compared with the North Ameri- years. The emergence of P. alni subsp. alni—the pathogen responsible for can collection. Selfing appears to be the predominant mating system in the epidemic—is linked to an interspecific hybridization event between both continental collections. The results suggest that the European P. alni two parental species: P. alni subsp. multiformis and P. alni subsp. uni- subsp. uniformis population is most likely alien and derives from the formis. One of the parental species, P. alni subsp. uniformis, has been iso- introduction of a few individuals, whereas the North American population lated in several European countries and, recently, in North America. The probably is an indigenous population. objective of this work was to assess the level of genetic diversity, the population genetic structure, and the putative reproduction mode and Additional keywords: Alnus, oomycetes. Diseases that increase in severity or expand their range pose versely, some alien populations display high levels of genetic important threats to natural ecosystems (4,17,45). Although the diversity (30,54) as a result of multiple introductions (15,18). In- emergence of disease can be the result of changes in host or deed, to study the genetic changes that may have occurred during environmental conditions, or evolution in pathogen populations and after an introduction event, it is important to identify the (4), the introduction of exotic pathogens has been shown to be a source of the introduction with as much precision as possible. major cause (4,16,17,46). However, assessing whether the causal Moreover, knowledge of the mode of reproduction (sexual versus organism of an emerging disease is alien is not always straight- asexual) and the mating system (selfing versus outcrossing) is of forward (43,56). This results mostly from a lack of knowledge fundamental importance to the evolutionary biology of pathogens and data on the biodiversity and ecology of endemic species (6,34). The reproduction mode and the mating system will affect (17,43). For example, in the genus Phytophthora, low genetic how diversity is distributed within and among individuals in a variability has often been taken as an indication that specific popu- population (60), and supply insights into the potential of patho- lations are exotic (see Phytophthora quercina [13], P. n emo ro sa , gens to spread and on their ability to evolve (33). Indeed, in Phy- P. pseudosyringae [56], and P. pinifolia [22]). Indeed, intro- tophthora spp., asexual (zoospores) and sexual (oospores) pro- duction into a new geographical area often results in a population pagules exhibit contrasted dispersal and survival abilities, with with low variability (36,72) because founder effects caused by the strong epidemiological consequences. The source region will pro- migration of a limited number of individuals result in reduced vide the benchmark against which genetic and evolutionary gene diversity and number of alleles in introduced populations changes can be assessed, representing the variation from which (55). However, low variability cannot be taken as definite proof of the introduction was actually derived (18). For example, for P. the exotic nature of a population as long as the diversity center cinnamomi, Papua New Guinea has been proposed as the center has not been identified (33,43). Low genetic variability may occur of origin (19,36). Indeed, this population presented a higher in a native population, especially when selfing is suspected. It is allelic diversity compared with other populations (19,36). How- noteworthy that many Phytophthora spp. are homothallic and ever, determining the center of origin of a species is not always reproduce mainly by selfing (33,43). Self-fertilization will impact obvious. In the case of P. infestans, two possible centers of origin population genetic characteristics by increasing linkage dis- have been proposed: either Central Mexico (37) or the Andean equilibrium (LD) and reducing genetic diversity (33,43). Con- region of South America (35). Alder decline caused by the P. alni species complex is a good example of poorly understood pathogen emergence in a natural Corresponding author: P. Frey; E-mail address: [email protected] ecosystem (24,76). This disease has posed a major threat to natural ecosystems in Europe during the last 20 years (74). For http://dx.doi.org/10.1094/ PHYTO-05-12-0116-R © 2013 The American Phytopathological Society example, in eastern France, disease prevalence has reached 17% 190 PHYTOPATHOLOGY of riparian alder (Alnus glutinosa) trees (76). The emergence of richment step, data analysis, and automated primer design were this disease is linked to an interspecific hybridization event (9,47). described previously by Malausa et al. (58). The enriched micro- Recent studies have clarified the genesis of the interspecific hy- satellite library generated a total of 34,483 microsatellite se- brid P. alni subsp. alni. P. alni subsp. uniformis and P. alni subsp. quences, with 550 putative microsatellite loci identified. Choice multiformis, initially identified as genetic variants of P. alni of microsatellite loci for further tests was constrained to motifs of subsp. alni (9), were shown to be the parental species of the ≥2 bp in length and a minimum repeat number of 5. Using these hybrid (47). The hybrid P. alni subsp. alni is more aggressive than criteria, 110 loci were further retained. These 110 primer pairs its progenitors and is responsible for disease outbreak (73). were tested for amplification on a panel of 10 P. alni subsp. However, it is not known when and where hybridization took uniformis, 10 P. alni subsp. multiformis, and 5 P. alni subsp. alni place. Moreover, the origin of the parental species, P. alni subsp. European isolates. No North American P. alni subsp. uniformis uniformis and P. alni subsp. multiformis, remains unknown. isolates were available when loci were tested. Microsatellite loci P. alni subsp. alni is widespread in Europe and has not been were amplified in a GeneAmp polymerase chain reaction (PCR) identified elsewhere. Although P. alni subsp. multiformis has been System 9700 Thermal
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