Reconstruction of the Sudden Oak Death epidemic in California through microsatellite analysis of the pathogen Phytophthora ramorum

The genetic structure of the clonally reproducing Sudden Oak Death (SOD) pathogen in California was investigated using seven variable microsatellites. A total of 35 multilocus genotypes were identified among 292 samples representative of populations from 14 forest sites and of the nursery trade. amova indicated significant genetic variability both within (44.34%) and among populations (55.66%). Spatial autocorrelation analyses indicated that Moran's index of similarity reached a minimum of 0.1 at 350 m, increased to 0.4 at 1500 m and then decreased to zero at 10 km. These results suggest a bimodal pattern of spread, with medium range dispersal (1500–10 000 m) putatively attributed to the presence of strong winds. Lack of genetic structure was identified for three groups of populations. One group notably included the nurseries’ population and two forest populations, both linked to early reports of the pathogen. A neighbour‐joining analysis based on pairwise ΦST values indicated that the clade inclusive of the nurseries’ populations is basal to all California populations. A network analysis identified three common genotypes as the likely founders of the California infestation and proposes a stepwise model for local evolution of novel genotypes. This was supported by the identification in the same locations of novel genotypes and of their 1‐ or 2‐step parents. We hypothesize that the few undifferentiated population groups indicate historical human spread of the pathogen, while the general presence of genetically structured populations indicates that new infestations are currently generated by rare medium or long‐range natural movement of the pathogen, followed by local generation of new genotypes.

[1]  D. Aylor,et al.  Relationship between aerial concentration of Venturia inaequalis ascospores and development of apple scab , 1993 .

[2]  Yves Van de Peer,et al.  zt: A Sofware Tool for Simple and Partial Mantel Tests , 2002 .

[3]  L. Stone,et al.  The checkerboard score and species distributions , 1990, Oecologia.

[4]  D. Rizzo,et al.  Non-oak native plants are main hosts for sudden oak death pathogen in California , 2003 .

[5]  R. Sokal.  A Phylogenetic Analysis of the Caminalcules. IV. Congruence and Character Stability , 1983 .

[6]  C. Tyler-Smith,et al.  Signature of recent historical events in the European Y-chromosomal STR haplotype distribution , 2005, Human Genetics.

[7]  O. Hardy,et al.  spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels , 2002 .

[8]  D. Rizzo,et al.  A California-Based Chronological Review (1995-2004) of Research on Phytophora ramorum , the Causal Agent of Sudden Oak Death , 2005 .

[9]  N Mantel,et al.  A technique of nonparametric multivariate analysis. , 1970, Biometrics.

[10]  L. Excoffier,et al.  Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. , 1994, Genetics.

[11]  R. Sokal.  Society of Systematic Biologists A Phylogenetic Analysis of the Caminalcules , 2010 .

[12]  E. Davison.  Phytophthora Diseases Worldwide , 1998 .

[13]  H. Schulenburg,et al.  A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level , 2004, Molecular ecology.

[14]  R. Sokal,et al.  Spatial autocorrelation in biology: 1. Methodology , 1978 .

[15]  Laura Baxter,et al.  Phytophthora Genome Sequences Uncover Evolutionary Origins and Mechanisms of Pathogenesis , 2006, Science.

[16]  Robert R. Sokal,et al.  Local spatial autocorrelation in biological variables , 1998 .

[17]  E. Hansen,et al.  Sudden Oak Death Caused by Phytophthora ramorum in Oregon. , 2002, Plant disease.

[18]  David M Rizzo,et al.  Transmission of Phytophthora ramorum in Mixed-Evergreen Forest in California. , 2005, Phytopathology.

[19]  D. Rizzo,et al.  AFLP and phylogenetic analyses of North American and European populations of Phytophthora ramorum. , 2004, Mycological research.

[20]  E. Hansen,et al.  First Report of A1 Mating Type of Phytophthora ramorum in North America. , 2003, Plant Disease.

[21]  I. Tommerup,et al.  Non-Mendelian inheritance revealed in a genetic analysis of sexual progeny of Phytophthora cinnamomi with microsatellite markers. , 2002, Fungal genetics and biology : FG & B.

[22]  H. Förster,et al.  Phytophthora sojae races have arisen by clonal evolution and by rare outcrosses. , 1994 .

[23]  J. Diniz‐Filho,et al.  Spatial Autocorrelation Analysis and the Identification of Operational Units for Conservation in Continuous Populations , 2002 .

[24]  Ross K. Meentemeyer,et al.  Mapping the risk of establishment and spread of sudden oak death in California , 2004 .

[25]  P. Bonants,et al.  A Rapid Diagnostic Test to Distinguish Between American and European Populations of Phytophthora ramorum. , 2004, Phytopathology.

[26]  David M. Rizzo,et al.  Sudden Oak Death and Associated Diseases Caused by Phytophthora ramorum , 2003 .

[27]  Shuijin Hu,et al.  Effect of prior tillage and soil fertility amendments on dispersal of Phytophthora capsici and infection of pepper , 2008, European Journal of Plant Pathology.

[28]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[29]  N. Grünwald,et al.  First Report of the European Lineage of Phytophthora ramorum on Viburnum and Osmanthus spp. in a California Nursery. , 2008, Plant disease.

[30]  M. Garbelotto,et al.  Microsatellite markers identify three lineages of Phytophthora ramorum in US nurseries, yet single lineages in US forest and European nursery populations , 2006, Molecular ecology.

[31]  M. Nei,et al.  Estimation of average heterozygosity and genetic distance from a small number of individuals. , 1978, Genetics.

[32]  R. Molina,et al.  Spatial analysis of within-population microsatellite variability reveals restricted gene flow in the Pacific golden chanterelle (Cantharellus formosus) , 2006, Mycologia.

[33]  F. Rousset,et al.  AN EXACT TEST FOR POPULATION DIFFERENTIATION , 1995, Evolution; international journal of organic evolution.

[34]  David M. Rizzo,et al.  Sudden oak death: endangering California and Oregon forest ecosystems , 2003 .

[35]  C. Brasier,et al.  Production of gametangia by Phytophthora ramorum in vitro. , 2004, Mycological research.

[36]  Dennis A. Johnson,et al.  Survival of detached sporangia ofPhytophthora infestans exposed to ambient, relatively dry atmospheric conditions , 2002, American Journal of Potato Research.

[37]  D. Rizzo,et al.  Phytophthora ramorum as the Cause of Extensive Mortality of Quercus spp. and Lithocarpus densiflorus in California. , 2002, Plant disease.

[38]  Laurent Excoffier,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[39]  L. Stone,et al.  Generating uniformly distributed random networks. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[40]  Peter J. M. Bonants,et al.  Phytophthora ramorum sp. nov., a new pathogen on Rhododendron and Viburnum , 2001 .

[41]  Aerial dispersal and drying of Peronospora tabacina conidia in tobacco shade tents. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[42]  R. Sokal,et al.  A simulation study of microevolutionary inferences by spatial autocorrelation analysis , 1997 .

[43]  David M. Rizzo,et al.  Establishment of an emerging generalist pathogen in redwood forest communities , 2005 .

[44]  D. Aylor,et al.  Biophysical scaling and the passive dispersal of fungus spores: relationship to integrated pest management strategies , 1999 .

[45]  E. Hansen,et al.  Population dynamics of the sudden oak death pathogen Phytophthora ramorum in Oregon from 2001 to 2004 , 2007, Molecular ecology.

[46]  S. Prospero,et al.  Isolation and characterization of microsatellite markers in Phytophthora ramorum, the causal agent of sudden oak death , 2004 .

[47]  David M Rizzo,et al.  Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. , 2005, Annual review of phytopathology.