The symptoms of crown rot on strawberry plants are considered typical for the pathogen Phytophthora cactorum, which causes high losses of this crop. However, an unknown number of related species of pathogens of Peronosporales cause symptoms quite similar to those caused by P. cactorum. To determine their spectrum and importance, strawberry plants were sampled from 41 farms in the Czech Republic. The cultures were isolated from the symptomatic plants using the baiting method, with subsequent cultivation on a semiselective medium. Isolates were identified to the species level using nuclear ribosomal internal transcribed spacer (ITS) barcoding after preliminary morphological determination. In total, 175 isolates of 24 species of Phytophthora, Phytopythium, Pythium, and Globisporangium were detected. The most represented was Phytophthora cactorum, with 113 (65%) isolates, which was recorded in 61% of farms, and the Pythium dissotocum complex with 20 (11%) isolates, which was recorded in 27% of farms. Other species were represented in units of percent. Large differences between farms in the species spectra were ascertained. The differences between species in cardinal growth temperatures and different management of the farms are discussed as a main reason for such a diversification. Regarding the dissimilar sensitivity of various species of Peronosporales against fungicides, the proper determination of the cause of disease is of crucial significance in plant protection.

Department of Plant Protection Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 165 00 Prague Czech Republic

Team of Ecology and Diagnostics of Fungal Plant Pathogens Crop Research Institute Drnovská 507 73 161 06 Prague Czech Republic

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Jarvis W.R. The infection of strawberry and raspberry fruits by Botrytis cinerea Fr. Ann. Appl. Biol. 1962;50:569–575. doi: 10.1111/j.1744-7348.1962.tb06049.x. DOI

Pegg G.F. The impact of Verticillium diseases in agriculture. Phytopathol. Mediterr. 1984;23:176–192.

Eikemo H., Stensvand A., Davik J., Tronsmo A.M. Resistance to crown rot (Phytophthora cactorum) in strawberry cultivars and in offspring from crosses between cultivars differing in susceptibility to the disease. Ann. Appl. Biol. 2003;142:83–89. doi: 10.1111/j.1744-7348.2003.tb00232.x. DOI

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

Hantula J., Lilja A., Parikka P. Genetic variation and host specificity of Phytophthora cactorum isolated in Europe. Mycol. Res. 1997;101:565–572. doi: 10.1017/S0953756296002900. DOI

Winterbottom C., Westerlund F., Mircetich J., Galper L., Welch N. Evaluation of relative resistance of different strawberry cultivars to Phytophthora and Verticillium dahliae as a potential alternative to methyl bromide; Proceedings of the Annual International Research Conference on Methyl Bromide Alternatives and Emissions Reductions; Orlando, FL, USA. 4–6 November 1996; pp. 36-31–36-35.

Delmas C.E., Mazet I.D., Jolivet J., Delière L., Delmotte F. Simultaneous quantification of sporangia and zoospores in a biotrophic oomycete with an automatic particle analyzer: Disentangling dispersal and infection potentials. J. Microbiol. Methods. 2014;107:169–175. doi: 10.1016/j.mimet.2014.10.012. PubMed DOI

Raftoyannis Y., Dick M.W. Zoospore encystment and pathogenicity of Phytophthora and Pythium species on plant roots. Microbiol. Res. 2006;161:1–8. doi: 10.1016/j.micres.2005.04.003. PubMed DOI

Darmono T.W., Parke J.L. Chlamydospores of Phytophthora cactorum: Their production, structure, and infectivity. Can. J. Bot. 1990;68:640–645. doi: 10.1139/b90-083. DOI

Harris D.C. Survival of Phytophthora syringae oospores in and on apple orchard soil. Trans. Br. Mycol. Soc. 1985;85:153–155. doi: 10.1016/S0007-1536(85)80165-0. DOI

Sneh B., McIntosh D.L. Studies on the behavior and survival of Phytophthora cactorum in soil. Can. J. Bot. 1974;52:795–802. doi: 10.1139/b74-103. DOI

Abad Z.G., Abad J.A., Coffey M.D., Oudemans P.V., Man in’t Veld W.A., de Gruyter H., Cunnington J., Louws F.J. Phytophthora bisheria sp. nov., a new species identified in isolates from the Rosaceous raspberry, rose and strawberry in three continents. Mycologia. 2008;100:99–110. doi: 10.1080/15572536.2008.11832502. PubMed DOI

Barboza E.A., Fonseca M.E.N., Boiteux L.S., Reis A. First worldwide report of a strawberry fruit rot disease caused by Phytophthora capsici isolates. Plant Dis. 2017;101:259. doi: 10.1094/PDIS-06-16-0864-PDN. DOI

Hickman C.J. The red core root disease of the strawberry caused by Phytophthora fragariae n.sp. J. Pomol. Hortic. Sci. 1941;18:89–118. doi: 10.1080/03683621.1941.11513556. DOI

Irzykowska L., Irzykowski W., Jarosz A., Golebniak B. Association of Phytophthora citricola with leather rot disease of strawberry. J. Phytopathol. 2005;153:680–685. doi: 10.1111/j.1439-0434.2005.01037.x. DOI

Parikka P.K., Vestberg M., Karhu S.T., Haikonen T., Hautsalo J. Possibilities for biological control of red core (Phytophthora fragariae) VIII Int. Strawb. Symp. 2017;1156:751–756. doi: 10.17660/ActaHortic.2017.1156.110. DOI

Rahman M.Z., Uematsu S., Takeuchi T., Shirai K., Ishiguro Y., Suga H., Kageyama K. Two new species, Phytophthora nagaii sp. nov. and P. fragariaefolia sp. nov., causing serious diseases on rose and strawberry plants, respectively, in Japan. J. Gen. Plant Pathol. 2014;80:348–365. doi: 10.1007/s10327-014-0519-1. DOI

Rytkönen A., Lilja A., Vercauteren A., Sirkiä S., Parikka P., Soukainen M., Hantula J. Identity and potential pathogenicity of Phytophthora species found on symptomatic Rhododendron plants in a Finnish nursery. Can. J. Plant Pathol. 2012;34:255–267. doi: 10.1080/07060661.2012.686455. DOI

Suzui T., Makino T., Ogoshi A. Phytophthora rot of strawberry caused by Phytophthora nicotianae var. parasitica in Shizuoka. Jap. J. Phytopathol. 1980;46:169–178. doi: 10.3186/jjphytopath.46.169. DOI

De Cock A.W., 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

Uzuhashi S., Tojo M., Kakishima M. Phylogeny of the genus Pythium and description of new genera. Mycoscience. 2010;51:337–365. doi: 10.1007/S10267-010-0046-7. DOI

Eden M.A., Hill R.A. First record of Pythium mastophorum in New Zealand and its pathogenicity relative to other Pythium spp. N. Z. J. Crop Hortic. Sci. 1998;26:253–256. doi: 10.1080/01140671.1998.9514061. DOI

Ishiguro Y., Otsubo K., Watanabe H., Suzuki M., Nakayama K., Fukuda T., Fujinaga M., Suga H., Kageyama K. Root and crown rot of strawberry caused by Pythium helicoides and its distribution in strawberry production areas of Japan. J. Gen. Plant Pathol. 2014;80:423–429. doi: 10.1007/s10327-014-0520-8. DOI

Marin M.V., Seijo T., Mertely J., Peres N.A. First report of crown rot caused by Phytopythium helicoides on strawberry in the Americas. Plant Dis. 2019;103:2696. doi: 10.1094/PDIS-03-19-0658-PDN. DOI

Mouden N., Benkirane R., Ouazzani Touhami A., Douira A. Fungal species associated with collapsed strawberry plants cultivated in strawberries plantations in Morocco. Int. J. Curr. Res. 2016;8:29108–29117.

Shennan C., Muramoto J., Koike S., Baird G., Fennimore S., Samtani J., Bolda M., Dara S., Daugovish O., Lazarovits G., et al. Anaerobic soil disinfestation is an alternative to soil fumigation for control of some soilborne pathogens in strawberry production. Plant Pathol. 2018;67:51–66. doi: 10.1111/ppa.12721. DOI

Toljamo A.R., Granlund L.J., Kokko H.I. DNA barcode identification and virulence testing of Phytophthora spp. and Pythium spp. isolated from soil of strawberry fields. VIII Int. Strawb. Symp. 2017;1156:727–734. doi: 10.17660/ActaHortic.2017.1156.107. DOI

Watanabe T. Pathogenicity of Pythium myriotylum isolated from strawberry roots in Japan. Ann. Phytopath. Soc. Jpn. 1977;43:306–309. doi: 10.3186/jjphytopath.43.306. DOI

Watanabe T., Hashimoto K., Sato M. Pythium species associated with strawberry roots in Japan, and their role in the strawberry stunt disease. Phytopathology. 1977;67:1324–1332. doi: 10.1094/Phyto-67-1324. DOI

Fang X.L., Phillips D., Li H., Sivasithamparam K., Barbetti M.J. Severity of crown and root diseases of strawberry and associated fungal and oomycete pathogens in Western Australia. Australas. Plant Pathol. 2011;40:109–119. doi: 10.1007/s13313-010-0019-5. DOI

Fang X.L., Phillips D., Li H., Sivasithamparam K., Barbetti M.J. Comparisons of virulence of pathogens associated with crown and root diseases of strawberry in Western Australia with special reference to the effect of temperature. Sci. Hortic. 2011;131:39–48. doi: 10.1016/j.scienta.2011.09.025. DOI

LaMondia J. Strawberry black root rot. Adv. Strawb. Res. 2004;23:1–10.

Martin F.N. Strawberry root rot and the recovery of Pythium and Rhizoctonia spp; Proceedings of the Annual International Research Conference on Methyl Bromide Alternatives and Emissions Reductions; San Diego, CA, USA. 1–4 November 1999.

Burdon J.J., Chilvers G.A. Epidemiology of damping-off disease (Pythium irregulare) in relation to density of Lepidium sativum seedlings. Ann. Appl. Biol. 1975;81:135–143. doi: 10.1111/j.1744-7348.1975.tb00530.x. DOI

Green H., Jensen D.F. Disease progression by active mycelial growth and biocontrol of Pythium ultimum var. ultimum studied using a rhizobox system. Phytopathology. 2000;90:1049–1055. doi: 10.1094/PHYTO.2000.90.9.1049. PubMed DOI

Redekar N.R., Eberhart J.L., Parke J.L. Diversity of Phytophthora, Pythium, and Phytopythium species in recycled irrigation water in a container nursery. Phytobiomes J. 2019;3:31–45. doi: 10.1094/PBIOMES-10-18-0043-R. DOI

Lookabaugh E.C., Ivors K.L., Shew B.B. Mefenoxam sensitivity, aggressiveness, and identification of Pythium species causing root rot on floriculture crops in North Carolina. Plant Dis. 2015;99:1550–1558. doi: 10.1094/PDIS-02-15-0232-RE. PubMed DOI

Htun Z.M., Rotchanapreeda T., Rujirawat T., Lohnoo T., Yingyong W., Kumsang Y., Sae-Chew P., Payattikul P., Yurayart C., Limsivilai O., et al. Loop-mediated isothermal amplification (LAMP) for identification of Pythium insidiosum. Int. J. Infect. Dis. 2020;101:149–159. doi: 10.1016/j.ijid.2020.09.1430. PubMed DOI

Olson J.D., Damicone J.P., Kahn B.A. Identification and characterization of isolates of Pythium and Phytophthora spp. from snap beans with cottony leak. Plant Dis. 2016;100:1446–1453. doi: 10.1094/PDIS-06-15-0662-RE. PubMed DOI

Radmer L., Anderson G., Malvick D.M., Kurle J.E., Rendahl A., Mallik A. Pythium, Phytophthora, and Phytopythium spp. associated with soybean in Minnesota, their relative aggressiveness on soybean and corn, and their sensitivity to seed treatment fungicides. Plant Dis. 2017;101:62–72. doi: 10.1094/PDIS-02-16-0196-RE. PubMed DOI

Themann K., Werres S. Baiting of Phytophthora sp. with the Rhododendron leaf test; Proceedings of the First International Meeting on Phytophthoras in Forest and Wildland Ecosystems; Grants Pass, OR, USA. 30 August–3 September 1999.

Balcì 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

Tsao P.H. Factors affecting isolation and quantitation of Phytophthora from soil. In: Erwin D.C., Bartnicki-Garcia S., Tsao P.H., editors. Phytophthora: Its Biology, Taxonomy, Ecology, and Pathology. 1st ed. American Phytopathological Society; St. Paul, MN, USA: 1983. pp. 219–236.

Kageyama K. Molecular taxonomy and its application to ecological studies of Pythium species. J. Gen. Plant Pathol. 2014;80:314–326. doi: 10.1007/s10327-014-0526-2. 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. 1st ed. Academic Press, Inc.; San Diego, CA, USA: 1990. pp. 315–322.

Lévesque C.A., de Cock A.W. Molecular phylogeny and taxonomy of the genus. Pythium. Mycol. Res. 2004;108:1363–1383. doi: 10.1017/S0953756204001431. PubMed DOI

Petkowski J.E., de Boer R.F., Norng S., Thomson F., Minchinton E.J. Pythium species associated with root rot complex in winter-grown parsnip and parsley crops in south eastern Australia. Australas. Plant Pathol. 2013;42:403–411. doi: 10.1007/s13313-013-0211-5. DOI

Bose T., Wingfield M.J., Roux J., Vivas M., Burgess T.I. Community composition and distribution of Phytophthora species across adjacent native and non-native forests of South Africa. Fungal Ecol. 2018;36:17–25. doi: 10.1016/j.funeco.2018.09.001. DOI

Khaliq I., Hardy G.E.S.J., White D., Burgess T.I. eDNA from roots: A robust tool for determining Phytophthora communities in natural ecosystems. FEMS Microbiol. Ecol. 2018;94:fiy048. doi: 10.1093/femsec/fiy048. PubMed DOI

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

Nechwatal J., Bakonyi J., Cacciola S.O., Cooke D.E.L., Jung T., Nagy Z.Á., Vannini A., Vettraino A.M., Brasier C.M. The morphology, behaviour and molecular phylogeny of Phytophthora taxon Salixsoil and its redesignation as Phytophthora lacustris sp. nov. Plant Pathol. 2013;62:355–369. doi: 10.1111/j.1365-3059.2012.02638.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

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

Scanu B., Linaldeddu B., Pérez-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. doi: 10.14601/Phytopathol_Mediterr-14048. DOI

Erwin D.C., Ribeiro O.K. Phytophthora Diseases Worldwide. 1st ed. American Phytopathological Society; St Paul, MN, USA: 1996. p. 592.

Mostowfizadeh-Ghalamfarsa R., Panabieres F., Banihashemi Z., Cooke D.E.L. Phylogenetic relationship of Phytophthora cryptogea Pethybr. & Laff and P. drechsleri Tucker. Fungal Biol. 2010;114:325–339. doi: 10.1016/j.funbio.2010.02.001. PubMed DOI

Cohen S., Allasia V., Venard P., Notter S., Vernière C., Panabières F. Intraspecific variation in Phytophthora citrophthora from citrus trees in Eastern Corsica. Eur. J. Plant Pathol. 2003;109:791–805. doi: 10.1023/A:1026190318631. DOI

Nemec S. Histopathology of Pythium infected strawberry roots. Can. J. Bot. 1972;50:1091–1096. doi: 10.1139/b72-135. DOI

Van der Plaats-Niterink A.J. Monograph of the Genus Pythium. 1st ed. Centraalbureau voor Schimmelcultures; Baarn, The Netherlands: 1981. p. 244.

Badali F., Abrinbana M., Abdollahzadeh J., Khaledi E. Molecular and morphological taxonomy of Pythium species isolated from soil in West Azarbaijan province (N.W. Iran) Rostaniha. 2016;17:78–91. doi: 10.22092/botany.2016.107005. DOI

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

Ekwamu A., Mukalazi J., Buruchara R.A. Pythium Species in Bean Fields in Uganda. 1st ed. LAP LAMBERT Academic Publishing; Chisinau, Moldova: 2013. p. 136.

Hosseini Badrbani A., Abbasi S., Bolboli Z., Jamali S., Sharifi R. Morphological and molecular characterization of Oomycetes associated with root and crown rot of cucurbits in Kermanshah province, Iran. Mycol. Iran. 2018;5:15–27. doi: 10.22043/MI.2019.118409. DOI

Chen J.J., Yu J., Zhou Y.H., Yang H.J. Pythium glomeratum and Py. nodosum, two new records from China. J. Microbiol. Exp. 2020;8:24–28. doi: 10.15406/jmen.2020.08.00281. DOI

Le D.P., Smith M.K., Aitken E.A.B. An assessment of Pythium spp. associated with soft rot disease of ginger (Zingiber officinale) in Queensland, Australia. Australas. Plant Pathol. 2016;45:377–387. doi: 10.1007/s13313-016-0424-5. DOI

Li Y.P., You M.P., Barbetti M.J. Species of Pythium associated with seedling root and hypocotyl disease on common bean (Phaseolus vulgaris) in Western Australia. Plant Dis. 2014;98:1241–1247. doi: 10.1094/PDIS-12-13-1231-RE. PubMed DOI

McLeod A., Botha W.J., Meitz J.C., Spies C.F., Tewoldemedhin Y.T., Mostert L. Morphological and phylogenetic analyses of Pythium species in South Africa. Mycol. Res. 2009;113:933–951. doi: 10.1016/j.mycres.2009.04.009. PubMed DOI

Nechwatal J., Oßwald W.F. Pythium montanum sp. nov., a new species from a spruce stand in the Bavarian Alps. Mycol. Prog. 2003;2:73–80. doi: 10.1007/s11557-006-0046-3. DOI

Paul B., Galland D., Bhatnagar T., Dulieu H. A new species of Pythium isolated from the Burgundy region in France. FEMS Microbiol. Lett. 1998;158:207–213. doi: 10.1111/j.1574-6968.1998.tb12822.x. PubMed DOI

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

Weiland J.E., Beck B.R., Davis A. Pathogenicity and virulence of Pythium species obtained from forest nursery soils on Douglas-fir seedlings. Plant Dis. 2013;97:744–748. doi: 10.1094/PDIS-09-12-0895-RE. PubMed DOI

Belbahri L., McLeod A., Paul B., Calmin G., Moralejo E., Spies C.F.J., Botha W.J., Clemente A., Descals E., Sánchez-Hernández E., et al. Intraspecific and within-isolate sequence variation in the ITS rRNA gene region of Pythium mercuriale sp. nov. (Pythiaceae) FEMS Microbiol. Lett. 2008;284:17–27. doi: 10.1111/j.1574-6968.2008.01168.x. PubMed DOI

Bouket A.C., Babai-Ahari A., Arzanlou M., Tojo M. Morphological and molecular characterization of Phytopythium litorale and Pp. oedochilum from Iran. Nova Hedwig. 2015;102:257–270. doi: 10.1127/nova_hedwigia/2015/0307. DOI

Javadi N., Sharifnabi B. Phytopythium litorale, the causal agent of almond root and crown rot in Iran; Proceedings of the 22nd Iranian Plant Protection Congress; Karaj, Iran. 27–30 August 2016.

Nam B., Choi Y.J. Phytopythium and Pythium species (Oomycota) isolated from freshwater environments of Korea. Mycobiology. 2019;47:261–272. doi: 10.1080/12298093.2019.1625174. PubMed DOI PMC

Redekar N.R., Bourret T.B., Eberhart J.L., Johnson G.E., Pitton B.J.L., Haver D.L., Oki L.R., Parke J.L. The population of oomycetes in a recycled irrigation water system at a horticultural nursery in southern California. Water Res. 2020;183:116050. doi: 10.1016/j.watres.2020.116050. PubMed DOI

Rezaei S., Abrinbana M., Ghosta Y. Taxonomic and pathogenic characterization of Phytopythium species from West Azarbaijan, Iran, and description of two new species. Mycologia. 2021;113:612–628. doi: 10.1080/00275514.2020.1853986. PubMed DOI

Lischke H., Guisan A., Fischlin A., Williams J., Bugmann H. Vegetation responses to climate change in the Alps: Modeling studies. In: Cebon P., Dahinden U., Davies H., Imboden D., Jaeger C.C., editors. Views from the Alps. Regional Perspectives on Climate Change. 1st ed. MIT Press; Cambridge, MA, USA: 1998. pp. 309–350.

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

Pánek M., Střížková I., Zouhar M., Kudláček T., Tomšovský M. Mixed-mating model of reproduction revealed in European Phytophthora cactorum by ddRADseq and effector gene sequence data. Microorganisms. 2021;9:345. doi: 10.3390/microorganisms9020345. PubMed DOI PMC

Pánek M., Fér T., Mráček J., Tomšovský M. Evolutionary relationships within the Phytophthora cactorum species complex in Europe. Fungal Biol. 2016;120:836–851. doi: 10.1016/j.funbio.2016.03.006. PubMed DOI

Hantula J., Lilja A., Nuorteva H., Parikka P., Werres S. Pathogenicity, morphology and genetic variation of Phytophthora cactorum from strawberry, apple, rhododendron, and silver birch. Mycol. Res. 2000;104:1062–1068. doi: 10.1017/S0953756200002999. DOI

Bhat R.G., Colowit P.M., Tai T.H., Aradhya M.K., Browne G.T. Genetic and pathogenic variation in Phytophthora cactorum affecting fruit and nut crops in California. Plant Dis. 2006;90:161–169. doi: 10.1094/PD-90-0161. PubMed DOI

Eikemo H., Klemsdal S.S., Riisberg I., Bonants P., Stensvand A., Tronsmo A.M. Genetic variation between Phytophthora cactorum isolates differing in their ability to cause crown rot in strawberry. Mycol. Res. 2004;108:317–324. doi: 10.1017/S0953756204009244. PubMed DOI

Cooke D.E., 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

Christova P., Lyubenova A., Kostov K., Slavov S. Diversity and pathogenicity of Phytophthora species, isolated from Osam River. J. Mt. Agric. Balk. 2018;21:179–191.

Aghighi S., Hardy G.E.S.J., Scott J.K., Burgess T.I. Phytophthora bilorbang sp. nov., a new species associated with the decline of Rubus anglocandicans (European blackberry) in Western Australia. Eur. J. Plant Pathol. 2012;133:841–855. doi: 10.1007/s10658-012-0006-5. DOI

Ilieva E., Jamart G., Kamoen O. Characterisation of some isolates of Phytophthora cryptogea. Parasitica. 1992;48:113–122.

Meszka B., Michalecka M. Identification of Phytophthora spp. isolated from plants and soil samples on strawberry plantations in Poland. J. Plant Dis. Prot. 2016;123:29–36. doi: 10.1007/s41348-016-0007-2. DOI

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

Olson H.A., Benson D.M. Host specificity and variations in aggressiveness of North Carolina isolates of Phytophthora cryptogea and P. drechsleri in greenhouse ornamental plants. Plant Dis. 2013;97:74–80. doi: 10.1094/PDIS-02-12-0170-RE. PubMed DOI

Larsson M., Gerhardson B. Isolates of Phytophthora cryptogea pathogenic to wheat and some other crop plants. J. Phytopathol. 1990;129:303–315. doi: 10.1111/j.1439-0434.1990.tb04307.x. 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

Brasier C.M., Cooke D.E., 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

Schoebel C.N., Stewart J., Grünwald N.J., Rigling D., Prospero S. Population history and pathways of spread of the plant pathogen Phytophthora plurivora. PLoS ONE. 2014;9:e85368. doi: 10.1371/journal.pone.0085368. PubMed DOI PMC

Ko W.H., Chang M.S., Su H.J. Isolates of Phytophthora cinnamomi from Taiwan as evidence for an Asian origin of the species. Trans. Br. Mycol. Soc. 1978;71:496–499. doi: 10.1016/S0007-1536(78)80080-1. 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

Jung T., Scanu B., Brasier C.M., Webber J., Milenković I., Corcobado T., Tomšovský M., 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

Lilja A., Rytkönen A., Hantula J., Müller M., Kurkela T. Phytophthora cactorum, P. ramorum, P. plurivora, Melampsoridium hiratsukamum, Dothiostroma septosporum and Chalara fraxinea, non-native pathogens in Finland; Proceedings of the 7th Meeting of IUFRO Working Party 7.03.04 Diseases and Insects in Forest Nurseries; Hilo, HI, USA. 13–17 July 2010; pp. 55–62.

Laviola C., Somma V., Evola C. Present status of Phytophthora species in the Mediterranean area, especially in relation to citrus. EPPO Bull. 1990;20:1–9. doi: 10.1111/j.1365-2338.1990.tb01173.x. DOI

Pánek M., Střížková I. A comparison of the virulence of selected Pythium, Globisporangium, Phytopythium and Phytophthora species against strawberry plants. J. Plant Dis. Prot. 2021;128:1447–1458. doi: 10.1007/s41348-021-00531-1. DOI

Sutton J.C., Sopher C.R., Owen-Going T.N., Liu W., Grodzinski B., Hall J.C., Benchimol R.L. Etiology and epidemiology of Pythium root rot in hydroponic crops: Current knowledge and perspectives. Summa Phytopathol. 2006;32:307–321. doi: 10.1590/S0100-54052006000400001. DOI

Lugauskas A., Repečkiene J., Uselis N., Rašinskiene A. Problems on a longtime strawberry growing in one plot. Hortum Cultus. 2003;2:59–68.

Rojas J.A., Jacobs J.L., Napieralski S., Karaj B., Bradley C.A., Chase T., Esker P.D., Giesler L.J., Jardine D.J., Malvick D.K., et al. Oomycete species associated with soybean seedlings in North America—part I: Identification and pathogenicity characterization. Phytopathology. 2017;107:280–292. doi: 10.1094/PHYTO-04-16-0177-R. PubMed DOI

Zitnick-Anderson K.K., Nelson B.D., Jr. Identification and pathogenicity of Pythium on soybean in North Dakota. Plant Dis. 2015;99:31–38. doi: 10.1094/PDIS-02-14-0161-RE. PubMed DOI

Granke L.L., Hausbeck M.K. Effects of temperature, concentration, age, and algaecides on Phytophthora capsici zoospore infectivity. Plant Dis. 2010;94:54–60. doi: 10.1094/PDIS-94-1-0054. PubMed DOI

Littrell R.H., McCarter S.M. Effect of soil temperature on virulence of Pythium aphanidermatum and Pythium myriotylum to rye and tomato. Phytopathology. 1970;60:704–707. doi: 10.1094/Phyto-60-704. DOI

Grove G.G., Madden L.V., Ellis M.A. Splash dispersal of Phytophthora cactorum from infected strawberry fruit. Phytopathology. 1985;75:611–615. doi: 10.1094/Phyto-75-611. DOI

Ali-Shtayeh M.S. Taxonomic notes on three Pythium species. Trans. Br. Mycol. Soc. 1986;86:659–663. doi: 10.1016/S0007-1536(86)80072-9. DOI

Zhang B.Q., Chen W.D., Yang X.B. Occurrence of Pythium species in long-term maize and soybean monoculture and maize/soybean rotation. Mycol. Res. 1998;102:1450–1452. doi: 10.1017/S0953756298006510. DOI

Zhang Z.G., Li Y.Q., Fan H., Wang Y.C., Zheng X.B. Molecular detection of Phytophthora capsici in infected plant tissues, soil and water. Plant Pathol. 2006;55:770–775. doi: 10.1111/j.1365-3059.2006.01442.x. DOI

Van Poucke K., Haegeman A., Goedefroit T., Focquet F., Leus L., Jung M.H., Nave C., Redondo M.A., Husson C., Kostov K., et al. Unravelling hybridization in Phytophthora using phylogenomics and genome size estimation. IMA Fungus. 2021;12:16. doi: 10.1186/s43008-021-00068-w. PubMed DOI PMC

Martin F. Meiotic instability of Pythium sylvaticum as demonstrated by inheritance of nuclear markers and karyotype analysis. Genetics. 1995;139:1233–1246. doi: 10.1093/genetics/139.3.1233. PubMed DOI PMC

Li Y., Shen H., Zhou Q., Qian K., van der Lee T., Huang S. Changing ploidy as a strategy: The Irish potato famine pathogen shifts ploidy in relation to its sexuality. Mol. Plant-Microbe Interact. 2017;30:45–52. doi: 10.1094/MPMI-08-16-0156-R. PubMed DOI

Christova P.K., Kostov K.V., Lyubenova A.B., Slavov S.B. A new hybrid of Phytophthora from Southeast Europe. Mycologia. 2021;113:734–747. doi: 10.1080/00275514.2021.1897378. PubMed DOI

Sheltzer J.M., Blank H.M., Pfau S.J., Tange Y., George B.M., Humpton T.J., Brito I.L., Hiraoka Y., Niwa O., Amon A. Aneuploidy drives genomic instability in yeast. Science. 2011;333:1026–1030. doi: 10.1126/science.1206412. PubMed DOI PMC

Shaver A.C., Dombrowski P.G., Sweeney J.Y., Treis T., Zappala R.M., Sniegowski P.D. Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. Genetics. 2002;162:557–566. doi: 10.1093/genetics/162.2.557. PubMed DOI PMC

Sniegowski P.D., Gerrish P.J., Lenski R.E. Evolution of high mutation rates in experimental populations of E. coli. Nature. 1997;387:703–705. doi: 10.1038/42701. PubMed DOI

Xue B.K., Leibler S. Benefits of phenotypic plasticity for population growth in varying environments. Proc. Natl. Acad. Sci. USA. 2018;115:12745–12750. doi: 10.1073/pnas.1813447115. PubMed DOI PMC

De Cara M., Palmero D., Durán C., Lacasa C., Santos M., Coffey M.D., Tello J.C. Phytophthora parasitica showing host specificity and pathogenic ability on tomato and sweet pepper. In: Mendez-Vilas A., editor. Microorganisms in Industry and Environment from Scientific and Industrial Research to Consumer Products. 1st ed. World Scientific Publishing Co.; Lisbon, Portugal: 2010. pp. 101–105.

Wang Y., Meng Y., Zhang M., Tong X., Wang Q., Sun Y., Quan J., Govers F., Shan W. Infection of Arabidopsis thaliana by Phytophthora parasitica and identification of variation in host specificity. Mol. Plant Pathol. 2011;12:187–201. doi: 10.1111/j.1364-3703.2010.00659.x. PubMed DOI PMC

McHau G.R.A., Coffey M.D. An integrated study of morphological and isozyme patterns found within a worldwide collection of Phytophthora citrophthora and a redescription of the species. Mycol. Res. 1994;98:1291–1299. doi: 10.1016/S0953-7562(09)80301-8. DOI

Spies C.F., Meitz-Hopkins J.C., Langenhoven S.D., Pretorius M.C., McLeod A. Two clonal lineages of Phytophthora citrophthora from citrus in South Africa represent a single phylogenetic species. Mycologia. 2014;106:1106–1118. doi: 10.3852/13-228. PubMed DOI

Pánek M., Helmer Š., Ali A. Use of metalaxyl against some soil plant pathogens of the class Peronosporomycetes—A review and two case studies. Plant Prot. Sci. 2022 doi: 10.17221/42/2021-PPS. in press . DOI