During a survey of Phytophthora diversity in Panama, fast-growing oomycete isolates were obtained from naturally fallen leaves of an unidentified tree species in a tropical cloud forest. Phylogenetic analyses of sequences from the nuclear ITS, LSU and ßtub loci and the mitochondrial cox1 and cox2 genes revealed that they belong to a new species of a new genus, officially described here as Synchrospora gen. nov., which resided as a basal genus within the Peronosporaceae. The type species S. medusiformis has unique morphological characteristics. The sporangiophores show determinate growth, multifurcating at the end, forming a stunted, candelabra-like apex from which multiple (8 to >100) long, curved pedicels are growing simultaneously in a medusa-like way. The caducous papillate sporangia mature and are shed synchronously. The breeding system is homothallic, hence more inbreeding than outcrossing, with smooth-walled oogonia, plerotic oospores and paragynous antheridia. Optimum and maximum temperatures for growth are 22.5 and 25-27.5 °C, consistent with its natural cloud forest habitat. It is concluded that S. medusiformis as adapted to a lifestyle as a canopy-dwelling leaf pathogen in tropical cloud forests. More oomycete explorations in the canopies of tropical rainforests and cloud forests are needed to elucidate the diversity, host associations and ecological roles of oomycetes and, in particular, S. medusiformis and possibly other Synchrospora taxa in this as yet under-explored habitat.

Faculty of Forestry University of Belgrade Kneza Višeslava 1 11030 Belgrade Serbia

Phytophthora Research and Consultancy 83131 Nußdorf Germany

Phytophthora Research Centre Faculty of Forestry and Wood Technology Mendel University in Brno 613 00 Brno Czech Republic

Smithsonian Tropical Research Institute Apartado Panamá Panama City 0843 03092 Panama

USDA Agricultural Research Service National Center for Agricultural Utilization Research Mycotoxin Prevention and Applied Microbiology Research Unit Peoria IL 61604 USA

USDA APHIS Plant Protection and Quarantine 4700 River Road Riverdale MD 20737 USA

Zobrazit více v PubMed

Dick M.W. Straminipilous fungi: Systematics of the Peronosporomycetes Including Accounts of the Marine Straminipilous Protists, the Plasmodiophorids and Similar Organisms. Kluwer; Dordrecht, The Netherlands: 2001.

Hulvey J., Telle S., Nigrelli L., Lamour K., Thines M. Salisapiliaceae—A new family of oomycetes from marsh grass litter of southeastern North America. Persoonia. 2010;25:109–116. doi: 10.3767/003158510X551763. PubMed DOI PMC

Beakes G.W., Honda T., Thines M. Systematics of the Stramenipila: Labyrinthulomycota, Hyphochytridiomycota, and Oomycota. In: McLaughlin D.J., Spatafora J., editors. Systematics and Evolution. Springer; New York, NY, USA: 2014. pp. 39–97.

Thines M., Choi Y.-J. Evolution, diversity and taxonomy of the Peronosporaceae, with focus on the genus Peronospora. Phytopathology. 2016;106:6–18. doi: 10.1094/PHYTO-05-15-0127-RVW. PubMed DOI

Bennett R.M., de Cock A.W.A.M., Lévesque A., Thines M. Calycofera gen. nov., an estuarine sister taxon to Phytopythium, Peronosporaceae. Mycol. Prog. 2017;16:947–954. doi: 10.1007/s11557-017-1326-9. DOI

Jung T., Scanu B., Bakonyi J., Seress D., Kovács G.M., Durán A., Sanfuentes von Stowasser E., Schena L., Mosca S., Thu P.Q., et al. Nothophytophthora gen. nov., a new sister genus of Phytophthora from natural and semi-natural ecosystems. Persoonia. 2017;39:143–174. doi: 10.3767/persoonia.2017.39.07. PubMed DOI PMC

Bourret T.B., Choudhury R.A., Mehl H.K., Blomquist C.L., McRoberts N., Rizzo D.M. Multiple origins of downy mildews and mito-nuclear discordance within the paraphyletic genus Phytophthora. PLoS ONE. 2018;13:e0192502. doi: 10.1371/journal.pone.0192502. PubMed DOI PMC

Scanu B., Jung T., Masigol H., Linaldeddu B.T., Horta Jung M., Brandano A., Mostowfizadeh-Ghalamfarsa R., Janoušek J., Riolo M., Cacciola S.O. Phytophthora heterospora sp. nov., a new pseudoconidia-producing sister species of P. palmivora. J. Fungi. 2021;7:870. doi: 10.3390/jof7100870. PubMed DOI PMC

Maia C., Horta Jung M., Carella G., Milenković I., Janoušek J., Tomšovský M., Mosca S., Schena L., Cravador A., Moricca S., et al. Eight new Halophytophthora species from marine and brackish-water ecosystems in Portugal and an updated phylogeny for the genus. Persoonia. 2022;48:54–90. doi: 10.3767/persoonia.2022.48.02. PubMed DOI PMC

Cooke D.E.L., Drenth A., Duncan J.M., Wagels G., Brasier C.M. A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet. Biol. 2000;30:17–32. doi: 10.1006/fgbi.2000.1202. PubMed DOI

Riethmüller A., Voglmayr H., Göker M., Weiß M., Oberwinkler F. Phylogenetic relationships of the downy mildews (Peronosporales) and related groups based on nuclear large subunit ribosomal DNA sequences. Mycologia. 2002;94:834–849. doi: 10.1080/15572536.2003.11833177. PubMed DOI

Kroon L.P.N.M., Bakker F.T., van den Bosch G.B.M., Bonants P.J.M., Flier W.G. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genet. Biol. 2004;41:766–782. doi: 10.1016/j.fgb.2004.03.007. PubMed DOI

Göker M., Voglmayer H., Riethmüller A., Oberwinkler F. How do obligate parasites evolve? A multi–gene phylogenetic analysis of downy mildews. Fungal Genet. Biol. 2007;44:105–122. doi: 10.1016/j.fgb.2006.07.005. PubMed DOI

Runge F., Telle S., Ploch S., Savory E., Day B., Sharma R., Thines M. The inclusion of downy mildews in a multi–locus–dataset and its reanalysis reveals a high degree of paraphyly in Phytophthora. IMA Fungus. 2011;2:163–171. doi: 10.5598/imafungus.2011.02.02.07. PubMed DOI PMC

Martin F.N., Blair J.E., Coffey M.D. A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora. Fungal Genet. Biol. 2014;66:19–32. doi: 10.1016/j.fgb.2014.02.006. PubMed DOI

Brasier C., Scanu B., Cooke D., Jung T. Phytophthora: An ancient, historic, biologically and structurally cohesive and evolutionarily successful generic concept in need of preservation. IMA Fungus. 2022;13:12. doi: 10.1186/s43008-022-00097-z. PubMed DOI PMC

Briard M., Dutertre M., Rouxel F., Brygoo Y. Ribosomal RNA sequence divergence within the Pythiaceae. Mycol. Res. 1995;99:1119–1127. doi: 10.1016/S0953-7562(09)80782-X. DOI

de Cock A.W.A.M., Lévesque C.A. New species of Pythium and Phytophthora. Stud. Mycol. 2004;50:481–487.

Villa N.O., Kageyama K., Asano T., Suga H. Phylogenetic relationships of Pythium and Phytophthora species based on ITS rDNA, cytochrome oxidase II and beta–tubulin gene sequences. Mycologia. 2006;98:410–422. PubMed

Bala K., Robideau G.P., Lévesque C.A., de Cock A.W.A.M., Abad Z.G., Lodhi A.M., Shahzad S., Ghaffar A., Coffey M.D. Phytopythium Abad, de Cock, Bala, Robideau, Lodhi & Lévesque, gen. nov. and Phytopythium sindhum Lodhi, Shahzad & Lévesque, sp. nov. Fungal Planet 49. Persoonia. 2010;24:136–137.

Uzuhashi S., Tojo M., Kakishima M. Phylogeny of the genus Pythium and description of new genera. Mycoscience. 2010;51:337–365. doi: 10.47371/mycosci.MYC51337. DOI

de Cock A.W.A.M., Lodhi A.M., Rintoul T.L., Bala K., Robideau G.P., Abad Z.G., Coffey M.D., Shahzad S., Lévesque C.A. Phytopythium: Molecular phylogeny and systematics. Persoonia. 2015;34:25–39. doi: 10.3767/003158515X685382. PubMed DOI PMC

Nguyen H.D.T., Dodge A., Dadej K., Rintoul T.L., Ponomareva E., Martin F.N., de Cock A.W.A.M., Lévesque C.A., Redhead S.A., Spies C.F.J. Whole genome sequencing and phylogenomic analysis show support for the splitting of genus Pythium. Mycologia. 2022;114:501–515. doi: 10.1080/00275514.2022.2045116. PubMed DOI

Gäumann E.A. The Fungi. A Description of Their Morphological Features and Evolutionary Development. Hafner Publishing; New York, NY, USA: London, UK: 1952.

Newell S.Y., Fell J.W. Do halophytophthoras (marine Pythiaceae) rapidly occupy fallen leaves by intraleaf mycelial growth? Can. J. Bot. 1995;73:761–765. doi: 10.1139/b95-083. DOI

Erwin D.C., Ribeiro O.K. Phytophthora Diseases Worldwide. APS Press; St. Paul, MN, USA: 1996.

Leaño E.M., Jones E.B.G., Vrijmoed L.L.P. Why are Halophytophthora species well adapted to mangrove habitats? Fungal Divers. 2000;5:131–151.

Nakagiri A. Ecology and biodiversity of Halophytophthora species. Fungal Divers. 2000;5:153–164.

Brasier C.M., Cooke D.E.L., Duncan J.M., Hansen E.M. 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

Jung T., Stukely M.J.C., Hardy G.E.S.J., White D., Paap T., Dunstan W.A., Burgess T.I. Multiple new Phytophthora species from ITS Clade 6 associated with natural ecosystems in Australia: Evolutionary and ecological implications. Persoonia. 2011;26:13–39. doi: 10.3767/003158511X557577. PubMed DOI PMC

Jung T., Milenković I., Corcobado T., Májek T., Janoušek J., Kudláček T., Tomšovský M., Nagy Z., Durán A., Tarigan M., et al. Extensive morphological and behavioural diversity among fourteen new and seven described species in Phytophthora Clade 10 and its evolutionary implications. Persoonia. 2022;49:1–57. doi: 10.3767/persoonia.2022.49.01. PubMed DOI PMC

Bennett R.M., Nam B., Dedeles G.R., Thines M. Phytopythium leanoi sp. nov. and Phytopythium dogmae sp. nov., Phytopythium species associated with mangrove leaf litter from the Philippines. Acta Mycol. 2017;52:1103. doi: 10.5586/am.1103. DOI

Jesus A.L., Marano A.V., Gonçalves D.R., Jerônimo G.H., Pires-Zottarelli C.L.A. Two new species of Halophytophthora from Brazil. Mycol. Prog. 2019;18:1411–1421. doi: 10.1007/s11557-019-01523-0. DOI

Chen Q., Bakhshi M., Balci Y., Broders K.D., Cheewangkoon R., Chen S.F., Fan X.L., Gramaje D., Halleen F., Horta Jung M., et al. Genera of phytopathogenic fungi: GOPHY 4. Stud. Mycol. 2022;101:417–564. doi: 10.3114/sim.2022.101.06. PubMed DOI PMC

Beakes G.W., Glockling S.L., Sekimoto S. The evolutionary phylogeny of the oomycete “fungi”. Protoplasma. 2012;249:3–19. doi: 10.1007/s00709-011-0269-2. PubMed DOI

O’Hanlon R., Destefanis M., Milenković I., Tomšovský M., Janoušek J., Bellgard S.E., Weir B.S., Kudláček T., Horta Jung M., Jung T. Two new Nothophytophthora species from streams in Ireland and Northern Ireland: Nothophytophthora irlandica and N. lirii sp. nov. PLoS ONE. 2021;16:e0250527. doi: 10.1371/journal.pone.0250527. PubMed DOI PMC

Brasier C.M., Robredo F., Ferraz J.F.P. Evidence for Phytophthora cinnamomi involvement in Iberian oak decline. Plant Pathol. 1993;42:140–145. doi: 10.1111/j.1365-3059.1993.tb01482.x. DOI

Brasier C.M., Kirk S.A., Delcan J., Cooke D.E.L., Jung T., In’T Veld W.A.M. Phytophthora alni sp. nov. and its variants: Designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycol. Res. 2004;108:1172–1184. doi: 10.1017/S0953756204001005. PubMed 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., Vettraino A.M., Cech T.L., Vannini A. The impact of invasive Phytophthora species on European forests. In: Lamour K., editor. Phytophthora: A Global Perspective. CABI; Wallingford, UK: 2013. pp. 146–158.

Jung T., Orlikowski L., Henricot B., Abad-Campos P., Aday A.G., Aguín Casal O., Bakonyi J., Cacciola S.O., Cech T., Chavarriaga D., et al. 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., 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. Persoonia. 2018;40:182–220. doi: 10.3767/persoonia.2018.40.08. PubMed DOI PMC

Jung T., Durán A., von Stowasser E.S., Schena L., Mosca S., Fajardo S., González M., Navarro Ortega A.D., Bakonyi J., Seress D., et al. Diversity of Phytophthora species in Valdivian rainforests and association with severe dieback symptoms. For. Pathol. 2018;48:e12443. doi: 10.1111/efp.12443. DOI

Jung T., Scanu B., Brasier C.M., Webber J., Milenković I., Corcobado T., Tomšovský T., Pánek M., Bakonyi J., Maia C., et al. A survey in natural forest ecosystems of Vietnam reveals high diversity of both new and described Phytophthora taxa including P. ramorum. Forests. 2020;11:93. doi: 10.3390/f11010093. DOI

Hansen E.M., Goheen D.J., Jules E.S., Ullian B. Managing Port–Orford–Cedar and the introduced pathogen Phytophthora lateralis. Plant Dis. 2000;84:4–14. doi: 10.1094/PDIS.2000.84.1.4. PubMed DOI

Hansen E.M., Reeser P.W., Sutton W. Phytophthora beyond agriculture. Annu. Rev. Phytopathol. 2012;50:359–378. doi: 10.1146/annurev-phyto-081211-172946. PubMed DOI

Rizzo D.M., Garbelotto M., Davidson J.M., Slaughter G.W., Koike S.T. Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Dis. 2002;86:205–214. doi: 10.1094/PDIS.2002.86.3.205. PubMed DOI

Vettraino A.M., Barzanti G.P., Bianco M.C., Ragazzi A., Capretti P., Paoletti E., Luisi N., Anselmi N., Vannini A. Occurrence of Phytophthora species in oak stands in Italy and their association with declining oak trees. For. Pathol. 2002;32:19–28. doi: 10.1046/j.1439-0329.2002.00264.x. DOI

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

Balci Y., Halmschlager E. Incidence of Phytophthora species in oak forests in Austria and their possible involvement in oak decline. For. Pathol. 2003;33:157–174. doi: 10.1046/j.1439-0329.2003.00318.x. DOI

Balci Y., Halmschlager E. Phytophthora species in oak ecosystems in Turkey and their association with declining oak trees. Plant Pathol. 2003;52:694–702. doi: 10.1111/j.1365-3059.2003.00919.x. DOI

Jönsson U., Lundberg L., Sonesson K., Jung T. First records of soilborne Phytophthora species in Swedish oak forests. For. Pathol. 2003;33:175–179. doi: 10.1046/j.1439-0329.2003.00320.x. DOI

Jung T., Blaschke M. Phytophthora root and collar rot of alders in Bavaria: Distribution, modes of spread and possible management strategies. Plant Pathol. 2004;53:197–208. doi: 10.1111/j.0032-0862.2004.00957.x. DOI

Hardham A.R. Phytophthora cinnamomi. Mol. Plant Pathol. 2005;6:589–604. doi: 10.1111/j.1364-3703.2005.00308.x. PubMed DOI

Balci Y., Balci S., Eggers J., MacDonald W.L., Juzwik J., Long R.P., Gottschalk K.W. Phytophthora spp. associated with forest soils in Eastern and North–Central U.S. oak ecosystems. Plant Dis. 2007;91:705–710. doi: 10.1094/PDIS-91-6-0705. PubMed DOI

Balci Y., Long R.P., Mansfield M., Balser D., MacDonald W.L. Involvement of Phytophthora species in white oak (Quercus alba) decline in southern Ohio. For. Pathol. 2010;40:430–442. doi: 10.1111/j.1439-0329.2009.00617.x. DOI

Greslebin A., Hansen E.M., Sutton W. Phytophthora austrocedrae sp. nov., a new species associated with Austrocedrus chilensis mortality in Patagonia (Argentina) Mycol. Res. 2007;111:308–316. doi: 10.1016/j.mycres.2007.01.008. PubMed DOI

Durán A., Gryzenhout M., Slippers B., Ahumada R., Rotella A., Flores F., Wingfield B.D., Wingfield M.J. Phytophthora pinifolia sp. nov. associated with a serious needle disease of Pinus radiata in Chile. Plant Pathol. 2008;57:715–727. doi: 10.1111/j.1365-3059.2008.01893.x. DOI

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., Burgess T.I. Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov. Persoonia. 2009;22:95–110. doi: 10.3767/003158509X442612. PubMed DOI PMC

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

Green S., Brasier C.M., Schlenzig A., McCracken A., MacAskill G.A., Wilson M., Webber J.F. The destructive invasive pathogen Phytophthora lateralis found on Chamaecyparis lawsoniana across the UK. For. Pathol. 2013;43:19–28.

Green S., Elliot M., Armstrong A., Hendry S.J. Phytophthora austrocedrae emerges as a serious threat to juniper (Juniperus communis) in Britain. Plant Pathol. 2015;64:456–466. doi: 10.1111/ppa.12253. DOI

Pérez-Sierra A., López-García C., León M., García-Jiménez J., Abad-Campos P., Jung T. Previously unrecorded low temperature Phytophthora species associated with Quercus decline in a Mediterranean forest in Eastern Spain. For. Pathol. 2013;43:331–339. doi: 10.1111/efp.12037. DOI

Pérez-Sierra A., Chitty R., Eacock A., Jones B., Biddle M., Crampton M., Lewis A., Olivieri L., Webber J.F. First report of Phytophthora pluvialis in Europe causing resinous cankers on western hemlock. New Dis. Rep. 2022;45:e12064. doi: 10.1002/ndr2.12064. DOI

Ginetti B., Moricca S., Squires J.N., Cooke D.E.L., Ragazzi A., Jung T. Phytophthora acerina sp. nov., a new species causing bleeding cankers and dieback of Acer pseudoplatanus trees in planted forests in Northern Italy. Plant Pathol. 2014;63:858–876. doi: 10.1111/ppa.12153. DOI

Scanu B., Linaldeddu B.T., Deidda A., Jung T. Diversity of Phytophthora species from declining Mediterranean maquis vegetation, including two new species, Phytophthora crassamura and P. ornamentata sp. nov. PLoS ONE. 2015;10:e0143234. doi: 10.1371/journal.pone.0143234. PubMed DOI PMC

Scanu B., Webber J.F. Dieback and mortality of Nothofagus in Britain: Ecology, pathogenicity and sporulation potential of the causal agent Phytophthora pseudosyringae. Plant Pathol. 2016;65:26–36. doi: 10.1111/ppa.12399. DOI

Milenković I., Keča N., Karadžić D., Radulović Z., Nowakowska J.A., Oszako T., Sikora K., Corcobado T., Jung T. Isolation and pathogenicity of Phytophthora species from poplar plantations in Serbia. Forests. 2018;9:330. doi: 10.3390/f9060330. DOI

Corcobado T., Cech T.L., 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

Jung T., Hansen E.M., Winton L., Oßwald W., Delatour C. Three new species of Phytophthora from European oak forests. Mycol. Res. 2002;106:397–411. doi: 10.1017/S0953756202005622. DOI

Jung T., Chang T.T., Bakonyi J., Seress D., Pérez-Sierra A., Yang X., Hong C., Scanu B., Fu C.H., Hsueh K.-L., et al. 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 D.M., Maia C., Pérez-Sierra A., Chang T.-T., Chandelier A., Heungens A., et al. Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Persoonia. 2017;38:100–135. doi: 10.3767/003158517X693615. PubMed DOI PMC

Jung T., Horta Jung M., Cacciola S.O., Cech T., Bakonyi J., Seress D., Mosca S., Schena L., Seddaiu S., Pane A., et al. Multiple new cryptic pathogenic Phytophthora species from Fagaceae forests in Austria, Italy and Portugal. IMA Fungus. 2017;8:219–244. doi: 10.5598/imafungus.2017.08.02.02. PubMed DOI PMC

Jung T., La Spada F., Pane A., Aloi F., Evoli M., Horta Jung M., Scanu B., Faedda R., Rizza C., Puglisi I., et al. Diversity and distribution of Phytophthora species in protected natural areas in Sicily. Forests. 2019;10:259. doi: 10.3390/f10030259. DOI

Zeng H.-C., Ho H.-H., Zheng F.-C. A survey of Phytophthora species on Hainan Island of South China. J. Phytopathol. 2009;157:33–39. doi: 10.1111/j.1439-0434.2008.01441.x. DOI

Brasier C.M., Vettraino A.M., Chang T.T., Vannini A. Phytophthora lateralis discovered in an old growth Chamaecyparis forest in Taiwan. Plant Pathol. 2010;59:595–603. doi: 10.1111/j.1365-3059.2010.02278.x. DOI

Rea A.J., Burgess T.I., Hardy G.E.S.J., Stukely M.J.C., Jung T. Two novel and potentially endemic species of Phytophthora associated with episodic dieback of kwongan vegetation in the south–west of Western Australia. Plant Pathol. 2011;60:1055–1068. doi: 10.1111/j.1365-3059.2011.02463.x. DOI

Reeser P.W., Sutton W., Hansen E.M., Remigi P., Adams G.C. Phytophthora species in forest streams in Oregon and Alaska. Mycologia. 2011;103:22–35. doi: 10.3852/10-013. PubMed DOI

Vettraino A.M., Brasier C.M., Brown A.V., Vannini A. Phytophthora himalsilva sp. nov. an unusually phenotypically variable species from a remote forest in Nepal. Fungal Biol. 2011;115:275–287. doi: 10.1016/j.funbio.2010.12.013. PubMed DOI

Huai W.X., Tian G., Hansen E.M., Zhao W.-X., Goheen E.M., Grünwald N.J., Cheng C. Identification of Phytophthora species baited and isolated from forest soil and streams in northwestern Yunnan province, China. For. Pathol. 2013;43:87–103. doi: 10.1111/efp.12015. DOI

Huberli D., Hardy G.E.S.J., White D., Williams N., Burgess T.I. Fishing for Phytophthora from Western Australia’ s waterways: A distribution and diversity survey. Australas. Plant Pathol. 2013;42:251–260. doi: 10.1007/s13313-012-0195-6. DOI

Oh E., Gryzenhout M., Wingfield B.D., Wingfield M.J., Burgess T.I. 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

Shrestha S.K., Zhou Y., Lamour K. Oomycetes baited from streams in Tennessee 2010–2012. Mycologia. 2013;105:1516–1523. doi: 10.3852/13-010. PubMed DOI

Català S., Peréz–Sierra A., Abad-Campos P. The use of genus–specific amplicon pyrosequencing to assess Phytophthora species diversity using eDNA from soil and water in Northern Spain. PLoS ONE. 2015;10:e0119311. doi: 10.1371/journal.pone.0119311. PubMed DOI PMC

Brazee N.J., Wick R.L., Hulvey J.P. Phytophthora species recovered from the Connecticut River Valley in Massachusetts, USA. Mycologia. 2016;108:6–19. doi: 10.3852/15-038. PubMed DOI

Dunstan W.A., Howard K., Hardy G.E.S.J., Burgess T.I. An overview of Australia’s Phytophthora species assemblage in natural ecosystems recovered from a survey in Victoria. IMA Fungus. 2016;7:47–58. doi: 10.5598/imafungus.2016.07.01.04. PubMed DOI PMC

O’Hanlon R., Choiseul J., Corrigan M., Catarame T., Destefanis M. Diversity and detections of Phytophthora species from trade and nontrade environments in Ireland. Bull. OEPP. 2016;46:594–602. doi: 10.1111/epp.12331. DOI

Burgess T.I., White D., McDougall K.M., Garnas J., Dunstan W.A., Català S., Carnegie A.J., Worboys S., Cahill D., Vettraino A.-M., et al. Distribution and diversity of Phytophthora across Australia. Pac. Conserv. Biol. 2017;23:1–13. doi: 10.1071/PC16032. DOI

Burgess T.I., Simamora A.V., White D., Williams B., Schwager M., Stukely M.J.C., Hardy G.E.S.J. New species from Phytophthora Clade 6a: Evidence for recent radiation. Persoonia. 2018;41:1–17. doi: 10.3767/persoonia.2018.41.01. PubMed DOI PMC

Burgess T.I., Dang Q.N., Le B.V., Pham N.Q., White D., Pham T.Q. Phytophthora acaciivora sp. nov. associated with dying Acacia mangium in Vietnam. FUSE. 2020;6:243–252. doi: 10.3114/fuse.2020.06.11. PubMed DOI PMC

Bose T., Hulbert J.M., Burgess T.I., Paap T., Roets F., Wingfield M.J. Two novel Phytophthora species from the southern tip of Africa. Mycol. Prog. 2021;20:755–767. doi: 10.1007/s11557-021-01702-y. DOI

Dang Q.N., Pham T.Q., Arentz F., Hardy G.E.S.J., Burgess T.I. New Phytophthora species in clade 2a from the Asia-Pacific region including a re-examination of P. colocasiae and P. meadii. Mycol. Prog. 2021;20:111–129. doi: 10.1007/s11557-020-01656-7. DOI

Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Lanfear R., Frandsen P., Wright A., Senfeld T., Calcott B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 2016;34:772–773. doi: 10.1093/molbev/msw260. PubMed DOI

Kozlov A., Darriba D., Flouri T., Morel B., Stamatakis A. RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics. 2019;35:4453–4455. doi: 10.1093/bioinformatics/btz305. PubMed DOI PMC

Pattengale N., Alipour M., Bininda-Emonds O., Moret B., Stamatakis A. How many bootstrap replicates are necessary? J. Comput. Biol. 2010;17:337–354. doi: 10.1089/cmb.2009.0179. PubMed DOI

Lemoine F., Domelevo Entfellner J., Wilkinson E., Correia D., Dávila Felipe M., De Oliveira T., Gascuel O. Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature. 2018;556:452–456. doi: 10.1038/s41586-018-0043-0. PubMed DOI PMC

Sukumaran J., Holder M.T. DendroPy: A Python library for phylogenetic computing. Bioinformatics. 2010;26:1569–1571. doi: 10.1093/bioinformatics/btq228. PubMed DOI

Müller N., Bouckaert R. Adaptive parallel tempering for BEAST 2. bioRxiv. 2019:603514. doi: 10.1101/603514. DOI

Kone A., Kofke D.A. Selection of temperature intervals for parallel-tempering simulations. J. Chem. Phys. 2005;122:1–2. doi: 10.1063/1.1917749. PubMed DOI

Atchadé Y.F., Roberts G.O., Rosenthal J.S. Towards optimal scaling of metropolis-coupled Markov chain Monte Carlo. Stat. Comput. 2011;21:555–568. doi: 10.1007/s11222-010-9192-1. DOI

Bouckaert R., Drummond A. bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evol. Biol. 2017;17:42. doi: 10.1186/s12862-017-0890-6. PubMed DOI PMC

Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006;4:699–710. doi: 10.1371/journal.pbio.0040088. PubMed DOI PMC

Rambaut A., Drummond A., Xie D., Baele G., Suchard M. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 2018;67:901–904. doi: 10.1093/sysbio/syy032. PubMed DOI PMC

Stöver B.C., Müller K.F. TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. BMC Bioinform. 2010;11:7. doi: 10.1186/1471-2105-11-7. PubMed DOI PMC

Tamura K., Stecher G., Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol. Biol. Evol. 2021;38:3022–3027. doi: 10.1093/molbev/msab120. PubMed DOI PMC

Blair J.E., Coffey M.D., Park S.-Y., Greiser D.M., Kang S. A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genet. Biol. 2008;45:266–277. doi: 10.1016/j.fgb.2007.10.010. PubMed DOI

Robideau G.P., de Cock A.W.A.M., Coffey M.D., Voglmayr H., Brouwer H., Bala K., Chitty D.W., Désaulniers N., Eggertson Q.A., Gachon C.M.M., et al. DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Mol. Ecol. Resour. 2011;11:1002–1011. doi: 10.1111/j.1755-0998.2011.03041.x. PubMed DOI PMC

Martin F.N. Phylogenetic relationships among some Pythium species inferred from sequence analysis of the mitochondrially encoded cytochrome oxidase II gene. Mycologia. 2000;92:711–727. doi: 10.1080/00275514.2000.12061211. PubMed DOI

Martin F.N., Tooley P.W. Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase I and II genes. Mycologia. 2003;95:269–284. doi: 10.1080/15572536.2004.11833112. PubMed DOI

Hudspeth D.S.S., Nadler S.A., Hudspeth M.E.S. A COX2 molecular phylogeny of the Peronosporomycetes. Mycologia. 2000;92:674–684. doi: 10.1080/00275514.2000.12061208. DOI

White T.J., Bruns T., Lee S., Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M.A., Gelfand D.H., Sninsky J.J., White T.J., editors. PCR Protocols: A Guide to Methods and Applications. Academic Press; San Diego, CA, USA: 1990. pp. 315–322.

Garbelotto M.M., Lee H.K., Slaughter G., Popenuck T., Cobb F.W., Brunset T.D. Heterokaryosis is not required for virulence of Heterobasidion annosum. Mycologia. 1997;89:92–102. doi: 10.1080/00275514.1997.12026759. DOI

Hopple J.S., Vilgalys R. Phylogenetic relationships among coprinoid taxa and allies based on data from restriction site mapping of nuclear rDNA. Mycologia. 1994;86:96–107. doi: 10.1080/00275514.1994.12026378. DOI

Dick M.W. Keys to Pythium. University of Reading Press; Reading, UK: 1990.

Jung T., Cooke D.E.L., Blaschke H., Duncan J.M., Oßwald W. Phytophthora quercina sp. nov., causing root rot of European oaks. Mycol. Res. 1999;103:785–798. doi: 10.1017/S0953756298007734. DOI

Thines M. Bridging the Gulf: Phytophthora and downy mildews are connected by rare grass parasites. PLoS ONE. 2009;4:e4790. doi: 10.1371/journal.pone.0004790. PubMed DOI PMC

Barreto R.W., Dick M.W. Monograph of Basidiophora (Oomycetes) with the description of a new species. Bot. J. Linn. Soc. 1991;107:313–332. doi: 10.1111/j.1095-8339.1991.tb00226.x. DOI

Telle S., Thines M. Reclassification of an enigmatic downy mildew species on lovegrass (Eragrostis) to the new genus Eraphthora, with a key to the genera of the Peronosporaceae. Mycol. Prog. 2012;11:121–129. doi: 10.1007/s11557-010-0735-9. DOI

Thines M., Telle S., Choi Y.-J., Tan Y.P., Shivas R.G. Baobabopsis, a new genus of graminicolous downy mildews from tropical Australia, with an updated key to the genera of downy mildews. IMA Fungus. 2015;6:483–491. doi: 10.5598/imafungus.2015.06.02.12. PubMed DOI PMC

Crouch J.A., Davis W.J., Shishkoff N., Castroagudín V.L., Martin F., Michelmore R., Thines M. Peronosporaceae species causing downy mildew diseases of Poaceae, including nomenclature revisions and diagnostic resources. FUSE. 2022;9:43–86. doi: 10.3114/fuse.2022.09.05. PubMed DOI PMC

Baxter L., Tripathy S., Ishaque L., Boot N., Cabral A., Kemen E., Thines M., Ah-Fong A., Anderson R., Badejoko W., et al. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsis genome. Science. 2010;330:1549–1551. doi: 10.1126/science.1195203. PubMed DOI PMC

Falloon R.E., Sutherland P.W. Peronospora viciae on Pisum sativum: Morphology of asexual and sexual reproductive structures. Mycologia. 1996;88:473–483. doi: 10.1080/00275514.1996.12026673. DOI

Nordskog B., Gadoury D.M., Seem R.C., Hermansen A. Impact of diurnal periodicity, temperature, and light on sporulation of Bremia lactucae. Phytopathology. 2007;97:979–986. doi: 10.1094/PHYTO-97-8-0979. PubMed DOI

Kandel S.L., Mou B., Shishkoff N., Shi A., Subbarao K.V., Klosterman S.J. Spinach downy mildew: Advances in our understanding of the disease cycle and prospects for disease management. Plant Dis. 2019;103:791–803. doi: 10.1094/PDIS-10-18-1720-FE. PubMed DOI

Brown A.V., Brasier C.M. 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

Dick M.A., Williams N.M., Bader M.K.-F., Gardner J.F., Bulman L.S. Pathogenicity of Phytophthora pluvialis to Pinus radiata and its relation with red needle cast disease in New Zealand. N. Z. J. For. Sci. 2014;44:6. doi: 10.1186/s40490-014-0006-7. DOI

Scanu B., Linaldeddu B.T., Peréz–Sierra A., Deidda A., Franceschini A. Phytophthora ilicis as a leaf and stem pathogen of Ilex aquifolium in Mediterranean islands. Phytopathol. Mediterr. 2014;53:480–490.

Sanfuentes E., Fajardo S., Sabag M., Hansen E., González M. Phytophthora kernoviae isolated from fallen leaves of Drymis winteri in native forest of southern Chile. Australas. Plant Dis. Notes. 2016;11:19. doi: 10.1007/s13314-016-0205-6. DOI

Jung T., Horta Jung M., Webber J.F., Kageyama K., Hieno A., Masuya H., Uematsu S., Pérez-Sierra A., Harris A.R., Forster J., et al. 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

Brasier C.M., Griffin M.J. Taxonomy of Phytophthora palmivora on cocoa. Trans. Br. Mycol. Soc. 1979;71:111–143. doi: 10.1016/S0007-1536(79)80015-7. DOI

Rajalakshmy V.K., Joseph A., Arthassery S. Occurrence of two mating groups in Phytophthora meadii causing abnormal leaf fall disease of rubber in South India. Trans. Br. Mycol. Soc. 1985;85:723–725. doi: 10.1016/S0007-1536(85)80269-2. DOI

Drenth A., Guest D.I. Diversity and Management of Phytophthora in Southeast Asia. Australian Centre for International Agricultural Research; Canberra, Australia: 2004.

Cerqueira A.O., Luz E.D.M.N., De Souza J.T. First record of Phytophthora tropicalis causing leaf blight and fruit rot on breadfruit in Brazil. Plant Pathol. 2006;55:296. doi: 10.1111/j.1365-3059.2006.01332.x. DOI

Guest D.I. Black pod: Diverse pathogens with a global impact on cocoa yield. Phytopathology. 2007;97:1650–1653. doi: 10.1094/PHYTO-97-12-1650. PubMed DOI

Akrofi A.Y., Amoako-Atta I., Assuah M., Asare E.K. Black pod disease on cacao (Theobroma cacao, L) in Ghana: Spread of Phytophthora megakarya and role of economic plants in the disease epidemiology. Crop Prot. 2015;72:66–75. doi: 10.1016/j.cropro.2015.01.015. DOI

Tri M.V., Van Hoa N., Minh Chau N., Pane A., Faedda R., De Patrizio A., Schena L., Olsson C.H.B., Wright S.A.I., Ramstedt M., et al. Decline of jackfruit (Artocarpus heterophyllus) incited by Phytophthora palmivora in Vietnam. Phytopathol. Mediterr. 2015;54:275–280.

Puglisi I., De Patrizio A., Schena L., Jung T., Evoli M., Pane A., Hoa N.V., Tri M.V., Wright S., Ramstedt M., et al. Two previously unknown Phytophthora species associated with brown rot of Pomelo (Citrus grandis) fruits in Vietnam. PLoS ONE. 2017;12:e0172085. doi: 10.1371/journal.pone.0172085. PubMed DOI PMC

Chávez-Ramírez B., Rodríguez-Velázquez N.D., Chávez-Sánchez M.E., Vásquez-Murrieta M.S., Hernández-Gallegos M.A., Velázquez-Martínez J.R., Avendaño-Arrazate C.H., Estrada-de los Santos P. Morphological and molecular identification of Phytophthora tropicalis causing black pod rot in Mexico. Can. J. Plant Pathol. 2021;43:670–679. doi: 10.1080/07060661.2020.1870003. DOI

Patil B., Hedge V., Sridhara S., Pandian R.T.P., Thube S.H., Palliath G.K., Gangurde S.S., Jha P.K. Multigene phylogeny and haplotype analysis reveals predominance of oomycetous fungus, Phytophthora meadii (McRae) associated with fruit rot disease of arecanut in India. Saudi J. Biol. Sci. 2019;29:103341. doi: 10.1016/j.sjbs.2022.103341. PubMed DOI PMC

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