Phylogeography, origin and population structure of the self-fertile emerging plant pathogen Phytophthora pseudosyringae
Jazyk angličtina Země Velká Británie, Anglie Médium print
Typ dokumentu časopisecké články
Grantová podpora
Biodiversa+
EU project POnTE (Pest Organisms Threatening Europe)
CZ.02.1.01/0.0/0.0/15_003/0000453
European Regional Development Fund
PubMed
38590129
PubMed Central
PMC11002350
DOI
10.1111/mpp.13450
Knihovny.cz E-zdroje
- Klíčová slova
- forest pathogen, homothallic, invasive pathogen, migration, outcrossing, population genetics,
- MeSH
- fylogeografie MeSH
- lidé MeSH
- nemoci rostlin MeSH
- Phytophthora * genetika MeSH
- rostliny MeSH
- stromy MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
Phytophthora pseudosyringae is a self-fertile pathogen of woody plants, particularly associated with tree species from the genera Fagus, Notholithocarpus, Nothofagus and Quercus, which is found across Europe and in parts of North America and Chile. It can behave as a soil pathogen infecting roots and the stem collar region, as well as an aerial pathogen infecting leaves, twigs and stem barks, causing particular damage in the United Kingdom and western North America. The population structure, migration and potential outcrossing of a worldwide collection of isolates were investigated using genotyping-by-sequencing. Coalescent-based migration analysis revealed that the North American population originated from Europe. Historical gene flow has occurred between the continents in both directions to some extent, yet contemporary migration is overwhelmingly from Europe to North America. Two broad population clusters dominate the global population of the pathogen, with a subgroup derived from one of the main clusters found only in western North America. Index of association and network analyses indicate an influential level of outcrossing has occurred in this preferentially inbreeding, homothallic oomycete. Outcrossing between the two main population clusters has created distinct subgroups of admixed individuals that are, however, less common than the main population clusters. Differences in life history traits between the two main population clusters should be further investigated together with virulence and host range tests to evaluate the risk each population poses to natural environments worldwide.
Agrobioinstitute Agricultural Academy Sofia Bulgaria
Department of Agricultural and Forest Sciences and Engineering University of Lleida Lleida Spain
Department of Agricultural Sciences University of Sassari Sassari Italy
Department of Botany and Plant Pathology Oregon State University Corvallis Oregon USA
Department of Cell and Molecular Biology Uppsala University Uppsala Sweden
Department of Plant Pathology UC Davis Davis California USA
Division of Biotechnology and Plant Health Norwegian Institute of Bioeconomy Research Ås Norway
Flanders Research Institute for Agriculture Fisheries and Food Plant Sciences Unit Merelbeke Belgium
Forest Research Alice Holt Lodge Farnham UK
Joint Research Unit CTFC AGROTECNIO CERCA Lleida Spain
National Bioinformatics Infrastructure Sweden Science for Life Laboratory Sweden
USDA ARS Mycology and Nematology Genetic Diversity and Biology Laboratory Beltsville Maryland USA
Zobrazit více v PubMed
Abdellaoui, A. , Hottenga, J.‐J. , Knijff, P.d. , Nivard, M.G. , Xiao, X. , Scheet, P. et al. (2013) Population structure, migration, and diversifying selection in the Netherlands. European Journal of Human Genetics, 21, 1277–1285. PubMed PMC
Aguayo, J. , Adams, G.C. , Halkett, F. , Catal, M. , Husson, C. , Nagy, Z.Á. et al. (2013) Strong genetic differentiation between north American and European populations of Phytophthora alni subsp. uniformis . Phytopathology, 103, 190–199. PubMed
Anonymous . (2006) California plant pest and disease report. California Department of Food and Agriculture, Sacramento, 23, 37–42.
Beales, P.A. , Giltrap, P.M. , Webb, K.M. & Ozolina, A. (2010) A further threat to UK heathland bilberry (Vaccinium myrtillus) by Phytophthora pseudosyringae . Plant Pathology, 59, 406.
Beerli, P. & Felsenstein, J. (1999) Maximum‐likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics, 152, 763–773. PubMed PMC
Beerli, P. & Felsenstein, J. (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences of the United States of America, 98, 4563–4568. PubMed PMC
Beerli, P. , Mashayekhi, S. , Sadeghi, M. , Khodaei, M. & Shaw, K. (2019) Population genetic inference with MIGRATE. Current Protocols in Bioinformatics, 68, e87. PubMed PMC
Beerli, P. & Palczewski, M. (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics, 185, 313–326. PubMed PMC
Bertier, L. , Leus, L. , D'hondt, L. , Cock, A.W.A.M.d. & Höfte, M. (2013) Host adaptation and speciation through hybridization and polyploidy in Phytophthora . PLoS One, 8, e85385. PubMed PMC
Bhat, R.G. , McBlain, B.A. & Schmitthenner, A.F. (1993) The inheritance of resistance to metalaxyl and to fluorophenylalanine in matings of homothallic Phytophthora sojae . Mycological Research, 97, 865–870.
Bhat, R.G. & Schmitthenner, A.F. (1993) Genetic crosses between physiologic races of Phytophthora sojae . Experimental Mycology, 17, 122–129.
Bily, D. , Nikolaeva, E. , Olson, T. & Kang, S. (2022) Phytophthora spp. associated with Appalachian oak forests and waterways in Pennsylvania, with P. abietivora as a pathogen of five native woody plant species. Plant Disease, 106, 1143–1156. PubMed
Bourret, T.B. , Mehl, H.K. , Aram, K. & Rizzo, D.M. (2023) Rhododendron leaf baiting of coastal California watersheds for Phytophthora and Nothophytophthora . Mycological Progress, 22, 62.
Boyer, F. , Mercier, C. , Bonin, A. , Le Bras, Y. , Taberlet, P. & Coissac, E. (2016) obitools: a unix‐inspired software package for DNA metabarcoding. Molecular Ecology Resources, 16, 176–182. PubMed
Brasier, C. & Webber, J. (2010) Sudden larch death. Nature, 466, 824–825. PubMed
Bregant, C. , Rossetto, G. , Meli, L. , Sasso, N. , Montecchio, L. , Brglez, A. et al. (2023) Diversity of Phytophthora species involved in new diseases of mountain vegetation in Europe with the description of Phytophthora pseudogregata sp. nov. Forests, 14, 1515.
Brown, A.H.D. , Feldman, M.W. & Nevo, E. (1980) Multilocus structure of natural populations of Hordeum spontaneum . Genetics, 96, 523–536. PubMed PMC
Burgess, T.I. (2015) Molecular characterization of natural hybrids formed between five related indigenous clade 6 Phytophthora species. PLoS One, 10, e0134225. PubMed PMC
Calus, M.P.L. & Vandenplas, J. (2018) SNPrune: an efficient algorithm to prune large SNP array and sequence datasets based on high linkage disequilibrium. Genetics, Selection, Evolution, 50, 34. PubMed PMC
Černý, K. (2016) Nepůvodní invazní patogeny dřevin – výzva, nebo předem ztracený boj? [Non‐indigenous invasive pathogens of woody plants – a challenge, or a battle already lost?]. Živa, 6, 286–291.
Chang, C.C. , Chow, C.C. , Tellier, L.C. , Vattikuti, S. , Purcell, S.M. & Lee, J.J. (2015) Second‐generation PLINK: rising to the challenge of larger and richer datasets. GigaScience, 4, s13742‐015‐0047‐8. PubMed PMC
Charlesworth, D. (2003) Effects of inbreeding on the genetic diversity of populations. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358, 1051–1070. PubMed PMC
Christova, P.K. , Lyubenova, A.B. , Kostov, K.V. & Slavov, S.B. (2019) First report of Phytophthora pseudosyringae recovered from aquatic ecosystems in Bulgaria. Forest Pathology, 49, e12505.
Cooke, D.E.L. , Jung, T. , Williams, N.A. , Schubert, R. , Oßwald, W. & Duncan, J.M. (2005) Genetic diversity of European populations of the oak fine‐root pathogen Phytophthora quercina . Forest Pathology, 35, 57–70.
Danecek, P. , Auton, A. , Abecasis, G. , Albers, C.A. , Banks, E. , DePristo, M.A. et al. (2011) The variant call format and VCFtools. Bioinformatics, 27, 2156–2158. PubMed PMC
Day, W.R. (1938) Root‐rot of sweet chestnut and beech caused by species of Phytophthora I. Cause and symptoms of disease: its relation to soil conditions. Forestry, 12, 101–116.
Declercq, B. , Van Buyten, E. , Claeys, S. , Cap, N. , De Nies, J. , Pollet, S. et al. (2010) Molecular characterization of Phytophthora porri and closely related species and their pathogenicity on leek (Allium porrum). European Journal of Plant Pathology, 127, 341–350.
Denman, S. , Rose, J . & Slippers, B. (2009) Phytophthora pseudosyringae found on European beech and hornbeam trees in the UK. In: Goheen, E.M. & Frankel, S.J. (Eds.) Proceedings of the fourth meeting of the IUFRO working party S07.02.09: Phytophthoras in forests and natural ecosystems. General Technical Report PSW‐GTR‐221. Albany, CA, USA: USDA Forest Service, pp. 273–280.
Dick, M.A. , Williams, N.M. , Bader, M.K.‐F. , Gardner, J.F. & Bulman, L.S. (2014) Pathogenicity of Phytophthora pluvialis to Pinus radiata and its relation with red needle cast disease in New Zealand. New Zealand Journal of Forestry Science, 44, 6.
Elshire, R.J. , Glaubitz, J.C. , Sun, Q. , Poland, J.A. , Kawamoto, K. , Buckler, E.S. et al. (2011) A robust, simple genotyping‐by‐sequencing (GBS) approach for high diversity species. PLoS One, 6, e19379. PubMed PMC
Erwin, D.C. & Ribeiro, O.K. (1996) Phytophthora diseases worldwide. St Paul, MN: APS Press.
Evanno, G. , Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620. PubMed
Fajardo, S.N. , Valenzuela, S. , Dos Santos, A.F. , González, M.P. & Sanfuentes, E.A. (2017) Phytophthora pseudosyringae associated with the mortality of Nothofagus obliqua in a pure stand in central‐southern Chile. Forest Pathology, 47, e12361.
Falush, D. , Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567–1587. PubMed PMC
Feau, N. , Mcdonald, M. , Van Der Meer, B. , Zhang, Y. , Herath, P. & Hamelin, R.C. (2022) Phytophthora species associated with red alder dieback in British Columbia, Canada. Canadian Journal of Plant Pathology, 44, 549–558.
Förster, H. , Tyler, B.M. & Coffey, M.D. (1994) Phytophthora sojae races have arisen by clonal evolution and by rare outcrosses. Molecular Plant‐Microbe Interactions, 7, 780.
Francis, D.M. & St. Clair, D.A. (1993) Outcrossing in the homothallic oomycete, Pythium ultimum, detected with molecular markers. Current Genetics, 24, 100–106. PubMed
Francis, D.M. & St. Clair, D.A. (1997) Population genetics of Pythium ultimum . Phytopathology, 87, 454–461. PubMed
González, M.P. , Mizubuti, E.S.G. , Gonzalez, G. & Sanfuentes, E.A. (2024) Uncovering the hidden hosts: identifying inoculum reservoirs for Phytophthora pseudosyringae in Nothofagus forests in Chile. Plant Pathology. Available from: 10.1111/ppa.13855 DOI
Goodwin, S.B. (1997) The population genetics of Phytophthora . Phytopathology, 87, 462–473. PubMed
Goss, E.M. , Carbone, I. & Grünwald, N.J. (2009) Ancient isolation and independent evolution of the three clonal lineages of the exotic sudden oak death pathogen Phytophthora ramorum . Molecular Ecology, 18, 1161–1174. PubMed
Goss, E.M. , Larsen, M. , Vercauteren, A. , Werres, S. , Heungens, K. & Grünwald, N.J. (2011) Phytophthora ramorum in Canada: evidence for migration within North America and from Europe. Phytopathology, 101, 166–171. PubMed
Goudet, J. (2005) Hierfstat, a package for R to compute and test hierarchical F‐statistics. Molecular Ecology Notes, 5, 184–186.
Green, S. , Riddell, C.E. , Frederickson‐Matika, D. , Armstrong, A. , Elliot, M. , Forster, J. et al. (2020) Diversity of woody‐host infecting Phytophthora species in public parks and botanic gardens as revealed by metabarcoding, and opportunities for mitigation through best practice. Sibbaldia, 18, 67–88.
Grünwald, N.J. , Garbelotto, M. , Goss, E.M. , Heungens, K. & Prospero, S. (2012) Emergence of the sudden oak death pathogen Phytophthora ramorum . Trends in Microbiology, 20, 131–138. PubMed
Hansen, E.M. , Goheen, D.J. , Jules, E.S. & Ullian, B. (2000) Managing Port‐Orford‐cedar and the introduced pathogen Phytophthora lateralis . Plant Disease, 84, 4–14. PubMed
Hansen, E.M. , Reeser, P.W. & Sutton, W. (2017) Ecology and pathology of Phytophthora ITS clade 3 species in forests in western Oregon, USA. Mycologia, 109, 100–114. PubMed
Hereford, J. (2009) A quantitative survey of local adaptation and fitness trade‐offs. The American Naturalist, 173, 579–588. PubMed
Herten, K. , Hestand, M.S. , Vermeesch, J.R. & Van Houdt, J.K. (2015) GBSX: a toolkit for experimental design and demultiplexing genotyping by sequencing experiments. BMC Bioinformatics, 16, 73. PubMed PMC
Hüberli, D. , Hardy, G.E.S.J. , White, D. , Williams, N. & Burgess, T.I. (2013) Fishing for Phytophthora from Western Australia's waterways: a distribution and diversity survey. Australasian Plant Pathology, 42, 251–260.
Huson, D.H. & Bryant, D. (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254–267. PubMed
Hwang, J. , Jeffers, S.N. & Oak, S.W. (2007) Occurrence and distribution of Phytophthora pseudosyringae in forest streams of North Carolina. Phytopathology, 97, S49.
Ingrouille, M. (2012) Historical ecology of the British flora. Dordrecht, Netherlands: Springer Science & Business Media.
Jankowiak, R. , Stępniewska, H. , Bilański, P. & Taerum, S.J. (2023) Phytophthora species cause sudden and severe decline of naturally regenerated European beech (Fagus sylvatica) seedlings. Plant Pathology, 72, 774–785.
Jombart, T. & Ahmed, I. (2011) Adegenet 1.3‐1: new tools for the analysis of genome‐wide SNP data. Bioinformatics, 27, 3070–3071. PubMed PMC
Jombart, T. & Collins, C. (2015) A tutorial for discriminant analysis of principal components (DAPC) using adegenet 2.0. 0. https://adegenet.r‐forge.r‐project.org/files/tutorial‐dapc.pdf [Accessed 15th March 2024].
Jombart, T. , Devillard, S. & Balloux, F. (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics, 11, 94. PubMed PMC
Judelson, H.S. (2009) Sexual reproduction in oomycetes: biology, diversity, and contributions to fitness. In: Lamour, K. & Kamoun, S. (Eds.) Oomycete genetics and genomics: diversity, interactions and research tools. Hoboken, NJ, USA: John Wiley & Sons, pp. 121–138.
Jung, T. (2009) Beech decline in central Europe driven by the interaction between Phytophthora infections and climatic extremes. Forest Pathology, 39, 73–94.
Jung, T. , Chang, T.T. , Bakonyi, J. , Seress, D. , Pérez‐Sierra, A. , Yang, X. et al. (2017) Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathology, 66, 194–211.
Jung, T. , Durán, A. , Sanfuentes von Stowasser, E. , Schena, L. , Mosca, S. , Fajardo, S. et al. (2018) Diversity of Phytophthora species in Valdivian rainforests and association with severe dieback symptoms. Forest Pathology, 48, e12443.
Jung, T. , Hansen, E.M. , Winton, L. , Oßwald, W. & Delatour, C. (2002) Three new species of Phytophthora from European oak forests. Mycological Research, 106, 397–411.
Jung, T. , Nechwatal, J. , Cooke, D.E.L. , Hartmann, G. , Blaschke, M. , Oßwald, W.F. et al. (2003) Phytophthora pseudosyringae sp. nov., a new species causing root and collar rot of deciduous tree species in Europe. Mycological Research, 107, 772–789. PubMed
Jung, T. , Orlikowski, L. , Henricot, B. , Abad‐Campos, P. , Aday, A.G. , Aguín Casal, O. et al. (2016) Widespread Phytophthora infestations in European nurseries put forest, semi‐natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology, 46, 134–163.
Jung, T. , Pérez‐Sierra, A. , Durán, A. , Jung, M.H. , Balci, Y. & Scanu, B. (2018) Canker and decline diseases caused by soil‐ and airborne Phytophthora species in forests and woodlands. Persoonia, 40, 182–220. PubMed PMC
Kamvar, Z.N. , Brooks, J.C. & Grünwald, N.J. (2015) Novel R tools for analysis of genome‐wide population genetic data with emphasis on clonality. Frontiers in Genetics, 6, 208. PubMed PMC
Kamvar, Z.N. , Tabima, J.F. & Grünwald, N.J. (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2, e281. PubMed PMC
Knaus, B.J. & Grünwald, N.J. (2017) vcfr: a package to manipulate and visualize variant call format data in R. Molecular Ecology Resources, 17, 44–53. PubMed
Kopelman, N.M. , Mayzel, J. , Jakobsson, M. , Rosenberg, N.A. & Mayrose, I. (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15, 1179–1191. PubMed PMC
Li, H. (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA‐MEM. arXiv:1303.3997 [Preprint].
Li, H. , Handsaker, B. , Wysoker, A. , Fennell, T. , Ruan, J. , Homer, N. et al. (2009) The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078–2079. PubMed PMC
Liebhold, A.M. , Brockerhoff, E.G. , Garrett, L.J. , Parke, J.L. & Britton, K.O. (2012) Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Frontiers in Ecology and the Environment, 10, 135–143.
Linzer, R.E. , Rizzo, D.M. , Cacciola, S.O. & Garbelotto, M. (2009) AFLPs detect low genetic diversity for Phytophthora nemorosa and P. pseudosyringae in the US and Europe. Mycological Research, 113, 298–307. PubMed
Malomane, D.K. , Reimer, C. , Weigend, S. , Weigend, A. , Sharifi, A.R. & Simianer, H. (2018) Efficiency of different strategies to mitigate ascertainment bias when using SNP panels in diversity studies. BMC Genomics, 19, 22. PubMed PMC
Martin, F.N. & Tooley, P.W. (2003) Phylogenetic relationships of Phytophthora ramorum, P. nemorosa, and P. pseudosyringae, three species recovered from areas in California with sudden oak death. Mycological Research, 107, 1379–1391. PubMed
Martin, M. (2011) Cutadapt removes adapter sequences from high‐throughput sequencing reads. EMBnet.journal, 17, 10–12.
May, K.J. , Drenth, A. & Irwin, J.A.G. (2003) Interspecific hybrids between the homothallic Phytophthora sojae and Phytophthora vignae . Australasian Plant Pathology, 32, 353–359.
McDade, L. (1990) Hybrids and phylogenetic systematics I. Patterns of character expression in hybrids and their implications for cladistic analysis. Evolution, 44, 1685–1700. PubMed
McDade, L. (1992) Hybrids and phylogenetic systematics II. The impact of hybrids on cladistic analysis. Evolution, 46, 1329–1346. PubMed
McKeever, K.M. & Chastagner, G.A. (2016) A survey of Phytophthora spp. associated with Abies in U.S. Christmas tree farms. Plant Disease, 100, 1161–1169. PubMed
McKenna, A. , Hanna, M. , Banks, E. , Sivachenko, A. , Cibulskis, K. , Kernytsky, A. et al. (2010) The genome analysis toolkit: a MapReduce framework for analyzing next‐generation DNA sequencing data. Genome Research, 20, 1297–1303. PubMed PMC
Milgroom, M.G. (1996) Recombination and the multilocus structure of fungal populations. Annual Review of Phytopathology, 34, 457–477. PubMed
Monahan, W.B. , Tse, J. , Koenig, W.D. & Garbelotto, M. (2008) Mycological research news 1. Mycological Research, 112, 757–758.
Motta, E. , Annesi, T. , Pane, A. , Cooke, D.E.L. & Cacciola, S.O. (2003) A new Phytophthora sp. causing a basal canker on beech in Italy. Plant Disease, 87, 1005. PubMed
Mullett, M.S. , Van Poucke, K. , Haegeman, A. , Focquet, F. , Cauldron, N.C. , Knaus, B.J. et al. (2023) Phylogeography and population structure of the global, wide host‐range hybrid pathogen Phytophthora × cambivora . IMA Fungus, 14, 4. PubMed PMC
Mussmann, S.M. , Douglas, M.R. , Chafin, T.K. & Douglas, M.E. (2019) BA3‐SNPs: contemporary migration reconfigured in BayesAss for next‐generation sequence data. Methods in Ecology and Evolution, 10, 1808–1813.
Nagel, J.H. , Gryzenhout, M. , Slippers, B. , Wingfield, M.J. , Hardy, G.E.S.J. , Stukely, M.J.C. et al. (2013) Characterization of Phytophthora hybrids from ITS clade 6 associated with riparian ecosystems in South Africa and Australia. Fungal Biology, 117, 329–347. PubMed
O'Hanlon, R. , McCracken, A.R. & Cooke, L.R. (2016) Diversity and ecology of Phytophthora species on the Island of Ireland. Biology and Environment: Proceedings of the Royal Irish Academy, 116B, 27–51.
Oh, E. , Gryzenhout, M. , Wingfield, B.D. , Wingfield, M.J. & Burgess, T.I. (2013) Surveys of soil and water reveal a goldmine of Phytophthora diversity in south African natural ecosystems. IMA Fungus, 4, 123–131. PubMed PMC
Palczewski, M. & Beerli, P. (2014) Population model comparison using multi‐locus datasets. In: Chen, M.‐H. , Kuo, L. & Lewis, P.O. (Eds.) Bayesian phylogenetics: methods, algorithms, and applications. Boca Raton, FL: CRC Press, pp. 187–200.
Parker, I.M. & Gilbert, G.S. (2004) The evolutionary ecology of novel plant–pathogen interactions. Annual Review of Ecology, Evolution, and Systematics, 35, 675–700.
Pérez‐Sierra, A. , Chitty, R. , Eacock, A. , Jones, B. , Biddle, M. , Crampton, M. et al. (2022) First report of Phytophthora pluvialis in Europe causing resinous cankers on western hemlock. New Disease Reports, 45, e12064.
Pérez‐Sierra, A. , López‐García, C. , León, M. , García‐Jiménez, J. , Abad‐Campos, P. & Jung, T. (2013) Previously unrecorded low‐temperature Phytophthora species associated with Quercus decline in a Mediterranean forest in eastern Spain. Forest Pathology, 43, 331–339.
Pirronitto, S. , Paquet, F. , Gaucet, V. & Chandelier, A. (2024) First report of Phytophthora pluvialis in Douglas fir plantations in Belgium. New Disease Reports, 49, e12244.
Poland, J.A. , Brown, P.J. , Sorrells, M.E. & Jannink, J.‐L. (2012) Development of high‐density genetic maps for barley and wheat using a novel two‐enzyme genotyping‐by‐sequencing approach. PLoS One, 7, e32253. PubMed PMC
Posada, D. & Crandall, K.A. (2001) Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology & Evolution, 16, 37–45. PubMed
Pritchard, J.K. , Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959. PubMed PMC
Privé, F. , Luu, K. , Blum, M.G.B. , McGrath, J.J. & Vilhjálmsson, B.J. (2020) Efficient toolkit implementing best practices for principal component analysis of population genetic data. Bioinformatics, 36, 4449–4457. PubMed PMC
R Development Core Team . (2020) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rambaut, A. (2018) FigTree. Figtree, a graphical viewer of phylogenetic trees.
Rambaut, A. , Drummond, A.J. , Xie, D. , Baele, G. & Suchard, M.A. (2018) Posterior summarization in Bayesian phylogenetics using tracer 1.7. Systematic Biology, 67, 901–904. PubMed PMC
Redondo, M.Á. , Boberg, J. , Stenlid, J. & Oliva, J. (2016) First report of Phytophthora pseudosyringae causing basal cankers on horse chestnut in Sweden. Plant Disease, 100, 1024.
Redondo, M.Á. & Oliva, J. (2016) First report of Phytophthora pseudosyringae causing stem canker on Fagus sylvatica in Spain. Plant Disease, 100, 1508.
Reeser, P. , Sutton, W. & Hansen, E. (2013) Phytophthora pluvialis, a new species from mixed tanoak‐Douglas‐fir forests of western Oregon, U.S.A. North American Fungi, 8, 1–8.
Reeser, P.W. , Sutton, W. , Hansen, E.M. , Remigi, P. & Adams, G.C. (2011) Phytophthora species in forest streams in Oregon and Alaska. Mycologia, 103, 22–35. PubMed
Rizzo, D.M. , Garbelotto, M. , Davidson, J.M. , Slaughter, G.W. & Koike, S.T. (2002) Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Disease, 86, 205–214. PubMed
Rosenberg, N.A. (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137–138.
Safaiefarahani, B. , Mostowfizadeh‐Ghalamfarsa, R. , Hardy, G.E.S.J. & Burgess, T.I. (2016) Species from within the Phytophthora cryptogea complex and related species, P. erythroseptica and P. sansomeana, readily hybridize. Fungal Biology, 120, 975–987. PubMed
Scanu, B. , Linaldeddu, B.T. & Franceschini, A. (2010) First report of Phytophthora pseudosyringae associated with ink disease of Castanea sativa in Italy. Plant Disease, 94, 1068. PubMed
Scanu, B. , Linaldeddu, B.T. , Peréz‐Sierra, A. , Deidda, A. & Franceschini, A. (2014) Phytophthora ilicis as a leaf and stem pathogen of Ilex aquifolium in Mediterranean islands. Phytopathologia Mediterranea, 53, 480–490.
Scanu, B. & Webber, J.F. (2016) Dieback and mortality of Nothofagus in Britain: ecology, pathogenicity and sporulation potential of the causal agent Phytophthora pseudosyringae . Plant Pathology, 65, 26–36.
Schmieder, R. & Edwards, R. (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics, 27, 863–864. PubMed PMC
Schoebel, C.N. , Stewart, J. , Gruenwald, N.J. , Rigling, D. & Prospero, S. (2014) Population history and pathways of spread of the plant pathogen Phytophthora plurivora . PLoS One, 9, e85368. PubMed PMC
Seddaiu, S. , Brandano, A. , Ruiu, P.A. , Sechi, C. & Scanu, B. (2020) An overview of Phytophthora species inhabiting declining Quercus suber stands in Sardinia (Italy). Forests, 11, 971.
Shakya, S.K. , Grünwald, N.J. , Fieland, V.J. , Knaus, B.J. , Weiland, J.E. , Maia, C. et al. (2021) Phylogeography of the wide‐host range panglobal plant pathogen Phytophthora cinnamomi . Molecular Ecology, 30, 5164–5178. PubMed
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post‐analysis of large phylogenies. Bioinformatics, 30, 1312–1313. PubMed PMC
Stukenbrock, E.H. & McDonald, B.A. (2008) The origins of plant pathogens in agro‐ecosystems. Annual Review of Phytopathology, 46, 75–100. PubMed
Tabima, J.F. , Coffey, M.D. , Zazada, I.A. & Grünwald, N.J. (2018) Populations of Phytophthora rubi show little differentiation and high rates of migration among states in the western United States. Molecular Plant–Microbe Interactions, 31, 614–622. PubMed
Tabima, J.F. , Gonen, L. , Gómez‐Gallego, M. , Panda, P. , Grünwald, N.J. , Hansen, E.M. et al. (2021) Molecular phylogenomics and population structure of Phytophthora pluvialis . Phytopathology, 111, 108–115. PubMed
Talgø, V. , Herrero, M.L. , Sundbye, A. , Brurberg, M.‐B. , Kitchingman, L. , Telfer, K. et al. (2013) Phytophthora spp.‐ en trussel mot blåbær i Skandinavia? [Phytophthora spp. – a threat to blueberries in Scandinavia?]. Bioforsk TEMA, 8, 4.
Thorpe, P. , Vetukuri, R.R. , Hedley, P.E. , Morris, J. , Whisson, M.A. , Welsh, L.R.J. et al. (2021) Draft genome assemblies for tree pathogens Phytophthora pseudosyringae and Phytophthora boehmeriae . G3: Genes, Genomes, Genetics, 11, jkab282. PubMed PMC
Tomura, T. , Molli, S.D. , Murata, R. & Ojika, M. (2017) Universality of the Phytophthora mating hormones and diversity of their production profile. Scientific Reports, 7, 5007. PubMed PMC
Tsykun, T. , Prospero, S. , Schoebel, C.N. , Rea, A. & Burgess, T.I. (2022) Global invasion history of the emerging plant pathogen Phytophthora multivora . BMC Genomics, 23, 153. PubMed PMC
Turner, R.S. (2005) After the famine: plant pathology, Phytophthora infestans, and the late blight of potatoes, 1845–1960. Historical Studies in the Physical and Biological Sciences, 35, 341–370.
Van Poucke, K. , Haegeman, A. , Goedefroit, T. , Focquet, F. , Leus, L. , Horta Jung, M. et al. (2021) Unravelling hybridization in Phytophthora using phylogenomics and genome size estimation. IMA Fungus, 12, 16. PubMed PMC
Whisson, S.C. , Drenth, A. , Maclean, D.J. & Irwin, J.A.G. (1994) Evidence for outcrossing in Phytophthora sojae and linkage of a DNA marker to two avirulence genes. Current Genetics, 27, 77–82. PubMed
Wickland, A.C. , Jensen, C.E. & Rizzo, D.M. (2008) Geographic distribution, disease symptoms and pathogenicity of Phytophthora nemorosa and Phytophthora pseudosyringae in California, USA. Forest Pathology, 38, 288–298.
Wilson, G.A. & Rannala, B. (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics, 163, 1177–1191. PubMed PMC
Yakabe, L.E. , Blomquist, C.L. , Thomas, S.L. & MacDonald, J.D. (2009) Identification and frequency of Phytophthora species associated with foliar diseases in California ornamental nurseries. Plant Disease, 93, 883–890. PubMed
Zhang, J. , Kobert, K. , Flouri, T. & Stamatakis, A. (2014) PEAR: a fast and accurate Illumina paired‐end reAd mergeR. Bioinformatics, 30, 614–620. PubMed PMC