Invasive, exotic plant pathogens pose a major threat to native and agricultural ecosystems. Phytophthora × cambivora is an invasive, destructive pathogen of forest and fruit trees causing severe damage worldwide to chestnuts (Castanea), apricots, peaches, plums, almonds and cherries (Prunus), apples (Malus), oaks (Quercus), and beech (Fagus). It was one of the first damaging invasive Phytophthora species to be introduced to Europe and North America, although its origin is unknown. We determined its population genetic history in Europe, North and South America, Australia and East Asia (mainly Japan) using genotyping-by-sequencing. Populations in Europe and Australia appear clonal, those in North America are highly clonal yet show some degree of sexual reproduction, and those in East Asia are partially sexual. Two clonal lineages, each of opposite mating type, and a hybrid lineage derived from these two lineages, dominated the populations in Europe and were predominantly found on fagaceous forest hosts (Castanea, Quercus, Fagus). Isolates from fruit trees (Prunus and Malus) belonged to a separate lineage found in Australia, North America, Europe and East Asia, indicating the disease on fruit trees could be caused by a distinct lineage of P. × cambivora, which may potentially be a separate sister species and has likely been moved with live plants. The highest genetic diversity was found in Japan, suggesting that East Asia is the centre of origin of the pathogen. Further surveys in unsampled, temperate regions of East Asia are needed to more precisely identify the location and range of the centre of diversity.

Department of Bioregulation and Biointeraction Laboratory of Molecular and Cellular Biology Tokyo University of Agriculture and Technology Fuchu Tokyo Japan

Department of Botany and Plant Pathology Oregon State University Corvallis OR USA

Department of Horticulture Oregon State University Corvallis OR USA

Flanders Research Institute for Agriculture Fisheries and Food Plant Sciences Unit Merelbeke Belgium

Forest Research Alice Holt Lodge Farnham Surrey UK

Forestry and Forest Products Research Institute Tsukuba Ibaraki Japan

Horticultural Crops Research Unit United States Department of Agriculture Agricultural Research Service Corvallis OR USA

Phytophthora Research and Consultancy Nussdorf Germany

Phytophthora Research Centre Department of Forest Protection and Wildlife Management Mendel University in Brno Brno Czech Republic

Plant Protection Institute Centre for Agricultural Research ELKH Budapest Hungary

River Basin Research Center Gifu University Gifu Japan

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Abdellaoui A, Hottenga J-J, de Knijff P, Nivard MG, Xiao X, Scheet P, Brooks A, Ehli EA, Hu Y, Davies GE, Hudziak JJ, Sullivan PF, van Beijsterveldt T, Willemsen G, de Geus EJ, Penninx BWJH, Boomsma DI. Population structure, migration, and diversifying selection in the Netherlands. Eur J Hum Genet. 2013;21:1277–1285. doi: 10.1038/ejhg.2013.48. PubMed DOI PMC

Ann P-J, Ko W-H. Effect of chloroneb and ethazol on mating type of Phytophthora parasitica and P. cinnamomi. Bot Bull Acad Sin. 1989;30:207–210.

Ashby SF. Oospores in cultures of Phytophthora faberi. Kew Bull. 1922;1922(9):257–262.

Ashu EE, Xu J. The roles of sexual and asexual reproduction in the origin and dissemination of strains causing fungal infectious disease outbreaks. Infect Genet Evol. 2015;36:199–209. doi: 10.1016/j.meegid.2015.09.019. PubMed DOI

Baduel P, Bray S, Vallejo-Marin M, Kolář F, Yant L. The “Polyploid Hop”: shifting challenges and opportunities over the evolutionary lifespan of genome duplications. Front Ecol Evol. 2018 doi: 10.3389/fevo.2018.00117. DOI

Barchenger DW, Lamour KH, Sheu Z-M, Shrestha S, Kumar S, Lin S-W, Burlakoti R, Bosland PW. Intra- and Intergenomic variation of ploidy and clonality characterize Phytophthora capsici on Capsicum sp. in Taiwan. Mycol Progress. 2017;16:955–963. doi: 10.1007/s11557-017-1330-0. DOI

Bertier L, Leus L, D’hondt L, de Cock AWAM, Höfte M. Host adaptation and speciation through hybridization and polyploidy in Phytophthora. PLoS ONE. 2013;8:e85385. doi: 10.1371/journal.pone.0085385. PubMed DOI PMC

Blischak PD (2021) pblischak-HyDe/Lobby. https://gitter.im/pblischak-HyDe/Lobby. Accessed 22 Apr 2021

Blischak P, Kubatko L (2019) HyDe Documentation Release 0.4.1a. 25

Blischak PD, Chifman J, Wolfe AD, Kubatko LS. HyDe: a Python package for genome-scale hybridization detection. Syst Biol. 2018;67:821–829. doi: 10.1093/sysbio/syy023. PubMed DOI PMC

Boyer F, Mercier C, Bonin A, Le Bras Y, Taberlet P, Coissac E. obitools: a unix-inspired software package for DNA metabarcoding. Mol Ecol Resour. 2016;16:176–182. doi: 10.1111/1755-0998.12428. PubMed DOI

Brasier C. Induction of sexual reproduction in single A2 isolates of Phytophthora species by Trichoderma viride. Nat New Biol. 1971;231:283. doi: 10.1038/newbio231283a0. DOI

Brasier C. Observations on the sexual mechanism in Phytophthora palmivora and related species. Trans Br Mycol Soc. 1972;58:237–251. doi: 10.1016/S0007-1536(72)80153-0. DOI

Brasier C. Stimulation of sex organ formation in Phytophthora by antagonistic species of Trichoderma. I. The effect in vitro. New Phytol. 1975;74:183–194. doi: 10.1111/j.1469-8137.1975.tb02604.x. DOI

Brasier C. Episodic selection as a force in fungal microevolution with special reference to clonal speciation and hybrid introgression. Can J Bot. 1995;73:1213–1221. doi: 10.1139/b95-381. DOI

Brasier C. Rapid evolution of introduced plant pathogens via interspecific hybridization. Bioscience. 2001;51:123–133. doi: 10.1641/0006-3568(2001)051[0123:REOIPP]2.0.CO;2. DOI

Brasier C. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol. 2008;57:792–808. doi: 10.1111/j.1365-3059.2008.01886.x. DOI

Brasier C, Kirk SA. Survival of clones of NAN Ophiostoma novo-ulmi around its probable centre of appearance in North America. Mycol Res. 2000;104:1322–1332. doi: 10.1017/S0953756200002732. DOI

Brasier C, Kirk SA. Comparative aggressiveness of standard and variant hybrid alder phytophthoras, Phytophthora cambivora and other Phytophthora species on bark of Alnus, Quercus and other woody hosts. Plant Pathol. 2001;50:218–229. doi: 10.1046/j.1365-3059.2001.00553.x. DOI

Brasier C, Webber J. Sudden larch death. Nature. 2010;466:824–825. doi: 10.1038/466824a. PubMed DOI

Brasier C, Cooke DEL, Duncan JM. Origin of a new Phytophthora pathogen through interspecific hybridization. PNAS. 1999;96:5878–5883. doi: 10.1073/pnas.96.10.5878. PubMed DOI PMC

Brasier C, Cooke DEL, Duncan JM, Hansen EM. Multiple new phenotypic taxa from trees and riparian ecosystems in Phytophthora gonapodyides-P. megasperma ITS Clade 6, which tend to be high-temperature tolerant and either inbreeding or sterile. Mycol Res. 2003;107:277–290. doi: 10.1017/S095375620300738X. PubMed DOI

Brasier C, Franceschini S, Forster J, Kirk S. Enhanced outcrossing, directional selection and transgressive segregation drive evolution of novel phenotypes in hybrid swarms of the Dutch elm disease pathogen ophiostoma novo-ulmi. J Fungi. 2021;7:452. doi: 10.3390/jof7060452. PubMed DOI PMC

Brown AV, Brasier CM. Colonization of tree xylem by Phytophthora ramorum, P. kernoviae and other Phytophthora species. Plant Pathol. 2007;56:227–241. doi: 10.1111/j.1365-3059.2006.01511.x. DOI

Brown AHD, Feldman MW, Nevo E. Multilocus structure of natural populations of Hordeum spontaneum. Genetics. 1980;96:523–536. doi: 10.1093/genetics/96.2.523. PubMed DOI PMC

Browne GT, Mircetich SM, Cummins JN. Relative resistance of eighteen selections of Malus spp. to three species of Phytophthora. Phytopathology. 1995;85:72. doi: 10.1094/Phyto-85-72. DOI

Buisman CJ. Root rots caused by Phycomycetes. Rev Appl Mycol. 1927;6:380–381.

Bumbieris M, Wicks T. Phytophthora cambivora associated with apple trees in South Australia. Austral Plant Pathol. 1980;9:114. doi: 10.1071/APP9800114. DOI

Burgess TI. Molecular characterization of natural hybrids formed between five related indigenous clade 6 Phytophthora species. PLoS ONE. 2015;10:e0134225. doi: 10.1371/journal.pone.0134225. PubMed DOI PMC

CABI (2017) Phytophthora cambivora (root rot of forest trees). http://www.cabi.org/isc/datasheet/40956. Accessed 23 Aug 2017

Calus MPL, Vandenplas J. SNPrune: an efficient algorithm to prune large SNP array and sequence datasets based on high linkage disequilibrium. Genet Sel Evol. 2018 doi: 10.1186/s12711-018-0404-z. PubMed DOI PMC

Catal M, King L, Tumbalam P, Wiriyajitsomboon P, Kirk WW, Adams GC. Heterokaryotic nuclear conditions and a heterogeneous nuclear population are observed by flow cytometry in Phytophthora infestans. Cytometry A. 2010;77A:769–775. doi: 10.1002/cyto.a.20888. PubMed DOI

Černý K, Gregorová B, Strnadová V, Holub V (2006) The genus Phytophthora on woody plants—findings in 2005. In: Damaging agents in forest of Czechia 2005/2006. Strnady, pp 20–26

Chandelier A, Heungens K, Werres S. Change of mating type in an EU1 lineage isolate of Phytophthora ramorum. J Phytopathol. 2014;162:43–47. doi: 10.1111/jph.12150. DOI

Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience. 2015 doi: 10.1186/s13742-015-0047-8. PubMed DOI PMC

Chen Q, Bakhshi M, Balci Y, Broders KD, Cheewangkoon R, Chen SF, Fan XL, Gramaje D, Halleen F, Horta Jung M, Jiang N, Jung T, Májek T, Marincowitz S, Milenković I, Mostert L, Nakashima C, Nurul Faziha I, Pan M, Raza M, Scanu B, Spies CFJ, Suhaizan L, Suzuki H, Tian CM, Tomšovský M, Úrbez-Torres JR, Wang W, Wingfield BD, Wingfield MJ, Yang Q, Yang X, Zare R, Zhao P, Groenewald JZ, Cai L, Crous PW. Genera of phytopathogenic fungi: GOPHY 4. Stud Mycol. 2022;101:417–564. doi: 10.3114/sim.2022.101.06. PubMed DOI PMC

Chhatre VE, Emerson KJ. StrAuto: automation and parallelization of STRUCTURE analysis. BMC Bioinform. 2017;18:192. doi: 10.1186/s12859-017-1593-0. PubMed DOI PMC

Chifman J, Kubatko L. Quartet inference from SNP data under the coalescent model. Bioinformatics. 2014;30:3317–3324. doi: 10.1093/bioinformatics/btu530. PubMed DOI PMC

Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR, Etherington GJ, Deahl KL, Farrer RA, Gilroy EM, Goss EM, Grünwald NJ, Hein I, MacLean D, McNicol JW, Randall E, Oliva RF, Pel MA, Shaw DS, Squires JN, Taylor MC, Vleeshouwers VGAA, Birch PRJ, Lees AK, Kamoun S. Genome analyses of an aggressive and invasive lineage of the Irish Potato Famine Pathogen. PLOS Pathogens. 2012;8:e1002940. doi: 10.1371/journal.ppat.1002940. PubMed DOI PMC

Corcobado T, Cech TL, Brandstetter M, Daxer A, Hüttler C, Kudláček T, Horta Jung M, Jung T. Decline of European beech in Austria: involvement of Phytophthora spp. and contributing biotic and abiotic factors. Forests. 2020;11:895. doi: 10.3390/f11080895. DOI

Crandall BS. The distribution and significance of the chestnut root rot Phytophthoras, P. cinnamomi and P. cambivora. Plant Dis Report. 1950;6:194–196.

Cristinzio G, Grassi G. Assessing resistance to ink disease (caused by Phytophthora cambivora and Phytophthora cinnamomi) in chestnut cultivars. Monti e Boschi. 1993;44:54–58.

Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group The variant call format and VCFtools. Bioinformatics. 2011;27:2156–2158. doi: 10.1093/bioinformatics/btr330. PubMed DOI PMC

Dowling TE, Secor CL. The role of hybridization and introgression in the diversification of animals. Annu Rev Ecol Syst. 1997;28:593–619. doi: 10.1146/annurev.ecolsys.28.1.593. DOI

Drenth A, McTaggart AR, Wingfield BD. Fungal clones win the battle, but recombination wins the war. IMA Fungus. 2019;10:18. doi: 10.1186/s43008-019-0020-8. PubMed DOI PMC

Dussert Y, Legrand L, Mazet ID, Couture C, Piron M-C, Serre R-F, Bouchez O, Mestre P, Toffolatti SL, Giraud T, Delmotte F. Identification of the first oomycete mating-type locus sequence in the grapevine downy mildew pathogen, Plasmopara viticola. Curr Biol. 2020;30:3897–3907.e4. doi: 10.1016/j.cub.2020.07.057. PubMed DOI PMC

Ehrendorfer F. Polyploidy and distribution. In: Lewis WH, editor. Polyploidy: biological relevance. Boston: Springer; 1980. pp. 45–60.

Ellstrand NC, Schierenbeck KA. Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci. 2000;97:7043–7050. doi: 10.1073/pnas.97.13.7043. PubMed DOI PMC

Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE. 2011;6:e19379. doi: 10.1371/journal.pone.0019379. PubMed DOI PMC

Erwin DC, Ribeiro OK. Phytophthora diseases worldwide. St. Paul: American Phytopathological Society (APS Press); 1996.

Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x. PubMed DOI

Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003;164:1567–1587. doi: 10.1093/genetics/164.4.1567. PubMed DOI PMC

Feau N, Taylor G, Dale AL, Dhillon B, Bilodeau GJ, Birol I, Jones SJM, Hamelin RC. Genome sequences of six Phytophthora species threatening forest ecosystems. Genomics Data. 2016;10:85–88. doi: 10.1016/j.gdata.2016.09.013. PubMed DOI PMC

Fernández-López J, Vazquez-Ruiz-de-Ocenda RA, Díaz-Vázquez R, Pereira-Lorenzo S. Evaluation of resistance of Castanea sp. clones to Phytophthora sp. using excised chestnut shoots. For Snow Landsc Res. 2001;76:451–454.

Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ. Emerging fungal threats to animal, plant and ecosystem health. Nature. 2012;484:186–194. doi: 10.1038/nature10947. PubMed DOI PMC

Fleisch MR. Vers une recrudescence de la maladie de l’encre du chataignier en foret? Les Cahiers du DSF (La Sante des Forets (France) en 2000 et 2001) Min Agri Alim Peche Aff Rur (DERF) Paris. 2002;1:63–66.

Fletcher K, Gil J, Bertier LD, Kenefick A, Wood KJ, Zhang L, Reyes-Chin-Wo S, Cavanaugh K, Tsuchida C, Wong J, Michelmore R. Genomic signatures of heterokaryosis in the oomycete pathogen Bremia lactucae. Nat Commun. 2019;10:2645. doi: 10.1038/s41467-019-10550-0. PubMed DOI PMC

Gauthier O, Lapointe F-J. Hybrids and phylogenetics revisited: a statistical test of hybridization using quartets. Syst Bot. 2007;32:8–15. doi: 10.1600/036364407780360238. DOI

Gompert Z, Mock KE. Detection of individual ploidy levels with genotyping-by-sequencing (GBS) analysis. Mol Ecol Resour. 2017;17:1156–1167. doi: 10.1111/1755-0998.12657. PubMed DOI

Goodwin SB. The population genetics of Phytophthora. Phytopathology. 1997;87:462–473. doi: 10.1094/PHYTO.1997.87.4.462. PubMed DOI

Goss EM, Carbone I, Grünwald NJ. Ancient isolation and independent evolution of the three clonal lineages of the exotic sudden oak death pathogen Phytophthora ramorum. Mol Ecol. 2009;18:1161–1174. doi: 10.1111/j.1365-294X.2009.04089.x. PubMed DOI

Goss EM, Tabima JF, Cooke DEL, Restrepo S, Fry WE, Forbes GA, Fieland VJ, Cardenas M, Grunwald NJ. The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. Proc Natl Acad Sci. 2014;111:8791–8796. doi: 10.1073/pnas.1401884111. PubMed DOI PMC

Groves CT, Ristaino JB. Commercial fungicide formulations induce in vitro oospore formation and phenotypic change in mating type in Phytophthora infestans. Phytopathology. 2000;90:1201–1208. doi: 10.1094/PHYTO.2000.90.11.1201. PubMed DOI

Grünwald NJ, Garbelotto M, Goss EM, Heungens K, Prospero S. Emergence of the sudden oak death pathogen Phytophthora ramorum. Trends Microbiol. 2012;20:131–138. doi: 10.1016/j.tim.2011.12.006. PubMed DOI

Haasis FA, Nelson RR. Studies on the biological relationship of species of Phytophthora as measured by oospore formation in intra-and interspecific crosses. Plant Dis Report. 1963;47:5–7.

Hansen ZR, Everts KL, Fry WE, Gevens AJ, Grünwald NJ, Gugino BK, Johnson DA, Johnson SB, Judelson HS, Knaus BJ, McGrath MT, Myers KL, Ristaino JB, Roberts PD, Secor GA, Smart CD. Genetic variation within clonal lineages of Phytophthora infestans revealed through genotyping-by-sequencing, and implications for late blight epidemiology. PLoS ONE. 2016;11:e0165690. doi: 10.1371/journal.pone.0165690. PubMed DOI PMC

Herben T, Suda J, Klimešová J. Polyploid species rely on vegetative reproduction more than diploids: a re-examination of the old hypothesis. Ann Bot. 2017;120:341–349. doi: 10.1093/aob/mcx009. PubMed DOI PMC

Herten K, Hestand MS, Vermeesch JR, Van Houdt JK. GBSX: a toolkit for experimental design and demultiplexing genotyping by sequencing experiments. BMC Bioinform. 2015;16:73. doi: 10.1186/s12859-015-0514-3. PubMed DOI PMC

Hollister JD. Polyploidy: adaptation to the genomic environment. New Phytol. 2015;205:1034–1039. doi: 10.1111/nph.12939. PubMed DOI

Hüberli D, Hardy GEStJ, White D, Williams N, Burgess TI. Fishing for Phytophthora from Western Australia’s waterways: a distribution and diversity survey. Austral Plant Pathol. 2013;42:251–260. doi: 10.1007/s13313-012-0195-6. DOI

Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23:254–267. doi: 10.1093/molbev/msj030. PubMed DOI

Husson C, Aguayo J, Revellin C, Frey P, Ioos R, Marçais B. Evidence for homoploid speciation in Phytophthora alni supports taxonomic reclassification in this species complex. Fungal Genet Biol. 2015;77:12–21. doi: 10.1016/j.fgb.2015.02.013. PubMed DOI

Jankowiak R, Banach J, Balonek A. Susceptibility of Polish provenances and families of pedunculate oak (Quercus robur L.) to colonisation by Phytophthora cambivora. For Res Pap. 2013;74:161–170. doi: 10.2478/frp-2013-0016. DOI

Jayasekera AU, McComb JA, Shearer BL, Hardy GESJ. In planta selfing and oospore production of Phytophthora cinnamomi in the presence of Acacia pulchella. Mycol Res. 2007;111:355–362. doi: 10.1016/j.mycres.2006.11.003. PubMed DOI

Jee H-J, Cho W-D, Kim W-G. Phytophthora diseases of apple in Korea: II. Occurrence of an unusual fruit rot caused by P. cactorum and P. cambivora. Korean J Plant Pathol. 1997;13:145–151.

Jombart T, Ahmed I. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics. 2011;27:3070–3071. doi: 10.1093/bioinformatics/btr521. PubMed DOI PMC

Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11:94. doi: 10.1186/1471-2156-11-94. PubMed DOI PMC

Jombart T, Collins C (2015) A tutorial for Discriminant Analysis of Principal Components (DAPC) using adegenet 2.0. 0

Jung T. Beech decline in Central Europe driven by the interaction between Phytophthora infections and climatic extremes. For Pathol. 2009;39:73–94. doi: 10.1111/j.1439-0329.2008.00566.x. DOI

Jung T, Blaschke H, Neumann P. Isolation, identification and pathogenicity of Phytophthora species from declining oak stands. Eur J for Pathol. 1996;26:253–272. doi: 10.1111/j.1439-0329.1996.tb00846.x. DOI

Jung T, Blaschke H, Oßwald W. Involvement of soilborne Phytophthora species in Central European oak decline and the effect of site factors on the disease. Plant Pathol. 2000;49:706–718. doi: 10.1046/j.1365-3059.2000.00521.x. DOI

Jung T, Hudler GW, Jensen-tracy SL, Griffiths HM, Fleischmann F, Osswald W. Involvement of Phytophthora species in the decline of European beech in Europe and the USA. Mycologist. 2005;19:159–166. doi: 10.1017/S0269-915X(05)00405-2. DOI

Jung T, Hudler GW, Jensen-Tracy SL, Griffiths HM, Fleischmann F, Osswald W. Involvement of Phytophthora species in the decline of European beech in Europe and the USA. MYT. 2006;19:159. doi: 10.1017/S0269915X05004052. DOI

Jung T, Stukely MJC, Hardy GEStJ, White D, Paap T, Dunstan WA, Burgess TI. Multiple new Phytophthora species from ITS Clade 6 associated with natural ecosystems in Australia: evolutionary and ecological implications. Pers Mol Phylogeny Evol Fungi. 2011;26:13–39. doi: 10.3767/003158511X557577. PubMed DOI PMC

Jung T, Colquhoun IJ, Hardy GEStJ. New insights into the survival strategy of the invasive soilborne pathogen Phytophthora cinnamomi in different natural ecosystems in Western Australia. For Pathol. 2013;43:266–288. doi: 10.1111/efp.12025. DOI

Jung T, Orlikowski L, Henricot B, Abad-Campos P, Aday AG, Aguín Casal O, Bakonyi J, Cacciola SO, Cech T, Chavarriaga D, Corcobado T, Cravador A, Decourcelle T, Denton G, Diamandis S, Doğmuş-Lehtijärvi HT, Franceschini A, Ginetti B, Green S, Glavendekić M, Hantula J, Hartmann G, Herrero M, Ivic D, Horta Jung M, Lilja A, Keca N, Kramarets V, Lyubenova A, Machado H, di San M, Lio G, Mansilla Vázquez PJ, Marçais B, Matsiakh I, Milenkovic I, Moricca S, Nagy ZÁ, Nechwatal J, Olsson C, Oszako T, Pane A, Paplomatas EJ, Pintos Varela C, Prospero S, Rial Martínez C, Rigling D, Robin C, Rytkönen A, Sánchez ME, Sanz Ros AV, Scanu B, Schlenzig A, Schumacher J, Slavov S, Solla A, Sousa E, Stenlid J, Talgø V, Tomic Z, Tsopelas P, Vannini A, Vettraino AM, Wenneker M, Woodward S, Peréz-Sierra A. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. For Pathol. 2016;46:134–163. doi: 10.1111/efp.12239. DOI

Jung T, Chang TT, Bakonyi J, Seress D, Pérez-Sierra A, Yang X, Hong C, Scanu B, Fu CH, Hsueh KL, Maia C, Abad-Campos P, Léon M, Horta Jung M. Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathol. 2017;66:194–211. doi: 10.1111/ppa.12564. DOI

Jung T, Horta Jung M, Scanu B, Seress D, Kovács GM, Maia C, Pérez-Sierra A, Chang T-T, Chandelier A, Heungens K, Van Poucke K, Abad-Campos P, Léon M, Cacciola SO, Bakonyi J. Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Pers Mol Phylogeny Evol Fungi. 2017;38:100–135. doi: 10.3767/003158517X693615. PubMed DOI PMC

Jung T, Durán A, Sanfuentes von Stowasser E, Schena L, Mosca S, Fajardo S, González M, Navarro Ortega AD, Bakonyi J, Seress D, Tomšovský M, Cravador A, Maia C, Horta Jung M (2018a) Diversity of Phytophthora species in Valdivian rainforests and association with severe dieback symptoms. For Pathol 48:e12443. 10.1111/efp.12443

Jung T, Pérez-Sierra A, Durán A, Horta Jung M, Balci Y, Scanu B. Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Pers Mol Phylogeny Evol Fungi. 2018;40:182–220. doi: 10.3767/persoonia.2018.40.08. PubMed DOI PMC

Jung T, Scanu B, Brasier C, Webber J, Milenković I, Corcobado T, Tomšovský M, Pánek M, Bakonyi J, Maia C, Bačová A, Raco M, Rees H, Pérez-Sierra A, Horta Jung M (2020) A survey in natural forest ecosystems of vietnam reveals high diversity of both new and described Phytophthora taxa including P. ramorum. Forests 11:93. 10.3390/f11010093

Jung T, Horta Jung M, Webber JF, Kageyama K, Hieno A, Masuya H, Uematsu S, Pérez-Sierra A, Harris AR, Forster J, Rees H, Scanu B, Patra S, Kudláček T, Janoušek J, Corcobado T, Milenković I, Nagy Z, Csorba I, Bakonyi J, Brasier C. The destructive tree pathogen Phytophthora ramorum originates from the laurosilva forests of East Asia. J Fungi. 2021;7:226. doi: 10.3390/jof7030226. PubMed DOI PMC

Kamvar ZN, Tabima JF, Grünwald NJ. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ. 2014;2:e281. doi: 10.7717/peerj.281. PubMed DOI PMC

Kamvar ZN, Brooks JC, Grünwald NJ. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front Genet. 2015 doi: 10.3389/fgene.2015.00208. PubMed DOI PMC

Knaus BJ, Grünwald NJ. vcfr: a package to manipulate and visualize variant call format data in R. Mol Ecol Resour. 2017;17:44–53. doi: 10.1111/1755-0998.12549. PubMed DOI

Knaus BJ, Grünwald NJ. Inferring variation in copy number using high throughput sequencing data in R. Front Genet. 2018 doi: 10.3389/fgene.2018.00123. PubMed DOI PMC

Knaus BJ, Tabima JF, Shakya SK, Judelson HS, Grünwald NJ. Genome-wide increased copy number is associated with emergence of dominant clones of the Irish potato famine pathogen Phytophthora infestans. Mbio. 2020 doi: 10.1128/mBio.00326-20. PubMed DOI PMC

Ko WH. Reversible change of mating type in Phytophthora parasitica. Microbiology. 1981;125:451–454. doi: 10.1099/00221287-125-2-451. DOI

Kong S, Kubatko LS (2020) Comparative performance of popular methods for hybrid detection using genomic data. Bioinformatics PubMed

Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. 2015;15:1179–1191. doi: 10.1111/1755-0998.12387. PubMed DOI PMC

Lamour KH, Stam R, Jupe J, Huitema E. The oomycete broad-host-range pathogen Phytophthora capsici. Mol Plant Pathol. 2012;13:329–337. doi: 10.1111/j.1364-3703.2011.00754.x. PubMed DOI PMC

Landolt J, Gross A, Holdenrieder O, Pautasso M. Ash dieback due to Hymenoscyphus fraxineus: what can be learnt from evolutionary ecology? Plant Pathol. 2016;65:1056–1070. doi: 10.1111/ppa.12539. DOI

Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997 [q-bio]

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC

Long M, Keen NT (1977) Evidence for heterokaryosis in Phytophthora megasperma var. sojae. Phytopathology 670–674

Malomane DK, Reimer C, Weigend S, Weigend A, Sharifi AR, Simianer H. Efficiency of different strategies to mitigate ascertainment bias when using SNP panels in diversity studies. BMC Genomics. 2018;19:22. doi: 10.1186/s12864-017-4416-9. PubMed DOI PMC

Martens C, Van de Peer Y. The hidden duplication past of the plant pathogen Phytophthora and its consequences for infection. BMC Genomics. 2010;11:353. doi: 10.1186/1471-2164-11-353. PubMed DOI PMC

Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J. 2011;17:10–12. doi: 10.14806/ej.17.1.200. DOI

McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–1303. doi: 10.1101/gr.107524.110. PubMed DOI PMC

Milgroom MG. Recombination and the multilocus structure of fungal populations. Annu Rev Phytopathol. 1996;34:457–477. doi: 10.1146/annurev.phyto.34.1.457. PubMed DOI

Milgroom MG, Brasier CM. Potential diversity of vegetative compatibility types of Ophiostoma novo-ulmi in North America. Mycologia. 1997;89:722–726. doi: 10.1080/00275514.1997.12026838. DOI

Mircetich SM, Matheron ME. Phytophthora root and crown rot of cherry trees. Phytopathology. 1976;66:549. doi: 10.1094/Phyto-66-549. DOI

Mukerjee N, Roy BA. Microbial influence on the formation of oospores in culture of Phytophthora parasitica var. sabdariffae. Phytopathology. 1962;52:583–584.

Nagel JH, Gryzenhout M, Slippers B, Wingfield MJ, Hardy GEStJ, Stukely MJC, Burgess TI. Characterization of Phytophthora hybrids from ITS clade 6 associated with riparian ecosystems in South Africa and Australia. Fungal Biol. 2013;117:329–347. doi: 10.1016/j.funbio.2013.03.004. PubMed DOI

Nechwatal J, Hahn J, Schönborn A, Schmitz G. A twig blight of understorey European beech (Fagus sylvatica) caused by soilborne Phytophthora spp. For Pathol. 2011;41:493–500. doi: 10.1111/j.1439-0329.2011.00711.x. DOI

Oh E, Gryzenhout M, Wingfield BD, Wingfield MJ, Burgess TI. Surveys of soil and water reveal a goldmine of Phytophthora diversity in South African natural ecosystems. IMA Fungus. 2013;4:123–131. doi: 10.5598/imafungus.2013.04.01.12. PubMed DOI PMC

Olave M, Meyer A. Implementing large genomic single nucleotide polymorphism data sets in phylogenetic network reconstructions: a case study of particularly rapid radiations of cichlid fish. Syst Biol. 2020;69:848–862. doi: 10.1093/sysbio/syaa005. PubMed DOI

Otto SP, Whitton J. Polyploid incidence and evolution. Annu Rev Genet. 2000;34:401–437. doi: 10.1146/annurev.genet.34.1.401. PubMed DOI

Oudemans P, Coffey MD. Isozyme comparison within and among worldwide sources of three morphologically distinct species of Phytophthora. Mycol Res. 1991;95:19–30. doi: 10.1016/S0953-7562(09)81358-0. DOI

Pandit MK, Tan HTW, Bisht MS. Polyploidy in invasive plant species of Singapore. Bot J Linn Soc. 2006;151:395–403. doi: 10.1111/j.1095-8339.2006.00515.x. DOI

Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35:526–528. doi: 10.1093/bioinformatics/bty633. PubMed DOI

Patterson N, Moorjani P, Luo Y, Mallick S, Rohland N, Zhan Y, Genschoreck T, Webster T, Reich D. Ancient admixture in human history. Genetics. 2012;192:1065–1093. doi: 10.1534/genetics.112.145037. PubMed DOI PMC

Peace TR. Pathology of trees and shrubs: with special reference to Britain. Oxford: Clarendon Press; 1962.

Pereira JG, Valdiviesso T, de Abreu CP, de Sousa AJT. Chestnut ink disease. Appraisal of the sensitivity of chestnut clones to ink disease. Phytoma. 1995;477:50–52.

Petri L. Ricerche sulla morfologia e biologia della Blepharospora cambivora, parassita del castagno. Atti Reale Accad Dei Lincei Rend Delle Classi Di Sci Fisiche Mat Nat. 1917;5:297–299.

Poland JA, Brown PJ, Sorrells ME, Jannink J-L. Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE. 2012;7:e32253. doi: 10.1371/journal.pone.0032253. PubMed DOI PMC

Posada D, Crandall KA. Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol. 2001;16:37–45. doi: 10.1016/S0169-5347(00)02026-7. PubMed DOI

Posada D, Crandall KA. The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol. 2002;54:396–402. doi: 10.1007/s00239-001-0034-9. PubMed DOI

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–959. doi: 10.1093/genetics/155.2.945. PubMed DOI PMC

Privé F, Luu K, Blum MGB, McGrath JJ, Vilhjálmsson BJ. Efficient toolkit implementing best practices for principal component analysis of population genetic data. Bioinformatics. 2020;36:4449–4457. doi: 10.1093/bioinformatics/btaa520. PubMed DOI PMC

R Development Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria

Rambaut A (2018) FigTree. In: Figtree, a graphical viewer of phylogenetic trees. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 2 Mar 2021

Ramsey J. Polyploidy and ecological adaptation in wild yarrow. PNAS. 2011;108:7096–7101. doi: 10.1073/pnas.1016631108. PubMed DOI PMC

Rigling D, Prospero S. Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and disease control. Mol Plant Pathol. 2018;19:7–20. doi: 10.1111/mpp.12542. PubMed DOI PMC

Robin C, Morel O, Vettraino A-M, Perlerou C, Diamandis S, Vannini A. Genetic variation in susceptibility to Phytophthora cambivora in European chestnut (Castanea sativa) For Ecol Manag. 2006;226:199–207. doi: 10.1016/j.foreco.2006.01.035. DOI

Rosenberg NA. DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes. 2004;4:137–138. doi: 10.1046/j.1471-8286.2003.00566.x. DOI

Saavedra A, Hansen EM, Goheen DJ. Phytophthora cambivora in Oregon and its pathogenicity to Chrysolepis chrysophylla. For Pathol. 2007;37:409–419. doi: 10.1111/j.1439-0329.2007.00515.x. DOI

Salesses G, Ronco L, Chauvin J-E, Chapa J (1993) Amelioration genetique du chataignier. Mise au point de tests d’evaluation du comportement vis-a-vis de la maladie de l’encre. Arboricult Fruit 23

Sansome ER. Reciprocal translocation heterozygosity in heterothallic species of Phytophthora and its significance. Trans Br Mycol Soc. 1980;74:175–185. doi: 10.1016/S0007-1536(80)80023-4. DOI

Santini A, Ghelardini L, De Pace C, Desprez-Loustau ML, Capretti P, Chandelier A, Cech T, Chira D, Diamandis S, Gaitniekis T, Hantula J, Holdenrieder O, Jankovsky L, Jung T, Jurc D, Kirisits T, Kunca A, Lygis V, Malecka M, Marcais B, Schmitz S, Schumacher J, Solheim H, Solla A, Szabò I, Tsopelas P, Vannini A, Vettraino AM, Webber J, Woodward S, Stenlid J. Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol. 2013;197:238–250. doi: 10.1111/j.1469-8137.2012.04364.x. PubMed DOI

Schierenbeck KA, Ellstrand NC. Hybridization and the evolution of invasiveness in plants and other organisms. Biol Invasions. 2008;11:1093. doi: 10.1007/s10530-008-9388-x. DOI

Schinkel CCF, Kirchheimer B, Dellinger AS, Klatt S, Winkler M, Dullinger S, Hörandl E (2016) Correlations of polyploidy and apomixis with elevation and associated environmental gradients in an alpine plant. AoB PLANTS. 10.1093/aobpla/plw064 PubMed PMC

Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27:863–864. doi: 10.1093/bioinformatics/btr026. PubMed DOI PMC

Seidl R, Klonner G, Rammer W, Essl F, Moreno A, Neumann M, Dullinger S. Invasive alien pests threaten the carbon stored in Europe’s forests. Nat Commun. 2018;9:1626. doi: 10.1038/s41467-018-04096-w. PubMed DOI PMC

Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N, Sorenson AL, De S, Kishony R, Michor F, Dowell R, Pellman D. Polyploidy can drive rapid adaptation in yeast. Nature. 2015;519:349–352. doi: 10.1038/nature14187. PubMed DOI PMC

Shakya SK, Grünwald NJ, Fieland VJ, Knaus BJ, Weiland JE, Maia C, Drenth A, Guest DI, Liew ECY, Crane C, Chang T-T, Fu C-H, Minh Chi N, Quang Thu P, Scanu B, von Stowasser ES, Durán Á, Horta Jung M, Jung T. Phylogeography of the wide-host range panglobal plant pathogen Phytophthora cinnamomi. Mol Ecol. 2021;30:5164–5178. doi: 10.1111/mec.16109. PubMed DOI

Solís-Lemus C, Ané C. Inferring phylogenetic networks with maximum pseudolikelihood under incomplete lineage sorting. PLoS Genet. 2016;12:e1005896. doi: 10.1371/journal.pgen.1005896. PubMed DOI PMC

Solís-Lemus C, Bastide P, Ané C. Phylonetworks: a package for phylogenetic networks. Mol Biol Evol. 2017;34:3292–3298. doi: 10.1093/molbev/msx235. PubMed DOI

Soltis PS, Soltis DE. The role of genetic and genomic attributes in the success of polyploids. PNAS. 2000;97:7051–7057. doi: 10.1073/pnas.97.13.7051. PubMed DOI PMC

Soltis PS, Soltis DE. The role of hybridization in plant speciation. Annu Rev Plant Biol. 2009;60:561–588. doi: 10.1146/annurev.arplant.043008.092039. PubMed DOI

Soltis DE, Buggs RJA, Doyle JJ, Soltis PS. What we still don’t know about polyploidy. Taxon. 2010;59:1387–1403. doi: 10.1002/tax.595006. DOI

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Suzui T, Hoshino Y. Collar rot of apple caused by Phytophthora cambivora (Petri) Buism. Jpn J Phytopathol. 1979;45:344–352. doi: 10.3186/jjphytopath.45.344. DOI

Swofford DL (2021) PAUP* (*Phylogenetic Analysis Using PAUP), Version 4a168, 2021. http://phylosolutions.com/paup-test/

Tabima JF, Coffey MD, Zazada IA, Grünwald NJ. Populations of Phytophthora rubi show little differentiation and high rates of migration among states in the western United States. MPMI. 2018;31:614–622. doi: 10.1094/MPMI-10-17-0258-R. PubMed DOI

Telfer KH, Brurberg MB, Herrero M-L, Stensvand A, Talgø V. Phytophthora cambivora found on beech in Norway. For Path. 2015;45:415–425. doi: 10.1111/efp.12215. DOI

Tomura T, Molli SD, Murata R, Ojika M. Universality of the Phytophthora mating hormones and diversity of their production profile. Sci Rep. 2017;7:5007. doi: 10.1038/s41598-017-05380-3. PubMed DOI PMC

Van Poucke K, Franceschini S, Webber JF, Vercauteren A, Turner JA, McCracken AR, Heungens K, Brasier C. Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2. Fungal Biol. 2012;116:1178–1191. doi: 10.1016/j.funbio.2012.09.003. PubMed DOI

Van Poucke K, Haegeman A, Goedefroit T, Focquet F, Leus L, Horta Jung M, Nave C, Redondo MA, Husson C, Kostov K, Lyubenova A, Christova P, Chandelier A, Slavov S, de Cock A, Bonants P, Werres S, Palau JO, Marçais B, Jung T, Stenlid J, Ruttink T, Heungens K. Unravelling hybridization in Phytophthora using phylogenomics and genome size estimation. IMA Fungus. 2021;12:16. doi: 10.1186/s43008-021-00068-w. PubMed DOI PMC

Vannini A, Vettraino AM. Ink disease in chestnuts: impact on the European chestnut. For Snow Landsc Res. 2001;76:345–350.

Vettraino AM, Natili G, Anselmi N, Vannini A. Recovery and pathogenicity of Phytophthora species associated with a resurgence of ink disease in Castanea sativa in Italy: Ink disease in sweet chestnut in Italy. Plant Pathol. 2001;50:90–96. doi: 10.1046/j.1365-3059.2001.00528.x. DOI

Vettraino AM, Morel O, Perlerou C, Robin C, Diamandis S, Vannini A. Occurrence and distribution of Phytophthora species in European chestnut stands, and their association with Ink Disease and crown decline. Eur J Plant Pathol. 2005;111:169–180. doi: 10.1007/s10658-004-1882-0. DOI

Wendel JF, Lisch D, Hu G, Mason AS. The long and short of doubling down: polyploidy, epigenetics, and the temporal dynamics of genome fractionation. Curr Opin Genet Dev. 2018;49:1–7. doi: 10.1016/j.gde.2018.01.004. PubMed DOI

Wicks TJ, Lee TC, Scott ES. Phytophthora crown rot of almonds in Australia 1. EPPO Bull. 1997;27:501–506. doi: 10.1111/j.1365-2338.1997.tb00673.x. DOI

Wilcox WF, Mircetich SM. Pathogenicity and relative virulence of seven Phytophthora spp. on Mahaleb and Mazzard cherry. Phytopathology. 1985;75:221–226. doi: 10.1094/Phyto-75-221. DOI

Wingfield MJ, Brockerhoff EG, Wingfield BD, Slippers B. Planted forest health: the need for a global strategy. Science. 2015;349:832–836. doi: 10.1126/science.aac6674. PubMed DOI

Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 2014;30:614–620. doi: 10.1093/bioinformatics/btt593. PubMed DOI PMC

Phylogeography, origin and population structure of the self-fertile emerging plant pathogen Phytophthora pseudosyringae

Worldwide forest surveys reveal forty-three new species in Phytophthora major Clade 2 with fundamental implications for the evolution and biogeography of the genus and global plant biosecurity