UNLABELLED: Waterways are ideal pathways for Phytophthora dispersal and potential introduction to terrestrial ecosystems. While many Phytophthora species from phylogenetic clades 6, 9 and 10 are predominant oomycetes in watercourses due to their adaptation to a lifestyle as saprotrophs and opportunistic pathogens of riparian plants, species from clades 2, 7 and 8 are predominantly soil- or airborne using aquatic habitats as temporal niches for spreading and invading terrestrial sites along the watercourses. In contrast to forest ecosystems, knowledge of Phytophthora diversity in watercourses in Central Europe is limited. Between 2014 and 2019 extensive surveys of streams and rivers were undertaken across Austria, in South Moravia, Czech Republic and Žilina province, Slovakia to unveil the diversity and distribution of Phytophthora and related oomycetes. In addition, in Austria riparian forests of black alder (Alnus glutinosa) and grey alder (A. incana) in lowlands and in the Alps were examined. A variety of Phytophthora species from clades 2, 6, 7, 8, 9 and 10 were isolated, with clade 6 species showing the widest distribution and abundance. Furthermore, interspecific clade 6 hybrids and other oomycetes such as Halophytophthora fluviatilis and undescribed Nothophytophthora spp. were also obtained. In riparian alders, symptoms of Phytophthora infections were associated with species from the P. × alni complex and P. plurivora. Phytophthora plurivora was most common in alder stands whereas P. uniformis was the oomycete species occurring at the highest altitude in alpine riparian areas. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11557-023-01898-1.

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

Global Change Research Institute of the Czech Academy of Sciences Belidla 986 4a 603 00 Brno Czech Republic

Natural Hazards and Landscape Unit of Phytopathology Department of Forest Protection Federal Research and Training Centre for Forests Seckendorff Gudent Weg 8 1131 Vienna Austria

Phytophthora Research and Consultancy Am Rain 9 83131 Nußdorf Germany

Phytophthora Research Centre Faculty of Forestry and Wood Technology Mendel University in Brno Zemědělská 3 61300 Brno Czech Republic

Zobrazit více v PubMed

Adams GC, Catal M, Trummer L, Hansen EM, Reeser P, Worrall JJ. Phytophthora alni subsp. uniformis found in Alaska beneath thinleaf alders. Plant Health Prog. 2008;9(1):38. doi: 10.1094/PHP-2008-1212-02-BR. DOI

Aday Kaya AG, Lehtijärvi A, Şaşmaz Y, Nowakowska JA, Oszako T, Doğmuş Lehtijärvi HT, Woodward S. Phytophthora species detected in the rhizosphere of Alnus glutinosa stands in the floodplain forests of Western Turkey. For Pathol. 2018;48(6):e12470. doi: 10.1111/efp.12470. DOI

Akilli S, Ulubaş Serçe Ç, Katırcıoğlu YZ, Maden S. Phytophthora dieback on narrow leaved ash in the Black Sea region of Turkey. For Pathol. 2013;43(3):252–256. doi: 10.1111/efp.12024. DOI

Aram K, Rizzo DM. Distinct trophic specializations affect how Phytophthora ramorum and clade 6 Phytophthora spp colonize and persist on Umbellularia californica leaves in streams. Phytopathology. 2018;108(7):858–869. doi: 10.1094/PHYTO-06-17-0196-R. PubMed DOI

Balci Y, Cech TL (2004) Alder decline in Austria caused by a hybrid Phytophthora. In: XV US Department of Agriculture Interagency Research Forum on Gypsy Moth and Other Invasive Species Proceedings January 13th to 16th 2004, Annapolis, USA. USDA Forest Service: 3

Belbahri L, Moralejo E, Calmin G, Oszako T, Garcia JA, Descals E, Lefort F. Phytophthora polonica, a new species isolated from declining Alnus glutinosa stands in Poland. FEMS Microbiol Lett. 2006;261:165–174. doi: 10.1111/j.1574-6968.2006.00349.x. PubMed DOI

Belisario A, Luongo L, Vitale S, Galli M, Haegi A. Phytophthora gonapodyides causes decline and death of English (Persian) walnut (Juglans regia) in Italy. Plant Dis. 2016;100(12):2537–2537. doi: 10.1094/PDIS-03-16-0394-PDN. DOI

Bertier L, Leus L, D’hondt L, De Cock AW, Höfte M. Host adaptation and speciation through hybridization and polyploidy in Phytophthora. PloS One. 2013;8(12):e85385. doi: 10.1371/journal.pone.0085385. PubMed DOI PMC

Bily DS, Diehl SV, Cook M, Wallace LE, Sims LL, Watson C, Baird RE. Temporal and locational variations of a Phytophthora spp community in an urban forested water drainage and stream-runoff system. Southeast Nat. 2018;17(1):176–201. doi: 10.1656/058.017.0118. DOI

Bily DS, Nikolaeva E, Olson T, Kang S. Phytophthora spp. associated with Appalachian oak forests and waterways in Pennsylvania, with P. abietivora as a pathogen of five native woody plant species. Plant Dis. 2022;106(4):1143–1156. doi: 10.1094/PDIS-05-21-0976-RE. PubMed DOI

Bourke A. Potato blight in Europe in 1845: the scientific controversy. In: Lucas JA, Shattock RD, Shaw DS, Cooke LR, editors. Phytophthora. New York: Cambridge University Press; 1991. pp. 12–24.

Brasier CM. Rise of the hybrid fungi. Nature. 2000;405:134–135. doi: 10.1038/35012193. PubMed DOI

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

Brasier CM, Rose J, Gibbs JN. An unusual Phytophthora associated with widespread alder mortality in Britain. Plant Pathol. 1995;44(6):999–1007. doi: 10.1111/j.1365-3059.1995.tb02658.x. DOI

Brasier CM, Cooke DE, Duncan JM, Hansen EM. Multiple new phenotypic taxa from trees and riparian ecosystems in Phytophthora gonapodyides–P. megasperma ITS Clade 6, which tend to be high-temperature tolerant and either inbreeding or sterile. Mycol Res. 2003;107(3):277–290. doi: 10.1017/S095375620300738X. PubMed DOI

Brasier CM, Kirk SA, Delcan J, Cooke DEL, Jung T, Man In't Veld WA. Phytophthora alni sp nov and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycol Res. 2004;108(10):1172–1184. doi: 10.1017/S0953756204001005. PubMed DOI

Brasier CM, 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(1):12. doi: 10.1186/s43008-022-00097-z. PubMed DOI PMC

Brazee NJ, Wick RL, Hulvey JP. Phytophthora species recovered from the Connecticut River Valley in Massachusetts, USA. Mycologia. 2016;108(1):6–19. doi: 10.3852/15-038. PubMed DOI

Bregant C, Sanna GP, Bottos A, Maddau L, Montecchio L, Linaldeddu BT. Diversity and pathogenicity of Phytophthora species associated with declining alder trees in Italy and description of Phytophthora alpina sp. nov. Forests. 2020;11(8):848. doi: 10.3390/f11080848. DOI

Browne GT, Ott NJ, Forbes H, Yaghmour MA, Milliron LK. First report of Phytophthora chlamydospora causing crown and root rot on almond in California. Plant Dis. 2020;104(7):2033–2033. doi: 10.1094/PDIS-10-19-2072-PDN. DOI

Browne GT, Hasey JK, Ott NJ, Forbes H, Arnold K, Milliron L. Flooding by California rivers results in walnut scion infections by species of Phytophthora. Plant Health Prog. 2021;22(3):368–373. doi: 10.1094/PHP-02-20-0011-RS. DOI

Burgess TI. Molecular characterization of natural hybrids formed between five related indigenous clade 6 Phytophthora species. PLoS ONE. 2015;10(8):e0134225. doi: 10.1371/journal.pone.0134225. PubMed DOI PMC

Bush EA, Hong C, Stromberg EL. Fluctuations of Phytophthora and Pythium spp in components of a recycling irrigation system. Plant Dis. 2003;87(12):1500–1506. doi: 10.1094/PDIS.2003.87.12.1500. PubMed DOI

Caballol M, Štraus D, Macia H, Ramis X, Redondo MÁ, Oliva J. Halophytophthora fluviatilis pathogenicity and distribution along a Mediterranean-subalpine gradient. J Fungi. 2021;7(2):112. doi: 10.3390/jof7020112. PubMed DOI PMC

Cech TL (2006) Monitoring of alder-Phytophthora in Vienna. In: IUFRO Working Party 7.03.10 Proceedings of the workshop on methodology of forest insect and disease survey in Central Europe Sept 11th to 14th 2006, Gmunden, Austria, p 136–141

Cech TL, Brandstetter M. Phytophthora-Erlensterben – Aktuelle Situation in Österreich. Forstschutz Aktuell. 1999;23(24):16–19.

Černý K, Strnadová V. Phytophthora alder decline: disease symptoms, causal agent and its distribution in the Czech Republic. Plant Prot Sci. 2010;46(1):12–18. doi: 10.17221/43/2009-PPS. DOI

Černý K, Gregorová B, Holub V, Strnadová V. First records of “alder-Phytophthora” in the Czech Republic. Czech Mycol. 2003;55(3/4):291–296. doi: 10.33585/cmy.55314. DOI

Černý K, Gregorova B, Strnadova V, Holub V, Tomsovsky M, Cervenka M. Phytophthora alni causing decline of black and grey alders in the Czech Republic. Plant Pathol. 2008;57(2):370. doi: 10.1111/j.1365-3059.2007.01718.x. DOI

Černý K, Tomšovský M, Mrázková M, Strnadová V. The present state of knowledge on Phytophthora spp. diversity in forest and ornamental woody plants in the Czech Republic. NZ J for Sci. 2011;41:75–82.

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

Choudhary CE, Burgos-Garay ML, Moorman GW, Hong C. Pythium and Phytopythium species in two Pennsylvania greenhouse irrigation water tanks. Plant Dis. 2016;100(5):926–932. doi: 10.1094/PDIS-07-15-0836-RE. PubMed DOI

Christova PK. Detection of Phytophthora gallica in Bulgaria and co-existence with other Phytophthora species in a small river. J Plant Dis Prot. 2022;129(6):1377–1387. doi: 10.1007/s41348-022-00664-x. DOI

Cleary M, Ghasemkhani M, Blomquist M, Witzell J. First report of Phytophthora gonapodyides causing stem canker on European beech (Fagus sylvatica) in Southern Sweden. Plant Dis. 2016;100(10):2174. doi: 10.1094/PDIS-04-16-0468-PDN. DOI

Cooke DE, Drenth A, Duncan JM, Wagels G, Brasier CM. A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Biol. 2000;30:17–32. doi: 10.1006/fgbi.2000.1202. PubMed DOI

Corcobado T, Cubera E, Pérez-Sierra A, Jung T, Solla A. First report of Phytophthora gonapodyides involved in the decline of Quercus ilex in xeric conditions in Spain. New Dis Rep. 2010;22:33. doi: 10.5197/j.2044-0588.2010.022.033. DOI

Corcobado T, Cech TL, Brandstetter M, Daxer A, Hüttler C, Kudláček T, Horta Jung M, Jung T. Decline of European beech in Austria: Involvement of Phytophthora spp. and contributing biotic and abiotic factors. Forests. 2020;11(8):895. doi: 10.3390/f11080895. DOI

Corcobado T, Milenković I, Saiz-Fernández I, Kudláček T, Plichta R, Májek T, Bačová A, Datková H, Dálya LB, Trifković M, Mureddu D, Račko V, Kardošová M, Ďurkovič J, Rattunde R, Jung T. Metabolomic and physiological changes in Fagus sylvatica seedlings infected with Phytophthora plurivora and the A1 and A2 mating types of P. × cambivora. J Fungi. 2022;8(3):298. doi: 10.3390/jof8030298. PubMed DOI PMC

Derviş S, Türkölmez Ş, Çiftçi O, Ulubaş Serçe Ç. First report of Phytophthora chlamydospora causing root rot on walnut (Juglans regia) trees in Turkey. Plant Dis. 2016;100(11):2336. doi: 10.1094/PDIS-03-16-0306-PDN. DOI

Derviş S, Türkölmez Ş, Çiftçi O, Özer G, Ulubaş Serçe Ç, Dikilitas M. Phytopythium littorale: A novel killer pathogen of plane (Platanus orientalis) causing canker stain and root and collar rot. Plant Dis. 2020;104(10):2642–2648. doi: 10.1094/PDIS-01-20-0141-RE. PubMed DOI

Deutschmann VF. Eine Wurzelfäule an Erdbeeren, hervorgerufen durch Phytophthora cactorum (Leb et Cohn) Schröt. Nachr Dtsch Pflanzenschutzd. 1954;6:7–9.

Fleischmann F, Schneider D, Matyssek R, Oßwald WF. Investigations on Net CO2 assimilation, transpiration and root growth of Fagus sylvatica infested with four different Phytophthora species. Plant Biol. 2002;4:144–152. doi: 10.1055/s-2002-25728. DOI

Fleischmann F, Göttlein A, Rodenkirchen H, Lütz C, Oßwald W. Biomass, nutrient and pigment content of beech (Fagus sylvatica) saplings infected with Phytophthora citricola, P. cambivora, P. pseudosyringae and P. undulata. For Pathol. 2004;34:79–92. doi: 10.1111/j.1439-0329.2004.00349.x. DOI

Gibbs JN, Lipscombe MA, Peace AJ. The impact of Phytophthora disease on riparian populations of common alder (Alnus glutinosa) in southern Britain. Eur J for Pathol. 1999;29(1):39–50. doi: 10.1046/j.1439-0329.1999.00129.x. DOI

Greslebin AG, Hansen EM, Winton LM, Rajchenberg M. Phytophthora species from declining Austrocedrus chilensis forests in Patagonia. Argentina Mycologia. 2005;97(1):218–228. doi: 10.1080/15572536.2006.11832855. PubMed DOI

Hansen E, Delatour C. Phytophthora species in oak forests of north-east France. Ann for Sci. 1999;56(7):539–547. doi: 10.1051/forest:19990702. DOI

Hansen EM, Reeser P, Sutton W, Brasier CM (2015) Redesignation of Phytophthora taxon Pgchlamydo as Phytophthorachlamydospora sp. nov. N Am Fungi 10:1–14

Hartmann G. Wurzelhalsfäule der Schwarzerle (Alnus glutinosa)–eine bisher unbekannte Pilzkrankheit durch Phytophthora cambivora. Forst Und Holz. 1995;50:555–557.

Hildebrand AA. A root and stalk rot of soybeans caused by Phytophthora megasperma Drechsler var. sojae var. nov. Canad J Bot. 1959;37(5):927–957. doi: 10.1139/b59-079. DOI

Hirst JM, Stedman OJ. The epidemiology of Phytophthora infestans: II The source of inoculum. Ann Appl Biol. 1960;48(3):489–517. doi: 10.1111/j.1744-7348.1960.tb03554.x. DOI

Hong CX, Gallegly ME, Richardson PA, Kong P, Moorman GW, Lea-Cox JD, Ross DS. Phytophthora hydropathica, a new pathogen identified from irrigation water, Rhododendron catawbiense and Kalmia latifolia. Plant Pathol. 2010;59(5):913–921. doi: 10.1111/j.1365-3059.2010.02323.x. DOI

Houston Durrant T, de Rigo D, Caudullo G (2016a) Alnus incana in Europe: Distribution, habitat, usage and threats. In: San-Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A (Eds.) European Atlas of Forest Tree Species. Publications Office of the European Union, Luxembourg, e01ff87+: 66–67

Houston Durrant T, de Rigo D, Caudullo G (2016b) Alnus glutinosa in Europe: distribution, habitat, usage and threats. In San-Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A (Eds.) European Atlas of Forest Tree Species. Publications Office of the European Union, Luxembourg, e01f3c0+: 64–65

Huai WX, Tian G, Hansen EM, Zhao WX, Goheen EM, Grünwald NJ, Cheng C. Identification of Phytophthora species baited and isolated from forest soil and streams in northwestern Yunnan province. China for Pathol. 2013;43(2):87–103. doi: 10.1111/efp.12015. DOI

Hüberli D, Hardy GSJ, White D, Williams N, Burgess TI. Fishing for Phytophthora from Western Australia’s waterways: a distribution and diversity survey. Australas Plant Pathol. 2013;42(3):251–260. doi: 10.1007/s13313-012-0195-6. DOI

Hwang J, Oak SW, Jeffers SN (2008) Detecting Phytophthora ramorum and other species of Phytophthora in streams in natural ecosystems using baiting and filtration methods. In: Proceedings of the Sudden Oak Death Third Symposium, vol PSW-GTR-214. US Forest Service, Pacific Southwest Research Station, Albany, pp 55–58

Hwang J, Oak SW, Jeffers SN. Recovery of Phytophthora species from drainage points and tributaries within two forest stream networks: a preliminary report. N Z J for Sci. 2011;41:S83–S87.

Jankowiak R, Stępniewska H, Bilański P, Kolařík M. Occurrence of Phytophthora plurivora and other Phytophthora species in oak forests of southern Poland and their association with site conditions and the health status of trees. Folia Microbiol. 2014;59(6):531–542. doi: 10.1007/s12223-014-0331-5. PubMed 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, Blaschke M. Phytophthora root and collar rot of alders in Bavaria: distribution, modes of spread and possible management strategies. Plant Pathol. 2004;53(2):197–208. doi: 10.1111/j.0032-0862.2004.00957.x. DOI

Jung T, Burgess TI. 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(1):95–110. PubMed PMC

Jung T, Nechwatal J. Phytophthora gallica sp. nov., a new species from rhizosphere soil of declining oak and reed stands in France and Germany. Mycol Res. 2008;112(10):1195–1205. doi: 10.1016/j.mycres.2008.04.007. 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(5):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, Nechwatal J, Cooke DE, Hartmann G, Blaschke M, Oßwald WF, Duncan JM, Delatour C. Phytophthora pseudosyringae sp. nov., a new species causing root and collar rot of deciduous tree species in Europe. Mycol Res. 2003;107(7):772–789. doi: 10.1017/S0953756203008074. PubMed DOI

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

Jung T, Vettraino AM, Cech TL, Vannini A. The impact of invasive Phytophthora species on European forests. In: Lamour K, editor. Phytophthora: A global perspective. Wallingford, UK: CABI; 2013. pp. 146–158.

Jung T, Orlikowski L, Henricot B, Abad-Campos P, Aday AG, Aguín Casal O, Bakonyi J, Cacciola SO, Cech T, Chavarriaga D, Corcobado T, Cravador A, Decourcelle T, Denton G, Diamandis S, Dogmus-Lehtijärvi HT, Franceschini A, Ginetti B, Glavendekić M, Green S, Hantula J, Hartmann G, Herrero M, Ivic D, Horta Jung M, Lilja A, Keca N, Kramarets V, Lyubenova A, Machado H, di San M, Lio G, Mansilla Vázquez PJ, Marçais B, Matsiakh I, Milenkovic I, Moricca S, Nagy ZÁ, Nechwatal J, Olsson C, Oszako T, Pane A, Paplomatas EJ, Pintos Varela C, Prospero S, Rial Martínez C, Rigling D, Robin C, Rytkönen A, Sánchez ME, Sanz Ros AV, Scanu B, Schlenzig A, Schumacher J, Slavov S, Solla A, Sousa E, Stenlid J, Talgø V, Tomic Z, Tsopelas P, Vannini A, Vettraino AM, Wenneker M, Woodward S, Peréz-Sierra A. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathol. 2016;46:134–163. doi: 10.1111/efp.12239. 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, Maia C, Abad-Campos P, Léon M, Horta Jung M. Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathol. 2017;66(2):194–211. doi: 10.1111/ppa.12564. DOI

Jung T, Horta Jung M, Scanu B, Seress D, Kovács GM, Maia C, Pérez-Sierra A, Chang T-T, Chandelier A, Heungens K, Van Poucke K, Abad-Campos P, Léon M, Caccioly SO, Bakonyi J. 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, Scanu B, Bakonyi J, Seress D, Kovács GM, Durán A, Sanfuentes von Stowasser E, Schena L, Mosca S, Thu PQ, Nguyen CM, Fajardo S, González M, Pérez-Sierra A, Rees H, Cravador A, Maia C, Horta Jung M. Nothophytophthora gen nov, a new sister genus of Phytophthora from natural and semi-natural ecosystems. Persoonia. 2017;39(1):143–174. doi: 10.3767/persoonia.2017.39.07. PubMed DOI PMC

Jung T, Durán A, Sanfuentes von Stowasser E, Schena L, Mosca S, Fajardo S, González M, Navarro Ortega AD, Bakonyi J, Seress D, Tomšovský M, Cravador A, Maia C, Horta Jung M. Diversity of Phytophthora species in Valdivian rainforests and association with severe dieback symptoms. For Pathol. 2018;48(5):e12443. doi: 10.1111/efp.12443. DOI

Jung T, Pérez-Sierra A, Durán A, Jung MH, Balci Y, Scanu B (2018b) Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia 40:182–220 PubMed PMC

Jung T, La Spada F, Pane A, Aloi F, Evoli M, Horta Jung M, Scanu B, Faedda R, Rizza C, Puglisi I, di San Lio GM, Schena L, Cacciola SO. Diversity and distribution of Phytophthora species in protected natural areas in Sicily. Forests. 2019;10(3):259. doi: 10.3390/f10030259. DOI

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

Jung T, Milenković I, Corcobado T, Májek T, Janoušek J, Kudláček T, Tomšovský M, Nagy Z, Durán A, Tarigan M, Sanfuentes von Stowasser E, Singh R, Ferreira M, Webber JF, Scanu B, Chi NM, Thu PQ, Junaid M, Rosmana A, Baharuddin B, Kuswinanti T, Nasri N, Kageyama K, Hieno A, Masuya H, Uematsu S, Oliva J, Redondo M, Maia C, Matsiakh I, Kramarets V, O’Hanlon R, Tomić Ž, Brasier CM, Horta Jung M. 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

Jung T, Blaschke M (2006) Management strategies for the Phytophthora root and collar rot epidemic of alders in Bavaria. In: Progress in Research on Phytophthora Diseases of Forest Trees. (Brasier, CM, Jung, T & Oßwald, W, eds). Proceedings of the 3rd International IUFRO Working Party 7.02.09 Meeting, 11th –17th Sept. 2004, Freising, Germany. Forest Research, Farnham, Surrey, UK: 61–66

Kanoun-Boulé M, Vasconcelos T, Gaspar J, Vieira S, Dias-Ferreira C, Husson C (2016) Phytophthora × alni and Phytophthora lacustris associated with common alder decline in Central Portugal. Forest Pathol 46:174–176

Kliejunas JT, Ko WH. Dispersal of Phytophthora cinnamomi on the island of Hawaii. Phytopathology. 1976;66(4):457–460. doi: 10.1094/Phyto-66-457. DOI

Klotz LJ, Wong PP, DeWolfe TA. Survey of irrigation water for the presence of Phytophthora spp. pathogenic to citrus. Plant Dis Rep. 1959;43:830–832.

Kreutzer WA, Bodine EW, Durrell LW (1940) Cucurbit diseases and rot of tomato fruit caused by Phytophthora capsici. Phytopathology 30:972–976

Kroon LPNM, Bakker FT, van den Bosch GBM, Bonants PJM, Flier WG. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genet Biol. 2004;41(8):766–782. doi: 10.1016/j.fgb.2004.03.007. PubMed DOI

Lacey J. The role of water in the spread of Phytophthora infestans in the potato crop. Ann Appl Biol. 1967;59(2):245–255. doi: 10.1111/j.1744-7348.1967.tb04433.x. DOI

Landa BB, Arias-Giraldo LF, Henricot B, Montes-Borrego M, Shuttleworth LA, Pérez-Sierra A. Diversity of Phytophthora species detected in disturbed and undisturbed British soils using high-throughput sequencing targeting ITS rRNA and COI mtDNA regions. Forests. 2021;12(2):229. doi: 10.3390/f12020229. DOI

Maia C, Horta Jung M, Carella G, Milenković I, Janoušek J, Tomšovský M, Mosca S, Schena L, Cravador A, Moricca S, Jung T. Eight new Halophytophthora species from marine and brackish-water ecosystems in Portugal and an updated phylogeny for the genus. Persoonia. 2022;48(1):54–90. doi: 10.3767/persoonia.2022.48.02. PubMed DOI PMC

Matsiakh I, Oszako T, Kramarets V, Nowakowska JA. Phytophthora and Pythium species detected in rivers of the Polish-Ukrainian border areas. Balt for. 2016;22(2):230–238.

Matsiakh I, Kramarets V, Cleary M. Occurrence and diversity of Phytophthora species in declining broadleaf forests in western Ukraine. For Pathol. 2021;51(1):e12662. doi: 10.1111/efp.12662. DOI

McIntosh DL. Phytophthora spp. in soils of the Okanagan and Similkameen valleys of British Columbia. Canad J Bot. 1964;42(10):1411–1415. doi: 10.1139/b64-137. DOI

Milenković I, Keča N, Karadžić D, Radulović Z, Nowakowska JA, Oszako T, Sikora K, Corcobado T, Jung T. Isolation and pathogenicity of Phytophthora species from poplar plantations in Serbia. Forests. 2018;9(6):330. doi: 10.3390/f9060330. DOI

Mrázkova M, Černý K, Tomšovský M, Strnadova V, Gregorová B, Holub V, Pánek M, Havrdová L, Hejna M. Occurrence of Phytophthora multivora and Phytophthora plurivora in the Czech Republic. Plant Prot Sci. 2013;49(4):155–164. doi: 10.17221/74/2012-PPS. DOI

Murphy SK, Lee C, Valachovic Y, Bienapfl J, Mark W, Jirka A, Rizzo DM (2008) Monitoring Phytophthoraramorum distribution in streams within California watersheds. In: Proceedings of the Sudden Oak Death Third Symposium. US Forest Service, Pacific Southwest Research Station, Albany, CA, USA, Vol. PSW-GTR-214, 409–411 pp

Nagel JH, Gryzenhout M, Slippers B, Wingfield MJ, Hardy GES, Stukely MJC, Burgess TI. Characterization of Phytophthora hybrids from ITS clade 6 associated with riparian ecosystems in South Africa and Australia. Fungal Biol. 2013;117(5):329–347. doi: 10.1016/j.funbio.2013.03.004. PubMed DOI

Nagel JH, Slippers B, Wingfield MJ, Gryzenhout M. Multiple Phytophthora species associated with a single riparian ecosystem in South Africa. Mycologia. 2015;107(5):915–925. doi: 10.3852/13-380. PubMed DOI

Nagy ZÁ, Bakonyi J, Ersek T. Standard and Swedish variant types of the hybrid alder Phytophthora attacking alder in Hungary. Pest Manag Sci. 2003;59(4):484–492. doi: 10.1002/ps.681. PubMed DOI

Navarro S, Sims L, Hansen E. Pathogenicity to alder of Phytophthora species from riparian ecosystems in western Oregon. For Pathol. 2015;45(5):358–366. doi: 10.1111/efp.12175. DOI

Nechwatal J, Bakonyi J, Cacciola SO, Cooke DEL, Jung T, Nagy ZÁ, Vannini A, Vettraino AM, Brasier CM. The morphology, behaviour and molecular phylogeny of Phytophthora taxon Salixsoil and its redesignation as Phytophthora lacustris sp nov. Plant Pathol. 2013;62(2):355–369. doi: 10.1111/j.1365-3059.2012.02638.x. DOI

Nigrelli L, Thines M. Tropical oomycetes in the German Bight – Climate warming or overlooked diversity? Fungal Ecol. 2013;6(2):152–160. doi: 10.1016/j.funeco.2012.11.003. DOI

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

O’Hanlon R, Choiseul J, Corrigan M, 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

O’Hanlon R, Choiseul J, Brennan JM, Grogan H. Assessment of the eradication measures applied to Phytophthora ramorum in Irish Larix kaempferi forests. For Pathol. 2018;48(1):e12389. doi: 10.1111/efp.12389. DOI

O’Hanlon R, Destefanis M, Milenković I, Tomšovský M, Janoušek J, Bellgard SE, Weir BS, 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(5):e0250527. doi: 10.1371/journal.pone.0250527. PubMed DOI PMC

Oberacker P, Stepper P, Bond DM, Höhn S, Focken J, Meyer V, Schelle L, Sugrue VJ, Jeunen GJ, Moser T, Hore SR, von Meyenn F, Hipp K, Hore TA, Jurkowski TP. Bio-On-Magnetic-Beads (BOMB): Open platform for high-throughput nucleic acid extraction and manipulation. PLoS Biol. 2019;17(1):e3000107. doi: 10.1371/journal.pbio.3000107. PubMed DOI PMC

Orlikowski LB, Ptaszek M, Rodziewicz A, Nechwatal J, Thinggaard K, Jung T. Phytophthora root and collar rot of mature Fraxinus excelsior in forest stands in Poland and Denmark. For Pathol. 2011;41(6):510–519. doi: 10.1111/j.1439-0329.2011.00714.x. DOI

Orlikowski LB, Oszako T, Szkuta G (2003) First record of alder Phytophthora in Poland. J Plant Prot Res 43(1):33–39

Oudemans PV. Phytophthora species associated with cranberry root rot and surface irrigation water in New Jersey. Plant Dis. 1999;83(3):251–258. doi: 10.1094/PDIS.1999.83.3.251. PubMed DOI

Pérez-Sierra A, Kalantarzadeh M, Sancisi-Frey S, Brasier CM (2015) Phytophthora siskiyouensis causing stem lesions and cankers on Alnus incana. New Dis Rep  31:17

Pintos C, Rial C, Aguín O, Ferreiroa V, Mansilla JP (2016) First report of Phytophthora hydropathica in river water associated with riparian alder in Spain. New Dis Rep 33:25

Pisetta M, Montecchio L, Longa CMO, Salvadori C, Zottele F, Maresi G. Green alder decline in the Italian Alps. For Ecol Manag. 2012;281:75–83. doi: 10.1016/j.foreco.2012.06.024. DOI

Podger FD, Doepel RF, Zentmyer GA. Association of Phytophthora cinnamomi with a disease of Eucalyptus marginata forest in Western Australia. Plant Dis Rep. 1965;49(11):943–957.

Redondo MA, Boberg J, Olsson CH, Oliva J (2015) Winter conditions correlate with Phytophthora alni subspecies distribution in Southern Sweden. Phytopathology 105(9):1191–1197 PubMed

Redondo MA, Boberg J, Stenlid J, Oliva J. Contrasting distribution patterns between aquatic and terrestrial Phytophthora species along a climatic gradient are linked to functional traits. ISME J. 2018;12:2967–2980. doi: 10.1038/s41396-018-0229-3. PubMed DOI PMC

Redondo MA, Boberg J, Stenlid J, Oliva J. Functional traits associated with the establishment of introduced Phytophthora spp in Swedish forests. J Appl Ecol. 2018;55(3):1538–1552. doi: 10.1111/1365-2664.13068. DOI

Reeser PW, Sutton W, Hansen EM, Remigi P, Adams GC. Phytophthora species in forest streams in Oregon and Alaska. Mycologia. 2011;103(1):22–35. doi: 10.3852/10-013. PubMed DOI

Riolo M, La Spada F, Aloi F, Giusso del Galdo G, Santilli E, Pane A, Cacciola SO. Phytophthora diversity in a sentinel arboretum and in a nature reserve area. Biol Life Sci Forum. 2020;4(1):51.

Robideau GP, de Cock AWAM, Coffey MD, Voglmayr H, Brouwer H, Bala K, Chitty DW, Désaulniers N, Eggertson QA, Gachon CMM, Hu CH, Küpper FC, Rintoul TL, Sarhan E, Verstappen ECP, Zhang Y, Bonants PJM, Ristaino JB, Lévesque AC. DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Mol Ecol Resour. 2011;11(6):1002–1011. doi: 10.1111/j.1755-0998.2011.03041.x. PubMed DOI PMC

Santilli E, Riolo M, La Spada F, Pane A, Cacciola SO. First report of root rot caused by Phytophthora bilorbang on Olea europaea in Italy. Plants. 2020;9(7):826. doi: 10.3390/plants9070826. PubMed DOI PMC

Santini A, Barzanti GP, Capretti P. A new Phytophthora root disease of alder in Italy. Plant Dis. 2001;85(5):560–560. doi: 10.1094/PDIS.2001.85.5.560A. PubMed DOI

Scanu B, Linaldeddu BT, 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(12):e0143234. doi: 10.1371/journal.pone.0143234. PubMed DOI PMC

Seddaiu S, Linaldeddu BT. First Report of Phytophthora acerina, P plurivora, and P pseudocryptogea associated with declining common alder trees in Italy. Plant. 2020;104(6):1874.

Seddaiu S, Brandano A, Ruiu PA, Sechi C, Scanu B. An Overview of Phytophthora species inhabiting declining Quercus suber stands in Sardinia (Italy) Forests. 2020;11(9):971. doi: 10.3390/f11090971. DOI

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

Sims LL, Sutton W, Reeser P, Hansen EM. The Phytophthora species assemblage and diversity in riparian alder ecosystems of western Oregon, USA. Mycologia. 2015;107(5):889–902. doi: 10.3852/14-255. PubMed DOI

Solla A, Pérez-Sierra A, Corcobado T, Haque MM, Diez JJ, Jung T. Phytophthora alni on Alnus glutinosa reported for the first time in Spain. Plant Pathol. 2010;59(4):798–798. doi: 10.1111/j.1365-3059.2009.02254.x. DOI

Stamler RA, Sanogo S, Goldberg NP, Randall JJ. Phytophthora species in rivers and streams of the southwestern United States. Appl Environ Microbiol. 2016;82(15):4696–4704. doi: 10.1128/AEM.01162-16. PubMed DOI PMC

Štěpánková P, Černý K, Strnadova V, Hanáček P, Tomšovský M. Identification of Phytophthora alni subspecies in riparian stands in the Czech Republic. Plant Prot Sci. 2013;49:3–10. doi: 10.17221/41/2013-PPS. DOI

Streito JC, Legrand PH, Tabary F, Jarnouen de Villartay GJD. Phytophthora disease of alder (Alnus glutinosa) in France: Investigations between 1995 and 1999. For Pathol. 2002;32(3):179–191. doi: 10.1046/j.1439-0329.2002.00282.x. DOI

Sutton W, Hansen EM, Reeser PW, Kanaskie A. Stream monitoring for detection of Phytophthora ramorum in Oregon tanoak forests. Plant Dis. 2009;93(11):1182–1186. doi: 10.1094/PDIS-93-11-1182. PubMed DOI

Thomson SV, Allen RM. Occurrence of Phytophthora species and other potential plant pathogens in recycled irrigation water. Plant Dis Rep. 1974;58(10):945–949.

Trzewik A, Orlikowski LB, Oszako T, Nowakowska JA, Orlikowska T. The characterization of Phytophthora isolates obtained from diseased Alnus glutinosa in Poland. Balt for. 2015;21(1):44–50.

Tsao PH. Why many Phytophthora root rots and crown rots of tree and horticultural crops remain undetected 1. Bull OEPP. 1990;20(1):11–17. doi: 10.1111/j.1365-2338.1990.tb01174.x. DOI

Tucker CM, Milbrath JA. Root rot of Chamaecyparis caused by a species of Phytophthora. Mycologia. 1942;34(1):94–103. doi: 10.1080/00275514.1942.12020875. DOI

Van Poucke K, Haegeman A, Goedefroit T, Focquet F, Leus L, Jung MH, Nave C, Redondo MA, Husson C, Kostov K, Lyubenova A, Christova P, Chandelier A, Slavov S, De Cock A, Bonants P, Werres S, Oliva Palau J, Marçais B, Jung T, Stenlid J, Ruttink T, Heungens K. Unravelling hybridization in Phytophthora using phylogenomics and genome size estimation. IMA Fungus. 2021;12(1):1–24. PubMed PMC

Von Broembsen S. Distribution of Phytophthora cinnamomi in rivers of the south-western Cape Province. Phytophylactica. 1984;16(3):227–230.

White TJ, Bruns T, Lee SJWT, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky J, White TJ, editors. PCR Protocols: a Guide to Methods and Applications. San Diego: Academic Press; 1990. pp. 315–322.

Xu X, Huai W, Hamiti ZX, Zhao W. Phytophthora species from Xinjiang wild apple forests in China. Forests. 2019;10:927. doi: 10.3390/f10100927. DOI

Yang X, Hong C (2014) Halophytophthora fluviatilis sp. nov. from freshwater in Virginia. FEMS Microbiol Lett 352:230–237 PubMed

Yang X, Richardson PA, Hong C. Phytophthora× stagnum nothosp nov, a new hybrid from irrigation reservoirs at ornamental plant nurseries in Virginia. PLoS ONE. 2014;9(7):e103450. doi: 10.1371/journal.pone.0103450. PubMed DOI PMC

Zamora-Ballesteros C, Haque MMU, Diez JJ, Martín-García J. Pathogenicity of Phytophthora alni complex and P. plurivora in Alnus glutinosa seedlings. For Pathol. 2017;47(2):e12299. doi: 10.1111/efp.12299. DOI

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