Extensive morphological and behavioural diversity among fourteen new and seven described species in Phytophthora Clade 10 and its evolutionary implications
Status PubMed-not-MEDLINE Jazyk angličtina Země Nizozemsko Médium print-electronic
Typ dokumentu časopisecké články
PubMed
38234379
PubMed Central
PMC10792230
DOI
10.3767/persoonia.2022.49.01
Knihovny.cz E-zdroje
- Klíčová slova
- Gondwana, Laurasia, Oomycete, allopatric, biogeography, evolution, phylogeny, radiation, sympatric,
- Publikační typ
- časopisecké články MeSH
During extensive surveys of global Phytophthora diversity 14 new species detected in natural ecosystems in Chile, Indonesia, USA (Louisiana), Sweden, Ukraine and Vietnam were assigned to Phytophthora major Clade 10 based on a multigene phylogeny of nine nuclear and three mitochondrial gene regions. Clade 10 now comprises three subclades. Subclades 10a and 10b contain species with nonpapillate sporangia, a range of breeding systems and a mainly soil- and waterborne lifestyle. These include the previously described P. afrocarpa, P. gallica and P. intercalaris and eight of the new species: P. ludoviciana, P. procera, P. pseudogallica, P. scandinavica, P. subarctica, P. tenuimura, P. tonkinensis and P. ukrainensis. In contrast, all species in Subclade 10c have papillate sporangia and are self-fertile (or homothallic) with an aerial lifestyle including the known P. boehmeriae, P. gondwanensis, P. kernoviae and P. morindae and the new species P. celebensis, P. chilensis, P. javanensis, P. multiglobulosa, P. pseudochilensis and P. pseudokernoviae. All new Phytophthora species differed from each other and from related species by their unique combinations of morphological characters, breeding systems, cardinal temperatures and growth rates. The biogeography and evolutionary history of Clade 10 are discussed. We propose that the three subclades originated via the early divergence of pre-Gondwanan ancestors > 175 Mya into water- and soilborne and aerially dispersed lineages and subsequently underwent multiple allopatric and sympatric radiations during their global spread. Citation: Jung T, Milenković I, Corcobado T, et al. 2022. Extensive morphological and behavioural diversity among fourteen new and seven described species in Phytophthora Clade 10 and its evolutionary implications. Persoonia 49: 1-57. https://doi.org/10.3767/persoonia.2022.49.01.
Center for Plant Protection Croatian Agency for Agriculture and Food 10000 Zagreb Croatia
Centre of Marine Sciences University of Algarve 8005 139 Faro Portugal
Department of Agricultural Sciences University of Sassari Viale Italia 39A 07100 Sassari Italy
Department of Agriculture Food and the Marine Dublin 2 D02 WK12 Ireland
Department of Crop and Forest Sciences University of Lleida Lleida 25198 Spain
Forest Protection Research Centre Vietnamese Academy of Forest Sciences 10000 Hanoi Vietnam
Forest Research Alice Holt Lodge Farnham Surrey GU10 4LH UK
Forestry and Forest Products Research Institute Tsukuba Ibaraki 305 8687 Japan
Phytophthora Research and Consultancy 83131 Nussdorf Germany
River Basin Research Center Gifu University Gifu 501 1193 Japan
Ukrainian National Forestry University Pryrodna st 19 79057 Lviv Ukraine
University of Belgrade Faculty of Forestry 11030 Belgrade Serbia
Zobrazit více v PubMed
Adami M, Bernardes S, Arai E, et al. 2018. Seasonality of vegetation types of South America depicted by moderate resolution imaging spectroradiometer (MODIS) time series. International Journal of Applied Earth Observation and Geoinformation 69: 148–163.
Adams GC, Catal M, Trummer L. 2010. Distribution and severity of alder Phytophthora in Alaska. In: Frankel SJ, Kliejunas T, Palmieri KM. (eds), Proceedings of the Sudden Oak Death Fourth Science Symposium, USDA Forest Service, Albany, California, USA. General Technical Report PSW-GTR-229: 29–49.
Aguayo J, Adams GC, Halkett F, et al. 2013. Strong genetic differentiation between North American and European populations of Phytophthora alni subsp. uniformis. Phytopathology 103: 190–199. PubMed
Anonymous 2010. Phytophthora kernoviae: A threat to our woodlands, heathlands and historic gardens. Plant Disease Fact Sheet. The Food and Environment Research Agency, Sand Hutton, York, UK.
Armesto J, Villagrán C, Arroyo MTK. 1995. Ecología de los bosques nativos de Chile. Santiago, Editorial Universitaria.
Atchadé YF, Roberts GO, Rosenthal JS. 2011. Towards optimal scaling of metropolis-coupled Markov chain Monte Carlo. Statistics and Computing 21: 555–568.
Balci Y, Balci S, Eggers J, et al. 2007. Phytophthora spp. associated with forest soils in Eastern and North-Central U.S. oak ecosystems. Plant Disease 91: 705–710. PubMed
Balci Y, Halmschlager E. 2003. Phytophthora species in oak ecosystems in Turkey and their association with declining oak trees. Plant Pathology 52: 694–702.
Baskin JM, Baskin CC. 2016. Origins and relationships of the mixed mesophytic forest of Oregon–Idaho, China, and Kentucky: Review and synthesis. Annals of the Missouri Botanical Garden 101: 525–552.
Bertier L, Leus L, D’hondt L, et al. 2013. Host adaptation and speciation through hybridization and polyploidy in Phytophthora. PloS ONE 8: e85385. PubMed PMC
Blair JE, Coffey MD, Park S-Y, et al. 2008. A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology 45: 266–277. PubMed
Bose T, Hulbert JM, Burgess TI, et al. 2021. Two novel Phytophthora species from the southern tip of Africa. Mycological Progress 20: 755–767.
Bouckaert R, Drummond A. 2017. bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology 17: 42. PubMed PMC
Bouckaert R, Heled J, Kühnert D, et al. 2014. BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10: e1003537. PubMed PMC
Bourret TB, Choudhury RA, Mehl HK, et al. 2018. Multiple origins of downy mildews and mito-nuclear discordance within the paraphyletic genus Phytophthora. PLoS ONE 13: e0192502. PubMed PMC
Brasier CM. 1986. The dynamics of fungal speciation. In: Rayner ADM, Brasier CM, Moore D. (eds), Evolutionary biology of the fungi: 231- 260. Cambridge University Press, Cambridge, UK.
Brasier CM. 2000. Rise of the hybrid fungi. Nature 405: 134–135. PubMed
Brasier CM. 2001. Rapid evolution of introduced plant pathogens via interspecific hybridization. Bioscience 51: 123–133.
Brasier CM, Beales PA, Kirk SA, et al. 2005. Phytophthora kernoviae sp. nov. an invasive pathogen causing bleeding stem lesions on forest trees and foliar necrosis of ornamentals in Britain. Mycological Research 109: 853–859. PubMed
Brasier CM, Cooke DEL, Duncan JM. 1999. Origins of a new Phytophthora pathogen through interspecific hybridisation. Proceedings of the National Academy of Sciences, USA 96: 5878–5883. PubMed PMC
Brasier CM, Cooke DEL, Duncan JM, et al. 2003. 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. Mycological Research 107: 277–290. PubMed
Brasier CM, Kirk SA, Delcan J, et al. 2004. Phytophthora alni sp. nov. and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycological Research 108: 1172–1184. PubMed
Brasier CM, Rayner ADM. 1987. Whither terminology below the species level in the fungi? In: Rayner ADM, Brasier CM, Moore D. (eds), Evolutionary biology of the fungi: 379-388. Cambridge University Press, Cambridge, UK.
Brasier CM, Webber J. 2010. Sudden larch death. Nature 466: 824–825. PubMed
Brazee NJ, Wick RL, Hulvey JP. 2016. Phytophthora species recovered from the Connecticut River valley in Massachusetts, USA. Mycologia 108: 6–19. PubMed
Burgess TI. 2015. Molecular characterization of natural hybrids formed between five related indigenous Clade 6 Phytophthora species. PLoS ONE 10: e0134225. PubMed PMC
Burgess TI, Edwards J, Drenth A, et al. 2021. Current status of Phytophthora in Australia. Persoonia 47: 151–177. PubMed
Burgess TI, White D, McDougall KM, et al. 2017. Distribution and diversity of Phytophthora across Australia. Pacific Conservation Biology 23: 1–13.
Català S, Pérez-Sierra A, Abad-Campos P. 2015. The use of genus-specific amplicon pyrosequencing to assess Phytophthora species diversity using eDNA from soil and water in Northern Spain. PLoS ONE 10: e0119311. PubMed PMC
Chen Q, Bakhshi M, Balci Y. et al. 2022. Genera of phytopathogenic fungi: GOPHY 4. Studies in Mycology 101: 417–564. PubMed PMC
Chen Y, Roxby R. 1996. Characterization of a Phytophthora infestans gene involved in vesicle transport. Gene 181: 89–94. PubMed
Chowdappa P, Madhura S, Nirmal Kumar BJ, et al. 2014. Phytophthora boehmeriae revealed as the dominant pathogen responsible for severe foliar blight of Capsicum annuum in South India. Plant Disease 98: 90–98. PubMed
Cooke DE, Drenth A, Duncan JM, et al. 2000. A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology 30: 17–32. PubMed
Corcobado T, Cech TL, Brandstetter M, et al. 2020. Decline of European beech in Austria: Involvement of Phytophthora spp. and contributing biotic and abiotic factors. Forests 11: 895.
Crous PW, Wingfield MJ, Le Roux JJ, et al. 2015. Fungal Planet description sheets: 371–399. Persoonia 35: 264–327. PubMed PMC
Ďatková H. 2020. Phytophthora diversity in forest streams of Moravia and Slovakia. Masters Thesis, Mendel University in Brno, Czech Republic.
Davis CC, Bell CD, Mathews S, et al. 2002. Laurasian migration explains Gondwanan disjunctions: Evidence from Malpighiaceae. Proceedings of the National Academy of Sciences USA 99: 6833–6837. PubMed PMC
Denk T, Grimm GW. 2009. The biogeographic history of beech trees. Review of Palaeobotany and Palynology 158: 83–100.
Dick MA, Dobbie K, Cooke DEL, et al. 2006. Phytophthora captiosa sp. nov. and P. fallax sp. nov. causing crown dieback of Eucalyptus in New Zealand. Mycological Research 110: 393–404. PubMed
Dick MW. 1990. Keys to Pythium. University of Reading Press, Reading, UK.
Dos Santos AF, Luz EDMN, De Souza JT. 2006. First report of Phytophthora boehmeriae on black wattle in Brazil. Plant Pathology 55: 813.
Drummond AJ, Ho SYW, Phillips MJ, et al. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4: 699–710. PubMed PMC
Elias S, Brigham-Grette J. 2013. Late Pleistocene glacial events in Beringia. In: Elias S. (ed), Encyclopedia of Quaternary Science, 2nd edn: 191- 201. Elsevier, Amsterdam, Netherlands.
Erwin DC, Ribeiro OK. 1996. Phytophthora diseases worldwide. APS Press, St. Paul, Minnesota.
Fletcher K, Gil J, Bertier LD, et al. 2019. Genomic signatures of heterokaryosis in the oomycete pathogen Bremia lactucae. Nature Communications 10: 2645. PubMed PMC
Fletcher K, Klosterman SJ, Derevnina L, et al. 2018. Comparative genomics of downy mildews reveals potential adaptations to biotrophy. BMC Genomics 19: 851. PubMed PMC
Foster ZSL, Albornoz FL, Fieland VJ, et al. 2022. A new oomycete metabarcoding method using the rps10 gene. Phytobiomes Journal: in press. 10.1094/PBIOMES-02-22-0009-R. DOI
Frankel SJ, Conforti C, Hillman J, et al. 2020. Phytophthora introductions in restoration areas: Responding to protect California native flora from human-assisted pathogen spread. Forests 11: 1291.
Frezzi MJ. 1941. Phytophthora boehmeriae, causante de la podredumbre morena de los frutos citricos, en la Republica Argentina (Phytophthora boehmeriae, the agent of brown rot of citrus fruits in the Argentine Republic). Revista Argentina de Agronomía 8: 200–205.
Frezzi MJ. 1950. Las especies de Phytophthora en la Argentina (The species of Phytophthora in Argentina). Revista de Investigaciones Agrícolas 4: 47–133.
Garbelotto MM, Lee HK, Slaughter G, et al. 1997. Heterokaryosis is not required for virulence of Heterobasidion annosum. Mycologia 89: 92–102.
Gardner JF, Dick MA, Bader MK-F. 2015. Susceptibility of New Zealand flora to Phytophthora kernoviae and its seasonal variability in the field. New Zealand Journal of Forestry Science 45: 23.
Givnish TJ. 1997. Adaptive radiation and molecular systematics: aims and conceptual issues. In: Givnish TJ, Systma KJ. (eds), Molecular evolution and adaptive radiation: 1-54. Cambridge University Press, New York, USA.
Givnish TJ. 2015. Adaptive radiation versus ‘radiation’ and ‘explosive diversification’: why conceptual distinctions are fundamental to understanding evolution. New Phytologist 207: 297–303. PubMed
Gladenkov AX, Oleinik AE, Marincovich L, et al. 2002. A refined age for the earliest opening of Bering Strait. Palaeogeography, Palaeoclimatology, Palaeoecology 183: 321–328.
Hansen E[M], Delatour C. 1999. Phytophthora species in oak forests of northeast France. Annales des Sciences Forestière 56: 539–547.
Hansen EM, Reeser PW, Sutton W. 2012a. Phytophthora beyond agriculture. Annual Review of Phytopathology 50: 359–378. PubMed
Hansen EM, Reeser PW, Sutton W. 2012b. Phytophthora borealis and Phytophthora riparia, new species in Phytophthora ITS Clade 6. Mycologia 104: 1133–1142. PubMed
Hansen EM, Reeser PW, Sutton W, et al. 2015. Redesignation of Phytophthora taxon Pgchlamydo as Phytophthora chlamydospora sp. nov. North American Fungi 10: 1–14.
Heaney LR. 1991. A synopsis of climatic and vegetational change in Southeast Asia. Climatic Change 19: 53–61.
Hope G. 2001. Environmental change in the Late Pleistocene and later Holocene at Wanda Site, Soroako, South Sulawesi, Indonesia. Palaeogeography, Palaeoclimatology, Palaeoecology 171: 129–145.
Hopple JS, Vilgalys R. 1994. Phylogenetic relationships among coprinoid taxa and allies based on data from restriction site mapping of nuclear rDNA. Mycologia 86: 96–107.
Huai WX, Tian G, Hansen EM, et al. 2013. Identification of Phytophthora species baited and isolated from forest soil and streams in northwestern Yunnan province, China. Forest Pathology 43: 87–103.
Hüberli D. 1995. Analysis of variability among isolates of Phytophthora cinnamomi Rands from Eucalyptus marginata Donn ex Sm. and E. calophylla R. Br. based on cultural characteristics, sporangia and gametangia morphology, and pathogenicity. Bachelor thesis, Murdoch University, Murdoch, Western Australia.
Hüberli D, Hardy GEStJ, White D, et al. 2013. Fishing for Phytophthora from Western Australia’ s waterways: A distribution and diversity survey. Australasian Plant Pathology 42: 251–260.
Hubert F, Grimm GW, Jousselin E, et al. 2014. Multiple nuclear genes stabilize the phylogenetic backbone of the genus Quercus. Systematics and Biodiversity 12: 405–423.
Hueck K. 1966. Die Wälder Südamerikas (‘The forests of South America’). Gustav Fischer, Stuttgart, Germany.
Husson C, Aguayo J, Revellin C, et al. 2015. Evidence for homoploid speciation in Phytophthora alni supports taxonomic reclassification in this species complex. Fungal Genetics and Biology 77: 12–21. PubMed
Jones LA, Worobo RW, Smart CD. 2014. Plant-pathogenic oomycetes, Escherichia coli strains, and Salmonella spp. frequently found in surface water used for irrigation of fruit and vegetable crops in New York State. Applied and Environmental Microbiology 80: 4814–4820. PubMed PMC
Jönsson U, Lundberg L, Sonesson K, et al. 2003. First records of soilborne Phytophthora species in Swedish oak forests. Forest Pathology 33: 175–179.
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, Blaschke H, Neumann P. 1996. Isolation, identification and pathogenicity of Phytophthora species from declining oak stands. European Journal of Forest Pathology 26: 253–272.
Jung T, Blaschke H, Osswald W. 2000. Involvement of soilborne Phytophthora species in Central European oak decline and the effect of site factors on the disease. Plant Pathology 49: 706–718.
Jung T, Blaschke M. 2004. Phytophthora root and collar rot of alders in Bavaria: distribution, modes of spread and possible management strategies. Plant Pathology 53: 197–208.
Jung T, Chang TT, Bakonyi J, et al. 2017a. Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathology 66: 194–211.
Jung T, Cooke DEL, Blaschke H, et al. 1999. Phytophthora quercina sp. nov., causing root rot of European oaks. Mycological Research 103: 785–798.
Jung T, Durán A, Sanfuentes von Stowasser E, et al. 2018a. Diversity of Phytophthora species in Valdivian rainforests and association with severe dieback symptoms. Forest Pathology 48: e12443.
Jung T, Hansen EM, Winton L, et al. 2002. Three new species of Phytophthora from European oak forests. Mycological Research 106: 397–411.
Jung T, Horta Jung M, Cacciola SO, et al. 2017b. Multiple new cryptic pathogenic Phytophthora species from Fagaceae forests in Austria, Italy and Portugal. IMA Fungus 8: 219–244. PubMed PMC
Jung T, Horta Jung M, Scanu B, et al. 2017c. Six new Phytophthora species from ITS clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Persoonia 38: 100–135. PubMed PMC
Jung T, Horta Jung M, Webber JF, et al. 2021. The destructive tree pathogen Phytophthora ramorum originates from the Laurosilva forests of East Asia. Journal of Fungi 7: 226. PubMed PMC
Jung T, La Spada F, Pane A, et al. 2019. Diversity and distribution of Phytophthora species in protected natural areas in Sicily. Forests 10: 259.
Jung T, Nechwatal J. 2008. Phytophthora gallica sp. nov., a new species from rhizosphere soil of declining oak and reed stands in France and Germany. Mycological Research 112: 1195–1205. PubMed
Jung T, Pérez-Sierra A, Durán A, et al. 2018b. Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia 40:182–220. PubMed PMC
Jung T, Scanu B, Bakonyi J, et al. 2017d. Nothophytophthora gen. nov., a new sister genus of Phytophthora from natural and semi-natural ecosystems. Persoonia 39: 143–174. PubMed PMC
Jung T, Scanu B, Brasier CM, et al. 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.
Jung T, Stukely MJC, Hardy GEStJ, et al. 2011. Multiple new Phytophthora species from ITS Clade 6 associated with natural ecosystems in Australia: evolutionary and ecological implications. Persoonia 26: 13–39. PubMed PMC
Kaliq I, Hardy GEStJ, McDougall KL, et al. 2019. Phytophthora species isolated from alpine and sub-alpine regions of Australia, including the description of two new species; Phytophthora cacuminis sp. nov. and Phytophthora oreophila sp. nov. Fungal Biology 123: 29e41. PubMed
Kalyaanamoorthy S, Minh BQ, Wong TKF, et al. 2017. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. PubMed PMC
Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. PubMed PMC
Kim J-S, Kim B-S. 2004. Leaf blight of Ailanthus altissima caused by Phytophthora boehmeriae. The Plant Pathology Journal 20: 106–109.
Kim S, De Medeiros BAS, Byun B-K, et al. 2018. West meets East: How do rainforest beetles become circum-Pacific? Evolutionary origin of Callipogon relictus and allied species (Cerambycidae: Prioninae) in the New and Old Worlds. Molecular Phylogenetics and Evolution 125: 163–176. PubMed
Kone A, Kofke DA. 2005. Selection of temperature intervals for parallel-tempering simulations. Journal of Chemical Physics 122: 1–2. PubMed
Kozak KH, Weisrock DR, Larson R. 2006. Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon). Proceedings of the Royal Society B 273: 539–546. PubMed PMC
Kroon LPNM, Bakker FT, Van den Bosch GBM, et al. 2004. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genetics and Biology 41: 766–782. PubMed
Lang P, Dane F, Kubisiak TL, et al. 2007. Molecular evidence for an Asian origin and a unique westward migration of species in the genus Castanea via Europe to North America. Molecular Phylogenetics and Evolution 43: 49–59. PubMed
Laumonier Y. 1997. The vegetation and physiography of Sumatra. Geobotany 22. Springer Science and Business Media, Dordrecht, Germany.
Legeay J, Husson C, Boudier B, et al. 2020. Surprising low diversity of the plant pathogen Phytophthora in Amazonian forests. Environmental Microbiology 22: 5019–5032. PubMed
Lohman DJ, De Bruyn M, Page T, et al. 2011. Biogeography of the Indo-Australian Archipelago. Annual Review of Ecology, Evolution, and Systematics 42: 205–226.
MacKinnon K, Hatta G, Halim H, et al. 1997. The ecology of Kalimantan. Ecology of Indonesia Series Vol. III; Oxford University Press, Oxford, UK.
Man in’t Veld WA, Rosendahl KCHM, Hong C. 2012. Phytophthora × serendipita sp. nov. and P. × pelgrandis, two destructive pathogens generated by natural hybridization. Mycologia 104: 1390–1396. PubMed
Martin FN, Tooley PW. 2003. Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase I and II genes. Mycologia 95: 269–284. PubMed
Maseko B, Burgess TI, Coutinho TA, et al. 2007. Two new Phytophthora species from South African Eucalyptus plantations. Mycological Research 111: 1321–1338. PubMed
Matsiakh I, Kramarets V, Cleary M. 2020. Occurrence and diversity of Phytophthora species in declining broadleaf forests in western Ukraine. Forest Pathology 51: e12662.
Mayr E. 1942. Systematics and the origin of species. Columbia University Press, New York.
McCarthy CGP, Fitzpatrick DA. 2017. Phylogenomic reconstruction of the oomycete phylogeny derived from 37 genomes. mSphere 2: e00095–e00017. PubMed PMC
McKenna MC. 1983. Cenozoic paleogeography of North Atlantic land bridges. In: Bott MHP, Saxov S, Talwani M, et al. (eds), Structure and development of the Greenland-Scotland Ridge: 351–399. Plenum Press, New York.
Milenković I, Keča N, Karadžić D, et al. 2018. Isolation and pathogenicity of Phytophthora species from poplar plantations in Serbia. Forests 9: 330.
Morley JR. 2003. Interplate dispersal paths for megathermal angiosperms. Perspectives in Plant Ecology, Evolution and Systematics 6: 5–20.
Müller N, Bouckaert R. 2019. Adaptive parallel tempering for BEAST 2. bioRxiv [online]. 10.1101/603514. DOI
Nagel JH, Gryzenhout M, Slippers B, 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
Nechwatal J, Bakonyi J, Cacciola SO, et al. 2013. The morphology, behaviour and molecular phylogeny of Phytophthora taxon Salixsoil and its redesignation as Phytophthora lacustris sp. nov. Plant Pathology 62: 355–369.
Nelson SC, Abad ZG. 2010. Phytophthora morindae, a new species causing black flag disease on noni (Morinda citrifolia L) in Hawaii. Mycologia 102: 122–134. PubMed
Nguyen LT, Schmidt HA, Von Haeseler A, et al. 2015. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274. PubMed PMC
O’Hanlon R, Choiseul J, Corrigan M, et al. 2016. Diversity and detections of Phytophthora species from trade and nontrade environments in Ireland. Bulletin OEPP/EPPO Bulletin 46: 594–602.
Oh E, Gryzenhout M, Wingfield BD, et al. 2013. Surveys of soil and water reveal a goldmine of Phytophthora diversity in South African natural ecosystems. IMA Fungus 4: 123–131. PubMed PMC
Pérez-Sierra A, Chitty R, Eacock A, et al. 2022. First report of Phytophthora pluvialis in Europe causing resinous cankers on western hemlock. New Disease Reports 45: e12064.
Pérez-Sierra A, Gorton C, Lewis C, et al. 2019. Phytophthora spp. on trees in Britain through the lens of the Tree Health Diagnostic and Advisory Service. In: Scanu B, Balmas V, Brandano A, et al. (eds), Phytophthoras in forests and natural ecosystems: Ninth meeting of the International Union of Forest Research Organizations (IUFRO) Working Party 7.02.09, La Maddalena, Sardinia, Italy, 17-26 Oct 2019. Book of Abstracts: P24. University of Sassari, Italy.
Qian H. 2002. Floristic relationships between Eastern Asia and North America: Test of Gray’s hypothesis. The American Naturalist 160: 317–332. PubMed
Rambaut A, Drummond A, Xie D, et al. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. PubMed PMC
Ramsfield TD, Dick MA, Beever RE. 2009. Phytophthora kernoviae in New Zealand. In: Goheen EM, Frankel SJ. (eds), Phytophthoras in forests and natural ecosystems. Fourth meeting of the International Union of Forest Research Organizations (IUFRO) Working Party S07.02.09. USDA Forest Service, Pacific Southwest Research Station, Albany, California. General Technical Report PSW-GTR-221: 47–53.
Rea AJ, Burgess TI, Hardy GEStJ, et al. 2011. Two novel and potentially endemic species of Phytophthora associated with episodic dieback of kwongan vegetation in the south-west of Western Australia. Plant Pathology 60: 1055–1068.
Redondo MA, Boberg J, Stenlid J, et al. 2018a. Contrasting distribution patterns between aquatic and terrestrial Phytophthora species along a climatic gradient are linked to functional traits. The ISME Journal 12: 2967–2980. PubMed PMC
Redondo MA, Boberg J, Stenlid J, et al. 2018b. Functional traits associated with the establishment of introduced Phytophthora spp. in Swedish forests. Journal of Applied Ecology 55: 1538–1552.
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 PW, Sutton W, Hansen EM, et al. 2011. Phytophthora species in forest streams in Oregon and Alaska. Mycologia 103: 22–35. PubMed
Rizzo DM, Garbelotto M, Davidson JM, et al. 2002. Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densi-florus in California. Plant Disease 86: 205–214. PubMed
Robideau GP, De Cock AW, Coffey MD, et al. 2011. DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Molecular Ecology Resources 11:1002–1011. PubMed PMC
Rundell RJ, Price TD. 2009. Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends in Ecology and Evolution 24: 394–399. PubMed
Sambles C, Schlenzig S, O’Neill P, et al. 2015. Draft genome sequences of Phytophthora kernoviae and Phytophthora ramorum lineage EU2 from Scotland. Genomics Data 6: 193–194. PubMed PMC
Sanfuentes E, Fajardo S, Sabag M, et al. 2016. Phytophthora kernoviae isolated from fallen leaves of Drymis winteri in native forest of southern Chile. Australasian Plant Disease Notes 11: 1–3.
Scanu B, Hunter GC, Linaldeddu BT, et al. 2014. A taxonomic re-evaluation reveals that Phytophthora cinnamomi and P. cinnamomi var. parvispora are separate species. Forest Pathology 44: 1–20.
Scanu B, Jung T, Masigol H, et al. 2021. Phytophthora heterospora sp. nov., a new pseudoconidia-producing sister species of P. palmivora. Journal of Fungi 7: 870. PubMed PMC
Scanu B, Linaldeddu BT, Deidda A, et al. 2015. Diversity of Phytophthora species from declining Mediterranean maquis vegetation, including two new species, Phytophthora crassamura and P. ornamentata sp. nov. PLoS ONE 10: e0143234. PubMed PMC
Scanu B, Webber JF. 2016. Dieback and mortality of Nothofagus in Britain: ecology, pathogenicity and sporulation potential of the causal agent Phytophthora pseudosyringae. Plant Pathology 65: 26–36.
Scott P, Williams N. 2014. Phytophthora diseases in New Zealand forests. New Zealand Journal of Forestry 59: 14–21.
Seddaiu S, Brandano A, Ruiu PA, et al. 2020. An overview of Phytophthora species inhabiting declining Quercus suber stands in Sardinia (Italy). Forests 11: 971.
Seibert P. 1996. Farbatlas Südamerika – Landschaften und Vegetation (‘Colour atlas South America – Landscapes and vegetation’). Eugen Ulmer, Stuttgart, Germany.
Shakya SK, Grünwald NK, Fieland VJ, et al. 2021. Phylogeography of the wide-host range panglobal plant pathogen Phytophthora cinnamomi. Molecular Ecology 30: 5164– 5178. PubMed
Sharma PP, Giribet G. 2012. Out of the Neotropics: Late Cretaceous colonization of Australasia by American arthropods. Proceedings of the Royal Society 279: 3501–3509. PubMed PMC
Shaw DE. 1984. ‘Microorganisms in Papua New Guinea.’ Department of Primary Industry, Port Moresby, Papua New Guinea. Research Bulletin No. 33.
Shrestha SK, Zhou Y, Lamour K. 2013. Oomycetes baited from streams in Tennessee 2010–2012. Mycologia 105: 1516–1523. PubMed
Sims LL, Sutton W, Reeser P. et al. 2015. The Phytophthora species assemblage and diversity in riparian alder ecosystems of western Oregon, USA. Mycologia 107: 889–902. PubMed
Stamler RA, Sanogo S, Goldberg NP, et al. 2016. Phytophthora species in rivers and streams of the Southwestern United States. Applied and Environmental Microbiology 82: 4696–4704. PubMed PMC
Stöver BC, Müller KF. 2010. TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11: 7. PubMed PMC
Studholme DJ, McDougal RL, Sambles C, et al. 2016. Genome sequences of six Phytophthora species associated with forests in New Zealand. Genomics Data 7: 54–56. PubMed PMC
Studholme DJ, Panda P, Sanfuentes von Stowasser E, et al. 2019. Genome sequencing of oomycete isolates from Chile supports the New Zealand origin of Phytophthora kernoviae and makes available the first Nothophytophthora sp. genome. Molecular Plant Pathology 20: 423–431. PubMed PMC
Sukumaran J, Holder MT. 2010. DendroPy: A Python library for phylogenetic computing. Bioinformatics 26: 1569–1571. PubMed
Tamura K, Stecher G, Kumar S. 2021. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38: 3022–3027. PubMed PMC
Tecklin D, DellaSala DA, Luebert F, et al. 2011. Valdivian temperate rainforests of Chile and Argentina. In: DellaSala DA. (ed), Temperate and boreal rainforests of the world: 132–153. Island Press, Washington, Covelo, London.
Thines M, Choi Y-J. 2016. Evolution, diversity, and taxonomy of the Peronosporaceae, with focus on the genus Peronospora. Phytopathology 106: 6–18. PubMed
Thorpe P, Vetukuri RR, Hedley PE, et al. 2021. Draft genome assemblies for tree pathogens Phytophthora pseudosyringae and Phytophthora boehmeriae. G3 11(11): jkab282. PubMed PMC
Tiffney BH. 1985. The Eocene North Atlantic land bridge: Its importance in tertiary and modern phytogeography of the northern hemisphere. Journal of the Arnold Arboretum 66: 243–273.
Toussaint EFA, Hendrich L, Hájek J, et al. 2017. Evolution of Pacific Rim diving beetles sheds light on Amphi-Pacific biogeography. Ecography 40: 500–510.
Tucker CM. 1931. Taxonomy of the genus Phytophthora de Bary. University of Missouri. Agricultural Experiment Station Research Bulletin 153.
Van Damme K, Sinev AY. 2013. Tropical Amphi-Pacific disjunctions in the Cladocera (Crustacea: Branchiopoda). Journal of Limnology 72: 209–244.
Van Poucke K, Haegeman A, Goedefroit T, et al. 2021. Unravelling hybridization in Phytophthora using phylogenomics and genome size estimation. IMA Fungus 12: 16. PubMed PMC
Vélez ML, La Manna L, Tarabini N, et al. 2020. Phytophthora austrocedri in Argentina and co-inhabiting Phytophthoras: Roles of anthropogenic and abiotic factors in species distribution and diversity. Forests 11: 1223.
Vettraino AM, Barzanti GP, Bianco MC, et al. 2002: Occurrence of Phytophthora species in oak stands in Italy and their association with declining oak trees. Forest Pathology 32: 19–28.
Vettraino AM, Morel O, Perlerou C, et al. 2005. Occurrence and distribution of Phytophthora species associated with ink disease of chestnut in Europe. European Journal of Plant Pathology 111: 169–180.
Vila R, Bell CD, Macniven R, et al. 2011. Phylogeny and palaeoecology of Polyommatus blue butterflies show Beringia was a climate-regulated gateway to the New World. Proceedings of the Royal Society B 278: 2737–2744. PubMed PMC
Wang J, Presser JW, Goss EM. 2016. Nuclear DNA content of the hybrid plant pathogen Phytophthora andina determined by flow cytometry. Mycologia 108: 899–904. PubMed
Wen J. 1999. Evolution of Eastern Asian and Eastern North American disjunct distributions in flowering plants. Annual Review of Ecology and Systematics 30: 421–455.
Wen J, Ickert-Bond S, Nie Z-L, et al. 2010. Timing and modes of evolution of eastern Asian-North American biogeographic disjunctions in seed plants. In: Long M, Gu H, Zhou Z. (eds), Darwin’s heritage today: Proceedings of the Darwin 2010 Beijing International Conference: 252–269. Higher Education Press, Bejing, China.
Wen J, Nie Z-L, Ickert-Bond SM. 2016. Intercontinental disjunctions between eastern Asia and western North America in vascular plants highlight the biogeographic importance of the Bering land bridge from late Cretaceous to Neogene. Journal of Systematics and Evolution 54: 469–490.
White TJ, Bruns T, Lee S, et al. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innes MA, Gelfand DH, Sninsky JJ, et al. (eds), PCR protocols: A guide to methods and applications: 315–322. Academic Press, San Diego, California, USA.
Whitten T, Damanik SJ, Anwar J, et al. 1997. The ecology of Sumatra. Ecology of Indonesia Series Vol. I. Oxford University Press, Oxford, UK.
Whitten T, Mustafa M, Henderson GS. 2002. The ecology of Sulawesi. Ecology of Indonesia Series Vol. IV. Oxford University Press, Oxford, UK.
Winkworth RC, Nelson BCW, Bellgard SE, et al. 2020. A LAMP at the end of the tunnel: A rapid, field deployable assay for the kauri dieback pathogen, Phytophthora agathidicida. PLoS ONE 15: e0224007. PubMed PMC
Xu X, Huai W, Hamiti, et al. 2019. Phytophthora species from Xinjiang wild apple forests in China. Forests 10: 927.
Yang X, Balci Y, Brazee NJ, et al. 2016. A unique species in Phytophthora clade 10, Phytophthora intercalaris sp. nov., recovered from stream and irrigation water in the eastern USA. International Journal of Systematic and Evolutionary Microbiology 66: 845–855. PubMed PMC
Yang X, Gallegly ME, Hong C. 2014. A high-temperature tolerant species in clade 9 of the genus Phytophthora: P. hydrogena sp. nov. Mycologia 106: 57–65. PubMed
Yang X, Hong C. 2013. Phytophthora virginiana sp. nov., a high-temperature tolerant species from irrigation water in Virginia. Mycotaxon 126: 167–176.
Yang X, Hong C. 2018. Differential usefulness of nine commonly used genetic markers for identifying Phytophthora species. Frontiers in Microbiology 9: 2334. PubMed PMC
Yang X, Tyler BM, Hong C. 2017. An expanded phylogeny for the genus Phytophthora. IMA Fungus 8: 355–384. PubMed PMC
Zeng H-C, Ho H-H, Zheng F-C. 2009. A survey of Phytophthora species on Hainan Island of South China. Journal of Phytopathology 157: 33–39.
Dryad
10.5061/dryad.41ns1rngw