Use of metalaxyl against some soil plant pathogens of the class Peronosporomycetes – A review and two case studies

https://doi.org/10.17221/42/2021-PPSCitation:

Pánek M., Ali A., Helmer Š. (2022): Use of metalaxyl against some soil plant pathogens of the class Peronosporomycetes – A review and two case studies. Plant Protect. Sci., 58: 92–109.

download PDF

Upon its discovery and implementation in plant protection, metalaxyl became one of the most important fungicides against Phytophthora infestans, but its efficiency has also been proven against other soil pathogens of the class Peronosporomycetes. The most important genus – Phytophthora comprises more than 150 plant pathogens, which cause significant losses in crop production or damage to natural plant associations. Many species of related genera Pythium, Phytopythium and Globisporangium have a similar ability as the species of Phytophthora. Those pathogens are able to quickly spread in wet soils by actively movable zoospores or in the air by means of zoosporangia; they are able to persist in an environment for long periods once they are introduced into the locality, having durability from their resting structures (chlamydospores, hyphal swelling and oospores). Metalaxyl has proven to be very efficient against these pathogens. However, shortly after its release, the rapid development of resistance against this compound was recorded in many species of the class Peronosporomycetes. Such easily developed resistance is due to the monogenic nature of the resistance, which also determines any anti-resistant strategies. The solution of this issue rests in the cautious use of metalaxyl, with consideration given to these strategies, and should be based also on precise information about the environment and the present pathogenic agents.

References:
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. (2008): Phytophthora bisheria sp. nov., a new species identified in isolates from the rosaceous raspberry, rose and strawberry in three continents. Mycologia, 100: 99–110.  https://doi.org/10.1080/15572536.2008.11832502
 
Adaskaveg J.E., Gubler D., Michailides T. (2017): Fungicides, Bactericides, and Biologicals for Deciduous Tree Fruit, Nut, Strawberry, and Vine Crops. Riverside, University of California.
 
Bagirova S.F., Li A.Z., Dolgova A.V., Elansky S.N., Shaw D.S., Dyakov Y.T. (2001): Mutants of Phytophthora infestans resistant to dimethomorph fungicide. Journal of Russian Phytopathological Society, 2: 19–24.
 
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. (2010): Phytopythium Abad, de Cock, Bala, Robideau, Lodhi & Lévesque, gen. nov. and Phytopythium sindhum Lodhi, Shahzad & Lévesque, sp. nov. Persoonia, 24: 137. doi: 10.3767/003158510X512748
 
Barboza E.A., Fonseca M.E.N., Boiteux L.S., Reis A. (2017): First worldwide report of a strawberry fruit rot disease caused by Phytophthora capsici isolates. Plant Disease, 101: 259. doi: 10.1094/PDIS-06-16-0864-PDN https://doi.org/10.1094/PDIS-06-16-0864-PDN
 
Barriuso J., Hogan D.A., Keshavarz T., Martínez M.J. (2018): Role of quorum sensing and chemical communication in fungal biotechnology and pathogenesis. FEMS Microbiology Reviews, 42: 627–638.  https://doi.org/10.1093/femsre/fuy022
 
Benfradj N., Migliorini D., Luchi N., Santini A., Boughalleb-M’Hamdi N. (2017): Occurrence of Pythium and Phytopythium species isolated from citrus trees infected with gummosis disease in Tunisia. Archives of Phytopathology and Plant Protection, 50: 286–302.  https://doi.org/10.1080/03235408.2017.1305479
 
Bergquist R.R. (1974): Effect of fungicide rate, spray interval, timing of spray application, and precipitation in relation to control of Phytophthora leaf blight of taro. Annals of Botany, 38: 213–221. https://doi.org/10.1093/oxfordjournals.aob.a084796
 
Bertier L., Leus L., D’hondt L., de Cock A.W.A.M., Höfte M. (2013): Host adaptation and speciation through hybridization and polyploidy in Phytophthora. PLoS One, 8: e85385. doi: 10.1371/journal.pone.0085385 https://doi.org/10.1371/journal.pone.0085385
 
Bhat R.G., McBlain B.A., Schmitthenner A.F. (1993): The inheritance of resistance to metalaxyl and to fluorophenylalanine in matings of homothallic Phytophthora sojae. Mycological Research, 97: 865–870.  https://doi.org/10.1016/S0953-7562(09)81164-7
 
Bourke P.M.A. (1964): Emergence of potato blight, 1843–46. Nature, 203: 805–808.  https://doi.org/10.1038/203805a0
 
Brantner J.R., Windels C.E. (1998): Variability in sensitivity to metalaxyl in vitro, pathogenicity, and control of Pythium spp. on sugar beet. Plant Disease, 82: 896–899.  https://doi.org/10.1094/PDIS.1998.82.8.896
 
Brasier C.M., Cooke D.E.L., Duncan J.M. (1999): Origin of a new Phytophthora pathogen through interspecific hybridization. Proceedings of the National Academy of Sciences of the United States of America, 96: 5878–5883.  https://doi.org/10.1073/pnas.96.10.5878
 
Brent K.J., Hollomon D.W. (2007): Fungicide Resistance in Crop Pathogens: How Can It Be Managed? Brussels, Fungicide Resistance Action Committee.
 
Broders K.D., Lipps P.E., Paul P.A., Dorrance A.E. (2007): Characterization of Pythium spp. associated with corn and soybean seed and seedling disease in Ohio. Plant Disease, 91: 727–735.  https://doi.org/10.1094/PDIS-91-6-0727
 
Bruck R.I., Fry W.E., Apple A.E. (1980): Effect of metalaxyl, an acylanine fungicide, on developmental stages of Phytophthora infestans. Phytopathology, 70: 597–601. https://doi.org/10.1094/Phyto-70-597
 
Burgess T.I. (2015): Molecular characterization of natural hybrids formed between five related indigenous clade 6 Phytophthora species. PLoS One, 10: e0134225. doi: 10.1371/journal.pone.0134225 https://doi.org/10.1371/journal.pone.0134225
 
Chabane K., Leroux P., Bompeix G., Maia N. (1996): Dimethomorph and metalaxyl sensitivity in somatic hybrids of Phytophthora parasitica obtained by protoplast fusion. Phytopathologia Mediteranea, 35: 111–116.
 
Chen F., Zhou Q., Xi J., Li D., Schnabel G., Zhan J. (2018): Analysis of RPA190 revealed multiple positively selected mutations associated with metalaxyl resistance in Phytophthora infestans. Pest Management Science, 74: 1916–1924.  https://doi.org/10.1002/ps.4893
 
Choudhary C.E., Burgos-Garay M.L., Moorman G.W., Hong C. (2016): Pythium and Phytopythium species in two Pennsylvania greenhouse irrigation water tanks. Plant Disease, 100: 926–932.  https://doi.org/10.1094/PDIS-07-15-0836-RE
 
Cohen Y., Samoucha Y. (1990): Competition between oxadixyl-sensitive and -resistant field isolates of Phytophthora infestans on fungicide-treated potato crops. Crop Protection, 9: 15–20. https://doi.org/10.1016/0261-2194(90)90040-E
 
Cohen Y., Reuveni M., Eyal H. (1979): The systemic antifungal activity of ridomil against Phytophthora infestans on tomato plants. Phytopathology, 69: 645–649. https://doi.org/10.1094/Phyto-69-645
 
Cooke L.R. (1992): Resistance to phenylamide fungicides: Strategies and their evaluation. In: Denholm I., Devonshire A.L., Hollomon D.W. (eds). Resistance ’91: Achievements and Developments in Combating Pesticide Resistance. Dordrecht, Springer: 100–111.
 
Crute I.R. (1992): The contribution of genetic studies to understanding fungicide resistance. In: Denholm I., Devonshire A.L., Hollomon D.W. (eds). Resistance ’91: Achievements and Developments in Combating Pesticide Resistance. Dordrecht, Springer: 190–202.
 
Daggett S.S. (1993): Phenotypic changes in populations of Phytophthora infestans from Eastern Germany. Phytopathology, 83: 319–323.  https://doi.org/10.1094/Phyto-83-319
 
Darvas J., Becker O. (1984): Failure to control Phytophthora cinnamomi and Pythium splendens with metalaxyl after its prolonged use. South African Avocado Growers’ Association Yearbook, 7: 77–78.
 
Davidse L.C. (1985): Resistance to acylalanines in Phytophthora infestans in The Netherlands. EPPO Bulletin, 15: 403–409.  https://doi.org/10.1111/j.1365-2338.1985.tb00247.x
 
Davidse L.C. (1995): Phenylamide fungicides: Biochemical action and resistance. In: Lyr H. (ed.). Modern Selective Fungicides. Jena, Gustav Fischer: 347–354.
 
Davidse L.C., Looijen D., Turkensteen L.J., van der Wal D. (1981): Occurrence of metalaxyl-resistant strains of Phytophthora infestans in Dutch potato fields. Netherlands Journal of Plant Pathology, 87: 65–68.  https://doi.org/10.1007/BF01976658
 
Davidse L.C., Danial D.L., van Westen C.J. (1983): Resistance to metalaxyl in Phytophthora infestans in the Netherlands. Netherlands Journal of Plant Pathology, 89: 1–20.  https://doi.org/10.1007/BF01974440
 
Davidse L.C., Gerritsma O.C.M., Ideler J., Pie K., Velthuis G.C.M. (1988): Antifungal modes of action of metalaxyl, cyprofuram, benalaxyl and oxadixyl in phenylamide-sensitive and phenylamide-resistant strains of Phytophthora megasperrna f. sp . medicaginis and Phytophthora infestans. Crop Protection, 7: 347–355. https://doi.org/10.1016/0261-2194(88)90001-4
 
Davis R.P., Dennis C. (1981): Properties of dicarboximide resistant strains of Botrytis cinerea. Pesticide Science, 12: 521–528. https://doi.org/10.1002/ps.2780120509
 
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. (2015): Phytopythium: Molecular phylogeny and systematics. Persoonia, 34: 25–39.  https://doi.org/10.3767/003158515X685382
 
Delmas C.E.L., Mazet I.D., Jolivet J., Delière L., Delmotte F. (2014): Simultaneous quantification of sporangia and zoospores in a biotrophic oomycete with an automatic particle analyzer: Disentangling dispersal and infection potentials. Journal of Microbiological Methods, 107: 169–175.  https://doi.org/10.1016/j.mimet.2014.10.012
 
Eden M.A., Hill R.A. (1998): First record of Pythium mastophorum in New Zealand and its pathogenicity relative to other Pythium spp. New Zealand Journal of Crop and Horticultural Science, 26: 253–256.  https://doi.org/10.1080/01140671.1998.9514061
 
Eikemo H., Stensvand A., Tronsmo A.M. (2000): Evaluation of methods of screening strawberry cultivars for resistance to crown rot caused by Phytophthora cactorum. Annals of Applied Biology, 137: 237–244.  https://doi.org/10.1111/j.1744-7348.2000.tb00064.x
 
Ellis M.A., Grove G.G., Ferree D.C. (1982): Effects of metalaxyl on Phytophthora cactorum and collar rot of apple. Phytopathology, 72: 1431–1434. https://doi.org/10.1094/Phyto-72-1431
 
Erwin D.C., Ribeiro O.K. (1996): Phytophthora diseases worldwide. St Paul, The American Phytopathological Society.
 
Fang X.L., Phillips D., Li H., Sivasithamparam K., Barbetti M.J. (2011): Severity of crown and root diseases of strawberry and associated fungal and Oomycete pathogens in Western Australia. Australasian Plant Pathology, 40: 109–119.  https://doi.org/10.1007/s13313-010-0019-5
 
Farih A., Tsao P.H., Menge J.A. (1981): In vitro effects of metalaxyl on growth, sporulation, and germination of Phytophthora parasitica and P. citrophthora. Plant Disease, 65: 651–654. https://doi.org/10.1094/PD-65-651
 
Fry W.E., Goodwin S.B., Dyer A.T., Matuszak J.M., Drenth A., Tooley P.W., Sujkowski L.S., Koh Y.J., Cohen B.A., Spielman L.J., Deahl K.L., Inglis D.A., Sandlan K.P. (1993): Historical and recent migrations of Phytophthora infestans: Chronology, pathways, and implications. Plant Disease, 77: 653–661. https://doi.org/10.1094/PD-77-0653
 
Fuller M.S., Gisi U. (1985): Comparative studies of the in vitro activity of the fungicides oxadixyl and metalaxyl. Mycologia, 77: 424–439.  https://doi.org/10.2307/3793199
 
Garcia-Rubio R., Cuenca-Estrella M., Mellado E. (2017): Triazole resistance in Aspergillus species: An emerging problem. Drugs, 77: 599–613.  https://doi.org/10.1007/s40265-017-0714-4
 
Garzón C.D., Geiser D.M., Moorman G.W. (2005): Diagnosis and population analysis of Pythium species using AFLP fingerprinting. Plant Disease, 89: 81–89.  https://doi.org/10.1094/PD-89-0081
 
Georgopoulos S.G. (1985): The genetic basis of classification of fungicides according to resistance risk. EPPO Bulletin, 15: 513–517.  https://doi.org/10.1111/j.1365-2338.1985.tb00263.x
 
Gisi U. (2007): Chemical control of downy mildews. In: Spencer-Phillips P.T.N., Gisi U., Lebeda A. (eds). Advances in Downy Mildew Research. Dordrecht, Springer: 119–159.
 
Gisi U., Cohen Y. (1996): Resistance to phenylamide fungicides: A case study with Phytophthora infestans involving mating type and race structure. Annual Review of Phytopathology, 34: 549–572.  https://doi.org/10.1146/annurev.phyto.34.1.549
 
Gisi U., Sierotzki H. (2008): Fungicide modes of action and resistance in downy mildews. European Journal of Plant Pathology, 122: 157–167. https://doi.org/10.1007/s10658-008-9290-5
 
Gisi U., Chin K.M., Knapova G., Küng Färber R., Mohr U., Parisi S., Sierotzki H., Steinfeld U. (2000): Recent developments in elucidating modes of resistance to phenylamide, DMI and strobilurin fungicides. Crop Protection, 19: 863–872.  https://doi.org/10.1016/S0261-2194(00)00114-9
 
Goodwin S.B., McGrath M.T. (1995): Insensitivity to metalaxyl among isolates of Phytophthora erythroseptica causing pink rot of potato in New York. Plant Disease, 79: 967. doi: 10.1094/PD-79-0967D https://doi.org/10.1094/PD-79-0967D
 
Goodwin S.B., Cohen B.A., Fry W.E. (1994): Panglobal distribution of a single clonal lineage of the Irish potato famine fungus. Proceedings of the National Academy of Sciences of the United States of America, 91: 11591–11595.  https://doi.org/10.1073/pnas.91.24.11591
 
Goodwin S.B., Sujkowski L.S., Fry W.E. (1996): Widespread distribution and probably origin of resistance to metalaxyl in clonal genotypes of Phytopthora infestans in the United States and Western Canada. Ecology and Epidemiology, 86: 793–800.
 
Grünwald N.J., Sturbaum A.K., Montes G.R., Serrano E.G., Lozoya-Saldaña H., Fry W.E. (2006): Selection for fungicide resistance within a growing season in field populations of Phytophthora infestans at the center of origin. Phytopathology, 96: 1397–1403.  https://doi.org/10.1094/PHYTO-96-1397
 
Hill S.N., Hausbeck M.K. (2008): Virulence and fungicide sensitivity of Phytophthora cactorum isolated from American ginseng gardens in Wisconsin and Michigan. Plant Disease, 92: 1183–1189. https://doi.org/10.1094/PDIS-92-8-1183
 
Hobbelen P.H.F., Paveley N.D., van den Bosch F. (2014): The emergence of resistance to fungicides. PLoS One, 9: e91910. doi: 10.1371/journal.pone.0091910 https://doi.org/10.1371/journal.pone.0091910
 
Hu J., Li Y. (2014): Inheritance of mefenoxam resistance in Phytophthora nicotianae populations from a plant nursery. European Journal of Plant Pathology, 139: 545–555.  https://doi.org/10.1007/s10658-014-0410-0
 
Huzar-Novakowiski J., Dorrance A.E. (2018): Genetic diversity and population structure of Pythium irregulare from soybean and corn production fields in Ohio. Plant Disease, 102: 1989–2000.  https://doi.org/10.1094/PDIS-11-17-1725-RE
 
Ioos R., Andrieux A., Marçais B., Frey P. (2006): Genetic characterization of the natural hybrid species Phytophthora alni as inferred from nuclear and mitochondrial DNA analyses. Fungal Genetics and Biology, 43: 511–529.  https://doi.org/10.1016/j.fgb.2006.02.006
 
Irzykowska L., Irzykowski W., Jarosz A., Golebniak B. (2005): Association of Phytophthora citricola with leather rot disease of strawberry. Journal of Phytopathology, 153: 680–685.  https://doi.org/10.1111/j.1439-0434.2005.01037.x
 
Ishiguro Y., Otsubo K., Watanabe H., Suzuki M., Nakayama K., Fukuda T., Fujinaga M., Suga H., Kageyama K. (2014): Root and crown rot of strawberry caused by Pythium helicoides and its distribution in strawberry production areas of Japan. Journal of General Plant Pathology, 80: 423–429.  https://doi.org/10.1007/s10327-014-0520-8
 
Jackson K.L., Yin J., Ji P. (2012): Sensitivity of Phytophthora capsici on vegetable crops in Georgia to mandipropamid, dimethomorph, and cyazofamid. Plant Disease, 96: 1337–1342.  https://doi.org/10.1094/PDIS-12-11-1082-RE
 
Jansen J.P., Lauvaux S., Gruntowy J., Denayer J. (2017): Possible synergistic effects of fungicide-insecticide mixtures on beneficial arthropods. Pesticides and Beneficial Organisms IOBC-WPRS Bulletin, 125: 28–35.
 
Jeffers S.N., Aldwinckle H.S. (1987): Enhancing detection of Phytophthora cactorum in naturally infested soil. Phytopathology, 77: 1475–1482. https://doi.org/10.1094/Phyto-77-1475
 
Jeffers S.N., Schnabel G., Smith J.P. (2004): First report of resistance to mefenoxam in Phytophthora cactorum in the United States and elsewhere. Plant Disease, 88: 576. doi: 10.1094/PDIS.2004.88.5.576A https://doi.org/10.1094/PDIS.2004.88.5.576A
 
Jeong S.Y., Lee C.H., Yi T., Kim T.G. (2020): Effects of quorum quenching on biofilm metacommunity in a membrane bioreactor. Microbial Ecology, 79: 84–97.  https://doi.org/10.1007/s00248-019-01397-5
 
Joseph M.C., Coffey M.D. (1984): Development of laboratory resistance to metalaxyl in Phytophthora citricola. Phytopathology, 74: 1411–1414.  https://doi.org/10.1094/Phyto-74-1411
 
Kato S., Coe R., New L., Dick M.W. (1990): Sensitivities of various Oomycetes to hymexazol and metalaxyl. Microbiology, 136: 2127–2134.
 
Kong P., Tyler B.M., Richardson P.A., Lee B.W.K., Zhou Z.S., Hong C. (2010): Zoospore interspecific signaling promotes plant infection by Phytophthora. BMC Microbiology, 10: 313. doi: 10.1186/1471-2180-10-313 https://doi.org/10.1186/1471-2180-10-313
 
Lebert H., Cohn F. (1870): Über die Fäule der Cactusstämme. Beiträge zur Biologie der Pflanzen, 1: 51–57. German.
 
Lucas J.A., Greer G., Oudemans P.V., Coffey M.D. (1990): Fungicide sensitivity in somatic hybrids of Phytophthora capsici obtained by protoplast fusion. Physiological and Molecular Plant Pathology, 36: 175–187.  https://doi.org/10.1016/0885-5765(90)90105-7
 
Mackrill J.J., Kehoe R.A., Zheng L., McKee M.L., O’Sullivan E.C., Prestwich B.M.D., McCarthy F.O. (2020): Inhibitory properties of aldehydes and related compounds against Phytophthora infestans – Identification of a new lead. Pathogens, 9: 542. doi: 10.3390/pathogens9070542 https://doi.org/10.3390/pathogens9070542
 
Malajczuk N., Boughton T.J., Campbell N.A., Litchfield R.T. (1983): Interaction between the fungicide metalaxyl and soil microorganisms on survival of Phytophthora cinnamomi. Annals of Applied Biology, 103: 57–61. https://doi.org/10.1111/j.1744-7348.1983.tb02740.x
 
Maridueña-Zavala M.G., Freire-Peñaherrera A., Cevallos-Cevallos J.M., Peralta E.L. (2017): GC-MS metabolite profiling of Phytophthora infestans resistant to metalaxyl. European Journal of Plant Pathology, 149: 563–574.  https://doi.org/10.1007/s10658-017-1204-y
 
Marin M.V., Seijo T., Mertely J., Peres N.A. (2019): First report of crown rot caused by Phytopythium helicoides on strawberry in the Americas. Plant Disease, 103: 2696. doi: 10.1094/PDIS-03-19-0658-PDN https://doi.org/10.1094/PDIS-03-19-0658-PDN
 
Martin F.N. (1999): Strawberry root rot and the recovery of Pythium and Rhizoctonia spp. In: Proceedings of Annual International Conference on Methyl Bromide: Alternatives and Emissions Reduction, November 1–4, 1999, San Diego, California: 1–3.
 
Matheron M.E., Porchas M. (2000): Impact of azoxystrobin, dimethomorph, fluazinam, fosetyl-Al, and metalaxyl on growth, sporulation, and zoospore cyst germination of three Phytophthora spp. Plant Disease, 84: 454–458.  https://doi.org/10.1094/PDIS.2000.84.4.454
 
Matson M.E.H., Small I.M., Fry W.E., Judelson H.S. (2015): Metalaxyl resistance in Phytophthora infestans: Assessing role of RPA190 gene and diversity within clonal lineages. Phytopathology, 105: 1594–1600.  https://doi.org/10.1094/PHYTO-05-15-0129-R
 
Mazzola M., Andrews P.K., Reganold J.P., Lévesque C.A. (2002): Frequency, virulence, and metalaxyl sensitivity of Pythium spp. isolated from apple roots under conventional and organic production systems. Plant Disease, 86: 669–675.  https://doi.org/10.1094/PDIS.2002.86.6.669
 
Middleton J.T. (1943): The taxonomy, host range and geographic distribution of the genus Pythium. Memoirs of the Torrey Botanical Club, 20: 1–171.
 
Mir A.A., Park S.Y., Sadat M.A., Kim S., Choi J., Jeon J., Lee Y.H. (2015): Systematic characterization of the peroxidase gene family provides new insights into fungal pathogenicity in Magnaporthe oryzae. Scientific Reports, 5: 11831. doi: 10.1038/srep11831 https://doi.org/10.1038/srep11831
 
Molina L., Constantinescu F., Michel L., Reimmann C., Duffy B., Défago G. (2003): Degradation of pathogen quorum-sensing molecules by soil bacteria: A preventive and curative biological control mechanism. FEMS Microbiology Ecology, 45: 71–81.  https://doi.org/10.1016/S0168-6496(03)00125-9
 
Montes M.S., Nielsen B.J., Schmidt S.G., Bødker L., Kjøller R., Rosendahl S. (2016): Population genetics of Phytophthora infestans in Denmark reveals dominantly clonal populations and specific alleles linked to metalaxyl-M resistance. Plant Pathology, 65: 744–753.  https://doi.org/10.1111/ppa.12462
 
Morton H.V., Urech P.A. (1988): History of development of resistance to phenylamide fungicides. In: Delp C.S. (ed.). Fungicide Resistance in North America. St. Paul, APS Press: 59–60.
 
Mouden N., Benkirane R., Ouazzani Touhami A., Douira A. (2016): Fungal species associated with collapsed strawberry plants cultivated in strawberries plantations in Morocco. International Journal of Current Research, 8: 29108–29117.
 
Nagel J.H., Gryzenhout M., Slippers B., Wingfield M.J., Hardy G.E.S.J., Stukely M.J.C., Burgess T.I. (2013): Characterization of Phytophthora hybrids from ITS clade 6 associated with riparian ecosystems in South Africa and Australia. Fungal Biology, 117: 329–347.  https://doi.org/10.1016/j.funbio.2013.03.004
 
Olson Å., Stenlid J. (2002): Pathogenic fungal species hybrids infecting plants. Microbes and Infection, 4: 1353–1359.  https://doi.org/10.1016/S1286-4579(02)00005-9
 
Pánek M., Fér T., Mráček J., Tomšovský M. (2016): Evolutionary relationships within the Phytophthora cactorum species complex in Europe. Fungal Biology, 120: 836–851.  https://doi.org/10.1016/j.funbio.2016.03.006
 
Pánek M., Střížková I., Zouhar M., Kudláček T., Tomšovský M. (2021a): Mixed-mating model of reproduction revealed in European Phytophthora cactorum by ddRADseq and effector gene sequence data. Microorganisms, 9: 345. doi: 10.3390/microorganisms9020345  https://doi.org/10.3390/microorganisms9020345
 
Pánek M., Hanáček A., Wenzlová J., Maňasová M., Zouhar M. (2021b): A comparison of the ability of some commercially produced biological control agents to protect strawberry plants against the plant pathogen Phytophthora cactorum. Agriculture, 11: 1086. doi: 10.3390/agriculture11111086 https://doi.org/10.3390/agriculture11111086
 
Parra G., Ristaino J.B. (2001): Resistance to mefenoxam and metalaxyl among field isolates of Phytophthora capsici causing Phytophthora blight of bell pepper. Plant Disease, 85: 1069–1075. https://doi.org/10.1094/PDIS.2001.85.10.1069
 
Patel N., Desa P., Patel N., Jha A., Gautam H.K. (2014): Agronanotechnology for plant fungal disease management: A review. International Journal of Current Microbiology and Applied Sciences, 3: 71–84.
 
Porter L.D., Hamm P.B., David N.L., Gieck S.L., Miller J.S., Gundersen B., Inglis D.A. (2009): Metalaxyl-M-resistant Pythium species in potato production areas of the Pacific Northwest of the U.S.A. American Journal of Potato Research, 86: 315–326.  https://doi.org/10.1007/s12230-009-9085-z
 
Rahman M.Z., Uematsu S., Takeuchi T., Shirai K., Ishiguro Y., Suga H., Kageyama K. (2014): Two new species, Phytophthora nagaii sp. nov. and P. fragariaefolia sp. nov., causing serious diseases on rose and strawberry plants, respectively, in Japan. Journal of General Plant Pathology, 80: 348–365.  https://doi.org/10.1007/s10327-014-0519-1
 
Randall E., Young V., Sierotzki H., Scalliet G., Birch P.R.J., Cooke D.E.L., Csukai M., Whisson S.C. (2014): Sequence diversity in the large subunit of RNA polymerase I contributes to mefenoxam insensitivity in Phytophthora infestans. Molecular Plant Pathology, 15: 664–676.  https://doi.org/10.1111/mpp.12124
 
Rani D.V., Sudini H. (2013): Management of soilborne diseases in crop plants: An overview. International Journal of Plant, Animal and Environmental Sciences, 3: 156–164.
 
Raymond M., Callaghan A., Fort P., Pasteur N. (1991): Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature, 350: 151–153.  https://doi.org/10.1038/350151a0
 
Reeleder R.D., Miller J., Capell B., Schooley J. (2007): Mefenoxam sensitivity and the impact of fumigation on Pythium species and Phytophthora cactorum in ginseng soils. Canadian Journal of Plant Pathology, 29: 427–436. https://doi.org/10.1080/07060660709507489
 
Rekanović E., Potočnik I., Milijašević-Marčić S., Stepanović M., Todorović B., Mihajlović M. (2012): Toxicity of metalaxyl, azoxystrobin, dimethomorph, cymoxanil, zoxamide and mancozeb to Phytophthora infestans isolates from Serbia. Journal of Environmental Science and Health, Part B, Pesticides, Food Contaminants, and Agricultural Wastes, 47: 403–409.
 
Reuveni M., Eyal H., Cohen Y. (1980): Development of resistance to metalaxyl in Pseudoperonospora cubensis. Plant Disease, 64: 1108–1109.  https://doi.org/10.1094/PD-64-1108
 
Richards T.A., Talbot N.J. (2007): Plant parasitic Oomycetes such as Phytophthora species contain genes derived from three eukaryotic lineages. Plant Signaling & Behavior, 2: 112–114.
 
Richards T.A., Soanes D.M., Jones M.D.M., Vasieva O., Leonard G., Paszkiewicz K., Foster P.G., Hall N., Talbot N. J. (2011): Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the Oomycetes. Proceedings of the National Academy of Sciences, 108: 15258–15263.  https://doi.org/10.1073/pnas.1105100108
 
Rieger P.H., Liermann J.C., Opatz T., Anke H., Thines E. (2010): Caripyrin, a new inhibitor of infection-related morphogenesis in the rice blast fungus Magnaporthe oryzae. Journal of Antibiotics, 63: 285–289.  https://doi.org/10.1038/ja.2010.31
 
Russell P.E. (1995): Fungicide resistance: Occurrence and management. The Journal of Agricultural Science, 124: 317–323.  https://doi.org/10.1017/S0021859600073275
 
Rytkönen A., Lilja A., Vercauteren A., Sirkiä S., Parikka P., Soukainen M., Hantula J. (2012): Identity and potential pathogenicity of Phytophthora species found on symptomatic Rhododendron plants in a Finnish nursery. Canadian Journal of Plant Pathology, 34: 255–267.  https://doi.org/10.1080/07060661.2012.686455
 
Sanders P.L. (1984): Failure of metalaxyl to control Pythium blight on turfgrass in Pennsylvania. Plant Disease, 68: 776–777. https://doi.org/10.1094/PD-68-776
 
Schwinn F., Staub T. (1995): Phenylamides and other fungicides against Oomycetes. In: Lyr H. (ed.). Modern Selective fungicides. Jena, Gustav Fischer: 323–346.
 
Schwinn F., Staub T., Urech P. (1977): Die Bekämpfung Falscher Mehltau-Krankheiten mit einem neuen Wirkstoff aus der Gruppe der Acylalanine. In: 41. Deutsche Pflanzenschutz-Tagung, October 10–14, 1977, Münster: 145–146. German.
 
Shattock R.C. (1988): Studies on the inheritance of resistance to metalaxyl in Phytophthora infestans. Plant Pathology, 37: 4–11.  https://doi.org/10.1111/j.1365-3059.1988.tb02188.x
 
Shennan C., Muramoto J., Koike S., Baird G., Fennimore S., Samtani J., Bolda M., Dara S., Daugovish O., Lazarovits G., Butler D., Rosskopf E., Kokalis-Burelle N., Klonsky K., Mazzola M. (2018): Anaerobic soil disinfestation is an alternative to soil fumigation for control of some soilborne pathogens in strawberry production. Plant Pathology, 67: 51–66.  https://doi.org/10.1111/ppa.12721
 
Staub T., Sozzi D. (1984): Fungicide resistance. Plant Disease, 68: 1026–1031. https://doi.org/10.1094/PD-68-1026
 
Staub T.H., Dahmen H., Schwinn F.J. (1980): Einfluß von Ridomil auf die Entwicklung von Plasmopara viticola und Phytophthora infestans auf ihren Wirtspflanzen. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz, 87: 83–91. German.
 
Suzui T., Makino T., Ogoshi A. (1980): Phytophthora rot of strawberry caused by Phytophthora nicotianae var. parasitica in Shizuoka. Japanese Journal of Phytopathology, 46: 169–178. https://doi.org/10.3186/jjphytopath.46.169
 
Takeda F. (1999): Strawberry production in soilless culture systems. Acta Horticulturae, 481: 289–296.  https://doi.org/10.17660/ActaHortic.1999.481.31
 
Tao Y., Zeng F., Ho H., Wei J., Wu Y., Yang L., He Y. (2011): Pythium vexans causing stem rot of Dendrobium in Yunnan province, China. Journal of Phytopathology, 159: 255–259.  https://doi.org/10.1111/j.1439-0434.2010.01756.x
 
Taylor R.J., Salas B., Secor G.A., Rivera V., Gudmestad N.C. (2002): Sensitivity of North American isolates of Phytophthora erythroseptica and Pythium ultimum to mefenoxam (metalaxyl). Plant Disease, 86: 797–802.  https://doi.org/10.1094/PDIS.2002.86.7.797
 
Thomidis T. (2002): Persistence of the systemic activity of metalaxyl and fosetyl-Al applied as a soil drench or foliar spray to control Phytophthora crown rot of peach. Phytopathologia Mediterranea, 41: 28–32.
 
Timmer L.W., Graham J.H., Zitko S.E. (1998): Metalaxyl-resistant isolates of Phytophthora nicotianae: Occurrence, sensitivity, and competitive parasitic ability on citrus. Plant Disease, 82: 254–261. https://doi.org/10.1094/PDIS.1998.82.2.254
 
Titone P., Mocioni M., Garibaldi A., Gullino M.L. (2009): Fungicide failure to control Pythium blight on turf grass in Italy. Journal of Plant Diseases and Protection, 116: 55–59.  https://doi.org/10.1007/BF03356286
 
Toljamo A.R., Granlund L.J., Kokko H.I. (2017): DNA barcode identification and virulence testing of Phytophthora spp. and Pythium spp. isolated from soil of strawberry fields. Acta Horticulturae, 1156: 727–733.  https://doi.org/10.17660/ActaHortic.2017.1156.107
 
Tsao P.H. (1983): Factors affection isolation and quantitation of Phytophthora from soil. In: Erwin D.C., Bartnicki-Garcia S., Tsao P.H. (eds). Phytophthora: Its Biology, Taxonomy, Ecology and Pathology. St Paul, The American Phytopathological Society: 219–236.
 
Urech P.A., Staub T. (1985): The resistance strategy for acylalanine fungicides. EPPO Bulletin, 15: 539–543.  https://doi.org/10.1111/j.1365-2338.1985.tb00266.x
 
Urech P.A., Schwinn F., Staub T. (1977): CGA 48988, a novel fungicide for the control of late blight, downy mildews and related soil borne diseases. In: Proceedings of the British Crop Protection Conference, November 21–24, 1977, Brighton: 623–631.
 
Utkhede R.S., Gupta V.K. (1988): In vitro selection of strains of Phytophthora cactorum resistant to metalaxyl. Journal of Phytopathology, 122: 35–44.  https://doi.org/10.1111/j.1439-0434.1988.tb00988.x
 
Utkhede R.S., Smith E.M. (1993): Long-term effects of chemical and biological treatments on crown and root rot of apple trees caused by Phytophthora cactorum. Soil Biology and Biochemistry, 25: 383–386. https://doi.org/10.1016/0038-0717(93)90138-2
 
Uzuhashi S., Kakishima M., Tojo M. (2010): Phylogeny of the genus Pythium and description of new genera. Mycoscience, 51: 337–365.  https://doi.org/10.1007/S10267-010-0046-7
 
Van den Bosch F., Paveley N., van den Berg F., Hobbelen P., Oliver R. (2014): Mixtures as a fungicide resistance management tactic. Phytopathology, 104: 1264–1273.  https://doi.org/10.1094/PHYTO-04-14-0121-RVW
 
Van der Plaats-Niterink A.J. (1981): Monograph of the genus Pythium. Studies in Mycology, 21: 1–242.
 
Van Poucke K., Haegeman A., Goedefroit T., Focquet F., Leus L., Jung M.H., Nave C., Redondo M.A., Husson C., Kostov K., Lyubenova A., Christova P., Chandelier A., Slavov S., de Cock A.W.A.M., Bonants P., Werres S., Palau J.O., Marçais B., Jung T., Stenlid J., Ruttink T., Heungens K. (2021): Unravelling hybridization in Phytophthora using phylogenomics and genome size estimation. IMA Fungus, 12: 16. doi: 10.1186/s43008-021-00068-w https://doi.org/10.1186/s43008-021-00068-w
 
Villa F., Pitts B., Stewart P.S., Giussani B., Roncoroni S., Albanese D., Giordano C., Tunesi M., Cappitelli F. (2016): Efficacy of zosteric acid sodium salt on the yeast biofilm model Candida albicans. Microbial Ecology, 62: 584–598. https://doi.org/10.1007/s00248-011-9876-x
 
Villa F., Cappitelli F., Cortesi P., Kunova A. (2017): Fungal biofilms: Targets for the development of novel strategies in plant disease management. Frontiers in Microbiology, 8: 654. doi: 10.3389/fmicb.2017.00654 https://doi.org/10.3389/fmicb.2017.00654
 
Vincelli P. (2014): Some principles of fungicide resistance. Plant Pathology Extension, 1: 123–125.
 
Wagner S., Kaminski K., Werres S. (2007): Evaluation of fungicides for control of Phytophthora ramorum. In: Proceedings of the Sudden Oak Death Third Science Symposium, Santa Rosa, California, March 5–9, 2007: 481–482.
 
Wang M., Hua X., Zhang Q., Yang Y., Shi H., Wang M. (2014): Enantioselective degradation of metalaxyl in grape, tomato, and rice plants. Chirality, 27: 109–114.  https://doi.org/10.1002/chir.22397
 
Wang F., Zhou T., Zhu L., Wang X., Wang J., Wang J., Du Z., Li B. (2019): Effects of successive metalaxyl application on soil microorganisms and the residue dynamics. Ecological Indicators, 103: 194–201.  https://doi.org/10.1016/j.ecolind.2019.04.018
 
Wang W., Liu X., Han T., Li K., Qu Y., Gao Z. (2020): Differential potential of Phytophthora capsici resistance mechanisms to the fungicide metalaxyl in peppers. Microorganisms, 8: 278. doi: 10.3390/microorganisms8020278 https://doi.org/10.3390/microorganisms8020278
 
Wang W., Liu D., Zhuo X., Wang Y., Song Z., Chen F., Pan Y., Gao Z. (2021): The RPA190-pc gene participates in the regulation of metalaxyl sensitivity, pathogenicity and growth in Phytophthora capsici. Gene, 764: 145081. doi: 10.1016/j.gene.2020.145081 https://doi.org/10.1016/j.gene.2020.145081
 
Watanabe T. (1977): Pathogenicity of Pythium myriotylum isolated from strawberry roots in Japan. Japanese Journal of Phytopathology, 43: 306–309.  https://doi.org/10.3186/jjphytopath.43.306
 
Watanabe T., Hashimoto K., Sato M. (1977): Pythium species associated with strawberry roots in Japan, and their role in strawberry stunt dissease. Phytopathology, 67: 1324–1332. https://doi.org/10.1094/Phyto-67-1324
 
White J., Stanghellini M., Ayoubi L. (1988): Variation in the sensitivity to metalaxyl of Pythium spp. isolated from carrot and other sources. Annals of Applied Biology, 113: 269–277.  https://doi.org/10.1111/j.1744-7348.1988.tb03303.x
 
White T.J., Bruns T., Lee S., Taylor J. (1990): Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M.A., Gelfand D.H., Sninsky J.J., White T.J. (eds). PCR Protocols: A Guide to Methods and Applications. New York, NY, Academic Press: 315–322.
 
Wollgiehn R., Bräutigam E., Schumann B., Erge D. (1984): Wirkung von Metalaxyl auf die Synthese von RNA, DNA und Protein in Phytophthora nicotianae. Zeitschrift für Allgemeine Mikrobiologie, 24: 269–279. German. https://doi.org/10.1002/jobm.19840240417
 
Zadra C., Marucchini C., Zazzerini A. (2002): Behavior of metalaxyl and its pure R-enantiomer in sunflower plants (Helianthus annus). Journal of Agricultural and Food Chemistry, 50: 5373–5377. https://doi.org/10.1021/jf020310w
 
download PDF

© 2022 Czech Academy of Agricultural Sciences | Prohlášení o přístupnosti