Various hypotheses have been proposed regarding the origin of the plant pathogen Phytophthora cinnamomi. P. cinnamomi is a devastating, highly invasive soilborne pathogen associated with epidemics of agricultural, horticultural and forest plantations and native ecosystems worldwide. We conducted a phylogeographic analysis of populations of this pathogen sampled in Asia, Australia, Europe, southern and northern Africa, South America, and North America. Based on genotyping-by-sequencing, we observed the highest genotypic diversity in Taiwan and Vietnam, followed by Australia and South Africa. Mating type ratios were in equal proportions in Asia as expected for a sexual population. Simulations based on the index of association suggest a partially sexual, semi-clonal mode of reproduction for the Taiwanese and Vietnamese populations while populations outside of Asia are clonal. Ancestral area reconstruction provides new evidence supporting Taiwan as the ancestral area, given our sample, indicating that this region might be near or at the centre of origin for this pathogen as speculated previously. The Australian and South African populations appear to be a secondary centre of diversity following migration from Taiwan or Vietnam. Our work also identified two panglobal, clonal lineages PcG1-A2 and PcG2-A2 of A2 mating type found on all continents. Further surveys of natural forests across Southeast Asia are needed to definitively locate the actual centre of origin of this important plant pathogen.

Bioforest S A Casilla 70 C Concepción Chile

Centre for Horticultural Science The University of Queensland Ecosciences Precinct Brisbane Queensland Australia

Centre of Marine Sciences Faculty of Sciences and Technology University of Algarve Faro Portugal

Department of Agricultural Sciences University of Sassari Sassari Italy

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

Forest Protection Division Taiwan Forestry Research Institute Taipei Taiwan

Forest Protection Research Centre Vietnamese Academy of Forest Sciences Hanoi Vietnam

Horticultural Crop Research Unit United States Department of Agriculture Agricultural Research Service Corvallis Oregon USA

Laboratorio de Patología Forestal Facultad Ciencias Forestales y Centro de Biotecnología Universidad de Concepción Concepción Chile

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

Research and Development Asia Pacific Resources International Limited Pangkalan Kerinci Indonesia

Research Centre for Ecosystem Resilience Australian Institute of Botanical Science The Royal Botanic Gardens and Domain Trust Sydney NSW Australia

Sydney Institute of Agriculture School of Life and Environmental Sciences The University of Sydney NSW Australia

Vegetation Health Service Kensington Washington Australia

Zobrazit více v PubMed

Alexander, D. H., Novembre, J., & Lange, K. (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19(9), 1655-1664. https://doi.org/10.1101/gr.094052.109

Arentz, F. (2017). Phytophthora cinnamomi A1: An ancient resident of New Guinea and Australia of Gondwanan origin? Forest Pathology, 47(4), e12342. https://doi.org/10.1111/efp.12342

Arentz, F., & Simpson, J. A. (1986). Distribution of Phytophthora cinnamomi in Papua New Guinea and notes on its origin. Transactions of the British Mycological Society, 87(2), 289-295. https://doi.org/10.1016/S0007-1536(86)80032-8

Balci, Y., Balci, S., Eggers, J., MacDonald, W. L., Juzwik, J., Long, R. P., & Gottschalk, K. W. (2007). Phytophthora spp. Associated with forest soils in eastern and north-central U.S. oak ecosystems. Plant Disease, 91(6), 705-710. https://doi.org/10.1094/PDIS-91-6-0705

Beakes, G. W., Honda, D., & Thines, M. (2014). Systematics of the Straminipila: Labyrinthulomycota, Hyphochytriomycota, and Oomycota. In D. J. McLaughlin, & J. W. Spatafora (Eds.), Systematics and Evolution: Part A (pp. 39-97). Springer. https://doi.org/10.1007/978-3-642-55318-9_3

Beaulieu, J., Ford, B., & Balci, Y. (2017). Genotypic diversity of Phytophthora cinnamomi and P. plurivora in Maryland’s nurseries and Mid-Atlantic forests. Phytopathology, 107(6), 769-776. https://doi.org/10.1094/PHYTO-05-16-0215-R

Beerli, P. (1998). Estimation of migration rates and population sizes in geographically structured populations. NATO ASI Series A Life Sciences, 306, 39-54.

Beerli, P. (2009). How to use MIGRATE or why are Markov chain Monte Carlo programs difficult to use? In G. Bertorelle, M. W. Bruford, H. C. Hauffe, A. Rizzoli, & C. Vernesi (Eds.), Population Genetics for Animal Conservation (pp. 42-79). Cambridge University Press. https://doi.org/10.1017/CBO9780511626920.004

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, 98(8), 4563-4568. https://doi.org/10.1073/pnas.081068098

Bienapfl, J. C., & Balci, Y. (2014). Movement of Phytophthora spp. Maryland’s Nursery trade. Plant Disease, 98(1), 134-144. https://doi.org/10.1094/PDIS-06-13-0662-RE

Brar, S., Tsui, C. K. M., Dhillon, B., Bergeron, M.-J., Joly, D. L., Zambino, P. J., El-Kassaby, Y. A., Hamelin, R. C. (2015). Colonization history, host distribution, anthropogenic influence and landscape features shape populations of white pine blister rust, an invasive alien tree pathogen. PLoS One, 10(5), e0127916. https://doi.org/10.1371/journal.pone.0127916

Brasier, C. M. (2008). The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology, 57(5), 792-808. https://doi.org/10.1111/j.1365-3059.2008.01886.x

Brasier, C. M., Franceschini, S., Vettraino, A., Hansen, E. M., Green, S., Robin, C., Webber, J. F., Vannini, A. (2012). Four phenotypically and phylogenetically distinct lineages in Phytophthora lateralis. Fungal Biology, 116, 1232-1249. https://doi.org/10.1016/j.funbio.2012.10.002

Brasier, C. M., Robredo, F., & Ferraz, J. F. P. (1993). Evidence for Phytophthora cinnamomi involvement in Iberian oak decline. Plant Pathology, 42(1), 140-145. https://doi.org/10.1111/j.1365-3059.1993.tb01482.x

Burgess, T. I., & Wingfield, M. J. (2017). Pathogens on the move: A 100-year global experiment with planted Eucalypts. BioScience, 67(1), 14-25. https://doi.org/10.1093/biosci/biw146

Cahill, D. M., Rookes, J. E., Wilson, B. A., Gibson, L., & McDougall, K. L. (2008). Phytophthora cinnamomi and Australia’s biodiversity: Impacts, predictions and progress towards control. Australian Journal of Botany, 56(4), 279-310. https://doi.org/10.1071/BT07159

Chang, T. T., Yang, W. W., & Wang, W. Y. (1996). Use of random amplified polymorphic DNA markers for the detection of genetic variation in Phytophthora cinnamomi in Taiwan. Botanical Bulletin- Academia Sinica, 37, 165-171.

Cooke, D. E., Drenth, A., Duncan, J. M., Wagels, G., & Brasier, C. M. (2000). A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology, 30(1), 17-32. https://doi.org/10.1006/fgbi.2000.1202

Crandall, B. S., & Gravatt, G. F. (1967). The distribution of Phytophthora cinnamomi. Ceiba, 13, 43-53.

Cui, L., Gao, P., Guo, J., Kang, Y., & Hu, Y. (2018). Mating type and sensitivity of Phytophthora nicotianae from tobacco to metalaxyl and dimethomorph in Henan province, China. Journal of Phytopathology, 166(9), 648-653. https://doi.org/10.1111/jph.12727

Dobrowolski, M. P., Tommerup, I. C., Shearer, B. L., & O’Brien, P. A. (2003). Three clonal lineages of Phytophthora cinnamomi in Australia revealed by microsatellites. Phytopathology, 93(6), 695-704.

Drenth, A., & D. I. Guest (Eds.) (2004). Diversity and management of Phytophthora in Southeast Asia. Australian Centre for International Agricultural Research.

Drenth, A., McTaggart, A. R., & Wingfield, B. D. (2019). Fungal clones win the battle, but recombination wins the war. IMA Fungus, 10(1), 18. https://doi.org/10.1186/s43008-019-0020-8

Drenth, A., Turkensteen, L. J., & Govers, F. (1993). The occurrence of the A2 mating type of Phytophthora infestans in the Netherlands; significance and consequences. Netherlands Journal of Plant Pathology, 99(S3), 57-67. https://doi.org/10.1007/BF03041396

Drew, J., Anderson, N., & Andow, D. (2010). Conundrums of a complex vector for invasive species control: A detailed examination of the horticultural industry. Biological Invasions, 12(8), 2837-2851. https://doi.org/10.1007/s10530-010-9689-8

Durán, A., Gryzenhout, M., Slippers, B., Ahumada, R., Rotella, A., Flores, F., Wingfield, B. D., Wingfield, M. J. (2008). Phytophthora pinifolia sp. Nov. Associated with a serious needle disease of Pinus radiata in Chile. Plant Pathology, 57(4), 715-727. https://doi.org/10.1111/j.1365-3059.2008.01893.x

Eggers, J. E., Balci, Y., & MacDonald, W. L. (2012). Variation among Phytophthora cinnamomi isolates from oak forest soils in the eastern United States. Plant Disease, 96(11), 1608-1614.

Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J. A., Kawamoto, K., Buckler, E. S., & Mitchell, S. E. (2011). A robust, simple Genotyping-by-Sequencing (GBS) approach for high diversity species. PLoS One, 6(5), e19379. https://doi.org/10.1371/journal.pone.0019379

Engelbrecht, J., Duong, T. A., Berg, N. V. D. (2017). New microsatellite markers for population studies of Phytophthora cinnamomi, an important global pathogen. Scientific Reports, 7(1), 17631. https://doi.org/10.1038/s41598-017-17799-9

Erwin, D. C., & Ribeiro, O. K. (1996). Phytophthora diseases worldwide. American Phytopathological Society Press.

Flier, W. G., Grünwald, N. J., Kroon, L. P. N. M., Sturbaum, A. K., van den Bosch, T. B. M., Garay-Serrano, E., Lozoya-Saldaña, H., Fry, W. E., Turkensteen, L. J. (2003). The population structure of Phytophthora infestans from the Toluca valley of Central Mexico suggests genetic differentiation between populations from cultivated potato and wild Solanum spp. Phytopathology, 93(4), 382-390. https://doi.org/10.1094/PHYTO.2003.93.4.382

Goodwin, S. B. (1997). The population genetics of Phytophthora. Phytopathology, 87(4), 462-473.

Goss, E. M., Cooke, D. E. L., Restrepo, S., Fry, W. E., Forbes, G. A., Fieland, V. J., Cardenas, M., & Grünwald, N. J. (2014). The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. Proceedings of the National Academy of Sciences, 111(24), 8791-8796. https://doi.org/10.1073/pnas.1401884111

Goss, E. M., Larsen, M., Chastagner, G. A., Givens, D. R., & Grünwald, N. J. (2009). Population genetic analysis infers migration pathways of Phytophthora ramorum in US nurseries. PLoS Path, 5(9), e1000583. https://doi.org/10.1371/journal.ppat.1000583

Gross, A., Holdenrieder, O., Pautasso, M., Queloz, V., & Sieber, T. N. (2014). Hymenoscyphus pseudoalbidus, the causal agent of European ash dieback. Molecular Plant Pathology, 15(1), 5-21. https://doi.org/10.1111/mpp.12073

Grünwald, N. J., & Flier, W. G. (2005). The biology of Phytophthora infestans at its center of origin. Annual Review of Phytopathology, 43, 171-190. https://doi.org/10.1146/annurev.phyto.43.040204.135906

Grünwald, N. J., Flier, W. G., Sturbaum, A. K., Garay-Serrano, E., van den Bosch, T. B. M., Smart, C. D., Matuszak, J. M., Lozoya-Saldaña, H., & Turkensteen, L. J., Fry, W. E. (2001). Population structure of Phytophthora infestans in the Toluca valley region of central Mexico. Phytopathology, 91(9), 882-890. https://doi.org/10.1094/PHYTO.2001.91.9.882

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(3), 131-138. https://doi.org/10.1016/j.tim.2011.12.006

Grünwald, N. J., Goss, E. M., Ivors, K., Garbelotto, M., Martin, F. N., Prospero, S., Hansen, E., Bonants, P. J. M., Hamelin, R. C., Chastagner, G., Werres, S., Rizzo, D. M., Abad, G., Beales, P., Bilodeau, G. J., Blomquist, C. L., Brasier, C., Brière, S. C., Chandelier, A., … Widmer, T. L. (2009). Standardizing the nomenclature for clonal lineages of the sudden oak death pathogen, Phytophthora ramorum. Phytopathology, 99(7), 792-795. https://doi.org/10.1094/PHYTO-99-7-0792

Grünwald, N. J., Martin, F. N., Larsen, M. M., Sullivan, C. M., Press, C. M., Coffey, M. D., Hansen, E. M., Parke, J. L. (2010). Phytophthora-ID.org: A sequence-based Phytophthora identification tool. Plant Disease, 95(3), 337-342. https://doi.org/10.1094/PDIS-08-10-0609

Grünwald, N. J., McDonald, B. A., & Milgroom, M. G. (2016). Population genomics of fungal and oomycete pathogens. Annual Review of Phytopathology, 54(1), 323-346. https://doi.org/10.1146/annurev-phyto-080614-115913

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(1), 4-14. https://doi.org/10.1094/PDIS.2000.84.1.4

Hardham, A. R., & Blackman, L. M. (2018). Phytophthora cinnamomi. Molecular Plant Pathology, 19(2), 260-285. https://doi.org/10.1111/mpp.12568

Jombart, T., & Ahmed, I. (2011). adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics, 27(21), 3070-3071. https://doi.org/10.1093/bioinformatics/btr521

Jung, T., Blaschke, H., & Neumann, P. (1996). Isolation, identification and pathogenicity of Phytophthora species from declining oak stands. European Journal of Forest Pathology, 26(5), 253-272. https://doi.org/10.1111/j.1439-0329.1996.tb00846.x

Jung, T., Chang, T. T., Bakonyi, J., Seress, D., Pérez-Sierra, A., Yang, X., Hong, C., Scanu, B., Fu, C. H., Hsueh, K. L., Maia, C., Abad-Campos, P., & Léon, M., Horta Jung, M. (2017). Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathology, 66(2), 194-211. https://doi.org/10.1111/ppa.12564

Jung, T., Colquhoun, I. J., & Hardy, G. E. (2013). New insights into the survival strategy of the invasive soilborne pathogen Phytophthora cinnamomi in different natural ecosystems in Western Australia. Forest Pathology, 43(4), 266-288. https://doi.org/10.1111/efp.12025

Jung, T., & Dobler, G. (2002). First Report of Littleleaf disease caused by Phytophthora cinnamomi on Pinus occidentalis in the Dominican Republic. Plant Disease, 86(11), 1275. https://doi.org/10.1094/PDIS.2002.86.11.1275C

Jung, T., Durán, A., von Stowasser, E. S., Schena, L., Mosca, S., Fajardo, S., Mariela, G., Angella D., N. O., Jozsef, B., Diana, S., Michal, T., Alfredo, C., Cristiana, M., Marilia, H. J., Jung, M. H. (2018). Diversity of Phytophthora species in Valdivian rainforests and association with severe dieback symptoms. Forest Pathology, 48(5), e12443. https://doi.org/10.1111/efp.12443

Jung, T., Horta Jung, M., Webber, J. F., Kageyama, K., Hieno, A., Masuya, H., Uematsu, S., Pérez-Sierra, A., Harris, A. R., Forster, J., Rees, H., Scanu, B., Patra, S., Kudláček, T., Janoušek, J., Corcobado, T., Milenković, I., Nagy, Z., Csorba, I., … Brasier, C. M. (2021). The destructive tree pathogen Phytophthora ramorum originates from the laurosilva forests of East Asia. Journal of Fungi, 7(3), 226. https://doi.org/10.3390/jof7030226

Jung, T., Orlikowski, L., Henricot, B., Abad-Campos, P., Aday, A. G., Casal, O. A., Bakonyi, J., Cacciola, S. O., Cech, T., Chavarriaga, D., Corcobado, T., Cravador, A., Decourcelle, T., Denton, G., Diamandis, S., Dogmus-Lehtijaervi, H. T., Franceschini, A., Ginetti, B., Green, S., Glavendekic, M., … Peréz-Sierra, A. (2016). Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology, 46(2), 134-163. https://doi.org/10.1111/efp.12239

Jung, T., Pérez-Sierra, A., Durán, A., Horta Jung, M., Balci, Y., & Scanu, B. (2018). Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia, 40, 182-220. https://doi.org/10.3767/persoonia.2018.40.08

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(1), 93. https://doi.org/10.3390/f11010093

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. https://doi.org/10.3389/fgene.2015.00208

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. https://doi.org/10.7717/peerj.281

Kass, R. E., & Raftery, A. E. (1995). Bayes Factors. Journal of the American Statistical Association, 90(430), 773-795. https://doi.org/10.1080/01621459.1995.10476572

Knaus, B. J., & Grünwald, N. J. (2017). vcfr: A package to manipulate and visualize variant call format data in R. Molecular Ecology Resources, 17(1), 44-53. https://doi.org/10.1111/1755-0998.12549

Ko, W. H. (1979). Mating-type distribution of Phytophthora colocasiae on the island of Hawaii. Mycologia, 71(2), 434. https://doi.org/10.2307/3759163

Ko, W. H., Chang, H. S., & Su, H. J. (1978). Isolates of Phytophthora cinnamomi from Taiwan as evidence for an Asian origin of the species. Transactions of the British Mycological Society, 71(3), 496-499. https://doi.org/10.1016/S0007-1536(78)80080-1

Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4), 357-359. https://doi.org/10.1038/nmeth.1923

Lemey, P., Rambaut, A., Drummond, A. J., & Suchard, M. A. (2009). Bayesian Phylogeography finds its roots. PLOS Computational Biology, 5(9), e1000520. https://doi.org/10.1371/journal.pcbi.1000520

Lewis, P. O. (2001). A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology, 50(6), 913-925. https://doi.org/10.1080/106351501753462876

Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., & Durbin, R. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25(16), 2078-2079. https://doi.org/10.1093/bioinformatics/btp352

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(3), 135-143. https://doi.org/10.1890/110198

Linde, C., Drenth, A., Kemp, G. H. J., Wingfield, M. J., & Von Broembsen, S. L. (1997). Population structure of Phytophthora cinnamomi in South Africa. Phytopathology, 87(8), 822-827.

Linde, C., Drenth, A., & Wingfield, M. J. (1999). Gene and genotypic diversity of Phytophthora cinnamomi in South Africa and Australia revealed by DNA polymorphisms. European Journal of Plant Pathology, 105(7), 667-680. https://doi.org/10.1023/A:1008755532135

Linde, C., Soo, S. H., & Drenth, A. (2001). Sexual recombination in Phytophthora cinnamomi in vitro and aggressiveness of single-oospore progeny to Eucalyptus: Single oospore progeny of P. cinnamomi. Plant Pathology, 50(1), 97-102. https://doi.org/10.1046/j.1365-3059.2001.00530.x

Longmuir, A. L., Beech, P. L., & Richardson, M. F. (2017). Draft genomes of two Australian strains of the plant pathogen, Phytophthora cinnamomi. F1000Research, 6, 1972. https://doi.org/10.12688/f1000research.12867.1

McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., DePristo, M. A. (2010). The Genome Analysis Toolkit: A mapreduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20(9), 1297-1303. https://doi.org/10.1101/gr.107524.110

McMullan, M., Rafiqi, M., Kaithakottil, G., Clavijo, B. J., Bilham, L., Orton, E., Percival-Alwyn, L., Ward, B. J., Edwards, A., Saunders, D. G. O., Garcia Accinelli, G., Wright, J., Verweij, W., Koutsovoulos, G., Yoshida, K., Hosoya, T., Williamson, L., Jennings, P., Ioos, R., … Clark, M. D. (2018). The ash dieback invasion of Europe was founded by two genetically divergent individuals. Nature Ecology & Evolution, 2(6), 1000. https://doi.org/10.1038/s41559-018-0548-9

O’Hanlon, S. J., Rieux, A., Farrer, R. A., Rosa, G. M., Waldman, B., Bataille, A., Kosch, T. A., Murray, K. A., Brankovics, B., Fumagalli, M., Martin, M. D., Wales, N., Alvarado-Rybak, M., Bates, K. A., Berger, L., Böll, S., Brookes, L., Clare, F., Courtois, E. A., … Fisher, M. C. (2018). Recent Asian origin of chytrid fungi causing global amphibian declines. Science, 360(6389), 621-627. https://doi.org/10.1126/science.aar1965

Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., & Wagner, H. (2016). vegan: Community Ecology Package. Retrieved from https://CRAN.R-project.org/package=vegan

Old, K. M., Dudzinski, M. J., & Bell, J. C. (1988). Isozyme variability in field populations of Phytophthora cinnamomi in Australia. Australian Journal of Botany, 36(3), 355-360. https://doi.org/10.1071/BT9880355

Old, K. M., Moran, G. F., & Bell, J. C. (1984). Isozyme variability among isolates of Phytophthora cinnamomi from Australia and Papua New Guinea. Canadian Journal of Botany, 62(10), 2016-2022. https://doi.org/10.1139/b84-274

Pagliaccia, D., Pond, E., McKee, B., & Douhan, G. W. (2013). Population genetic structure of Phytophthora cinnamomi associated with avocado in California and the discovery of a potentially recent introduction of a new clonal lineage. Phytopathology, 103(1), 91-97. https://doi.org/10.1094/PHYTO-01-12-0016-R

Paradis, E., Claude, J., & Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20(2), 289-290. https://doi.org/10.1093/bioinformatics/btg412

Parke, J., Knaus, B. J., Fieland, V. J., Lewis, C., & Grünwald, N. J. (2014). Phytophthora community structure analyses in Oregon nurseries inform systems approaches to disease management. Phytopathology, 104(10), 1052-1062. https://doi.org/10.1094/PHYTO-01-14-0014-R

Pratt, B. H., & Heather, W. A. (1973). The origin and distribution of Phytophthora cinnamomi Rands in Australian native plant communities and the significance of its association with particular plant species. Australian Journal of Biological Sciences, 26(3), 559-574. https://doi.org/10.1071/BI9730559

Pratt, B. H., Heather, W. A., & Shepherd, C. J. (1973). Recovery of Phytophthora cinnamomi from native vegetation in a remote area of New South Wales. Transactions of the British Mycological Society, 60(2), 197-204. https://doi.org/10.1016/S0007-1536(73)80003-8

Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945-959. https://doi.org/10.1093/genetics/155.2.945

Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., Sham, P. C. (2007). PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81(3), 559-575. https://doi.org/10.1086/519795

Rands, R. D. (1922). Streepkanker van Kaneel, veroorzaakt door Phytophthora cinnamomi n. Sp. (Stripe canker of cinnamon caused by Phytophthora cinnamomi n. Sp.). Medeelingen van het Instituut voor Plantenziekten.

Ree, R. H., & Smith, S. A. (2008). Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology, 57(1), 4-14. https://doi.org/10.1080/10635150701883881

Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217-223. https://doi.org/10.1111/j.2041-210X.2011.00169.x

Revell, L. J. (2014). Ancestral character estimation under the threshold model from quantitative genetics. Evolution, 68(3), 743-759. https://doi.org/10.1111/evo.12300

Rigling, D., & Prospero, S. (2018). Cryphonectria parasitica, the causal agent of chestnut blight: Invasion history, population biology and disease control. Molecular Plant Pathology, 19(1), 7-20. https://doi.org/10.1111/mpp.12542

Santini, A., Ghelardini, L., Pace, C. D., Desprez-Loustau, M. L., 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., … Stenlid, J. (2013). Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytologist, 197(1), 238-250. https://doi.org/10.1111/j.1469-8137.2012.04364.x

Santos, Á. F. D., Tessmann, D. J., Alves, T. C. A., Vida, J. B., & Harakava, R. (2011). Root and crown rot of Brazilian pine (Araucaria angustifolia) caused by Phytophthora cinnamomi. Journal of Phytopathology, 159(3), 194-196. https://doi.org/10.1111/j.1439-0434.2010.01741.x

Scanu, B., Hunter, G. C., Linaldeddu, B. T., Franceschini, A., Maddau, L., Jung, T., & Denman, S. (2014). A taxonomic re-evaluation reveals that Phytophthora cinnamomi and P. cinnamomi var. Parvispora are separate species. Forest Pathology, 44(1), 1-20. https://doi.org/10.1111/efp.12064

Shakya, S. K., Larsen, M. M., Cuenca-Condoy, M. M., Lozoya-Saldaña, H., & Grünwald, N. J. (2018). Variation in genetic diversity of Phytophthora infestans populations in Mexico from the center of origin outwards. Plant Disease, 102(8), 1534-1540. https://doi.org/10.1094/PDIS-11-17-1801-RE

Shearer, B. L., Crane, C. E., Barrett, S., & Cochrane, A. (2007). Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia. Australian Journal of Botany, 55(3), 225. https://doi.org/10.1071/BT06019

Shearer, B. L., Crane, C. E., & Cochrane, A. (2004). Quantification of the susceptibility of the native flora of the South-West Botanical Province, Western Australia, to Phytophthora cinnamomi. Australian Journal of Botany, 52(4), 435. https://doi.org/10.1071/BT03131

Shearer, B. L., & Tippett, J. T. (1989). Jarrah dieback: The dynamics and management of Phytophthora cinnamomi in the jarrah (Eucalyptus marginata) forest of south-western Australia. Dept. of Conservation and Land Management.

Shepherd, C. J. (1975). Phytophthora cinnamomi-An ancient immigrant to Australia. Search, 6, 484-490.

Socorro Serrano, M., Osmundson, T., Almaraz-Sánchez, A., Croucher, P. J. P., Swiecki, T., Alvarado-Rosales, D., & Garbelotto, M. (2019). A microsatellite analysis used to identify global pathways of movement of Phytophthora cinnamomi and the likely sources of wildland infestations in California and Mexico. Phytopathology®, 109(9), 1577-1593. https://doi.org/10.1094/PHYTO-03-19-0102-R

Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22(21), 2688-2690. https://doi.org/10.1093/bioinformatics/btl446

Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312-1313. https://doi.org/10.1093/bioinformatics/btu033

Studholme, D. J., McDougal, R. L., Sambles, C., Hansen, E., Hardy, G., Grant, M., Ganley, R. J., & Williams, N. M. (2015). Genome sequences of six Phytophthora species associated with forests in New Zealand. Genomics Data, 7, 54-56. https://doi.org/10.1016/j.gdata.2015.11.015

Stukenbrock, E. H., & McDonald, B. A. (2008). The origins of plant pathogens in agro-ecosystems. Annual Review of Phytopathology, 46(1), 75-100. https://doi.org/10.1146/annurev.phyto.010708.154114

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(6), 614-622. https://doi.org/10.1094/MPMI-10-17-0258-R

Tainter, F. H., O’Brien, J. G., Hernández, A., Orozco, F., & Rebolledo, O. (2000). Phytophthora cinnamomi as a cause of oak mortality in the State of Colima, Mexico. Plant Disease, 84(4), 394-398. https://doi.org/10.1094/PDIS.2000.84.4.394

Truong, N. V., Liew, E. C. Y., & Burgess, L. W. (2010). Characterisation of Phytophthora capsici isolates from black pepper in Vietnam. Fungal Biology, 114(2-3), 160-170. https://doi.org/10.1016/j.funbio.2009.11.005

Van Poucke, K., Franceschini, S., Webber, J. F., Vercauteren, A., Turner, J. A., McCracken, A. R., Heungens, K., & Brasier, C. M. (2012). Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2. Fungal Biology, 116(11), 1178-1191. https://doi.org/10.1016/j.funbio.2012.09.003

Vettraino, A. M., Morel, O., Perlerou, C., Robin, C., Diamandis, S., & Vannini, A. (2005). Occurrence and distribution of Phytophthora species in European chestnut stands, and their association with Ink Disease and crown decline. European Journal of Plant Pathology, 111(2), 169. https://doi.org/10.1007/s10658-004-1882-0

Weiland, J. E., Scagel, C. F., Grünwald, N. J., Davis, E. A., Beck, B. R., Foster, Z. S. L., & Fieland, V. J. (2020). Soilborne Phytophthora and Pythium diversity from rhododendron in propagation, container, and field production systems of the Pacific Northwest. Plant Disease, 104(6), 1841-1850. https://doi.org/10.1094/PDIS-08-19-1672-RE

White, T., Bruns, T., Lee, S., Taylor, F. J. R. M., White, T. J., Lee, S.-H., Taylor, L., Shawe-Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: A guide to methods and applications. Retrieved from https://www.scienceopen.com/document?vid=36d59e39-6250-4a7f-b5fe-7155abbb4e03

Wickland, D. P., Battu, G., Hudson, K. A., Diers, B. W., & Hudson, M. E. (2017). A comparison of genotyping-by-sequencing analysis methods on low-coverage crop datasets shows advantages of a new workflow, GB-eaSy. BMC Bioinformatics, 18(1), 586. https://doi.org/10.1186/s12859-017-2000-6

Yang, X., Tyler, B. M., & Hong, C. (2017). An expanded phylogeny for the genus Phytophthora. IMA Fungus, 8(2), 355-384. https://doi.org/10.5598/imafungus.2017.08.02.09

Zentmyer, G. A. (1988). Origin and distribution of four species of Phytophthora. Transactions of the British Mycological Society, 91(3), 367-378. https://doi.org/10.1016/S0007-1536(88)80111-6

The virome of the panglobal, wide host-range plant pathogen Phytophthora cinnamomi: phylogeography and evolutionary insights

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

Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora × cambivora

Extensive morphological and behavioural diversity among fourteen new and seven described species in Phytophthora Clade 10 and its evolutionary implications

Eight new Halophytophthora species from marine and brackish-water ecosystems in Portugal and an updated phylogeny for the genus

Genera of phytopathogenic fungi: GOPHY 4

Differences in the Proteomic and Metabolomic Response of Quercus suber and Quercus variabilis During the Early Stages of Phytophthora cinnamomi Infection

Phytophthora heterospora sp. nov., a New Pseudoconidia-Producing Sister Species of P. palmivora