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Oomycete Fungicides: Phenylamides, Quinone Outside Inhibitors, and Carboxylic Acid Amides

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Fungicide Resistance in Plant Pathogens

Abstract

Oomycetes are “fungal-like” protista that are phylogenetically distinct from fungi, they are diploid, and cell walls contain cellulose. Oomycetes comprise major plant pathogens within the orders Saprolegniales, Pythiales, Peronosporales (“downy mildews” including species of Plasmopara, Phytophthora, Peronospora, Pseudoperonospora, Bremia), and Sclerosporales. Control of oomycete diseases relies mainly on chemical measures using products within 16 different chemical groups, among which the phenylamides (PAs), quinone outside inhibitors (QoIs), carboxylic acid amides (CAAs), and multisite inhibitors are most widely used. However, resistance evolved against most single-site inhibitors in many oomycete pathogen species. Resistance against PAs (inhibitors of RNA polymerase I) was detected in most oomycete pathogen species; the molecular mechanism was associated recently with the presence of the Y382F mutation in the RNApolI gene. QoIs inhibit electron transport in complex III of the respiration chain; two major mutations, G143A (in Plasmopara viticola) and F129L (in Pythium spp.), have been identified in the cytochrome b, cyt b gene coding for resistance. However, no resistant isolates were observed in Phytophthora species. CAAs inhibit cellulose synthase; several mutations, G1105S/V (in P. viticola) and G1105V/W (in Pseudoperonospora cubensis), were detected in the cellulose synthase, CesA3 gene of CAA-resistant field isolates. In Phytophthora infestans and P. capsici, no CAA-resistant field isolates were discovered, whereas in artificial mutants, the mutations G1105A/V and V1109L/M were found. The L1109 and M1109 amino acid configurations are responsible for the intrinsic insensitivity to CAAs of the entire genus Pythium and all oomycetes outside Peronosporales. Resistance is inherited by one recessive nuclear gene (CesA3) for CAAs, one maternal mitochondrial gene (cytb) for QoIs, and mainly one semidominant nuclear gene for PAs. The consequences of the molecular mechanisms for evolution and stability of resistance are discussed in the light of oomycete pathogen biology.

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References

  • Abu-El Samen FM, Oberoi K, Taylor RJ, Secor GA, Gudmestad NC (2005) Inheritance of mefenoxam resistance in selfed populations of the homothallic oomycete Phytophthora erythroseptica (Pethybr.), cause of pink rot of potato. Am J Potato Res 82:105–115

    Article  Google Scholar 

  • Bhat RG, McBlain BA, Schmitthenner AF (1993) The inheritance of resistance to metalaxyl and to fluorophenylalanine in matings of homothallic Phytophthora sojae. Mycol Res 97:865–870

    Article  CAS  Google Scholar 

  • Blum M, Gisi U (2008) Inheritance of fungicide resistance in Plasmopara viticola. In: Dehne HW, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds V, Proceedings 15th international Reinhardsbrunn symposium. DPG Selbstverlag, Braunschweig, pp 101–104

    Google Scholar 

  • Blum M, Gisi U (2012) Insights into the molecular mechanism of tolerance to Carboxylic Acid Amide (CAA) fungicides in Pythium aphanidermatum. Pest Manag Sci 68:1171–1183

    Article  CAS  PubMed  Google Scholar 

  • Blum M, Boehler M, Randall E, Young V, Csukai M, Kraus S, Moulin F, Scalliet G, Avrova AO, Whisson SC, Fonné-Pfister R (2010a) Mandipropamid targets the cellulose synthase-like PiCesA3 to inhibit cell wall biosynthesis in the oomycete plant pathogen Phytophthora infestans. Mol Plant Pathol 11:227–243

    Article  CAS  PubMed  Google Scholar 

  • Blum M, Waldner M, Gisi U (2010b) A single point mutation in the novel PvCesA3 gene confers resistance to the carboxylic acid amide fungicide mandipropamid in Plasmopara viticola. Fungal Genet Biol 47:499–510

    Article  CAS  PubMed  Google Scholar 

  • Blum M, Waldner M, Olaya G, Cohen Y, Gisi U, Sierotzki H (2011) Resistance mechanism to carboxylic acid amide (CAA) fungicides in the cucurbit downy mildew pathogen Pseudoperonospora cubensis. Pest Manag Sci 67:1211–1214

    Article  CAS  PubMed  Google Scholar 

  • Blum M, Gamper HA, Waldner M, Sierotzki H, Gisi U (2012) The cellulose synthase 3 (CesA3) gene of oomycetes: structure phylogeny and influence on sensitivity to carboxylic acid amide (CAA) fungicides. Fungal Biol 116:529–542

    Article  CAS  PubMed  Google Scholar 

  • Bosshard E, Schüepp H (1983) Variability of selected strains of Plasmopara viticola with respect to their metalaxyl sensitivity under field conditions. Z Pflkrank Pflschutz 90:449–459 (in German)

    Google Scholar 

  • Brasseur G, Saribas AS, Daldal F (1996) A compilation of mutations located in the cytochrome b subunit of the bacterial and mitochondrial bc1 complex. Biochim Biophys Acta 1275:61–69

    Article  PubMed  Google Scholar 

  • Brown S, Koike ST, Ochoa OE, Laemmlen F, Michelmore RW (2004) Insensitivity to the fungicide fosetyl-aluminium in California isolates of the lettuce downy mildew pathogen Bremia lactucae. Plant Dis 88:502–508

    Article  CAS  Google Scholar 

  • Café-Filho AC, Ristaino JB (2008) Fitness of isolates of Phytophthora capsici resistant to mefenoxam from squash and pepper fields in North Carolina. Plant Dis 92:1439–1443

    Article  CAS  Google Scholar 

  • Catal M, King L, Tumbalam P, Wiriyajitsomboon P, Kirk WW, Adams GC (2010) Heterokaryotic nuclear conditions and a heterogeneous nuclear population are observed by flow cytometry in Phytophthora infestans. Cytometry Part A 77A:769–775

    Article  CAS  Google Scholar 

  • Chabane K, Leroux P, Maia N, Bompeix G (1996) Resistance to dimethomorph in laboratory mutants of Phytophthora parasitica. In: Lyr H, Russell PE, Sisler HD, Lyr H (eds) Modern fungicides and antifungal compounds I, Proceedings 11th international Reinhardsbrunn symposium. Intercept, Andover, pp 387–391

    Google Scholar 

  • Chapara V, Taylor RJ, Pasche JS, Gudmestad NC (2010) Prevalence of mefenoxam resistance among Phytophthora erythroseptica (Pethybridge) isolates in Minnesota and North Dakota. Am J Potato Res 87:521–530

    Article  CAS  Google Scholar 

  • Chapara V, Taylor RJ, Pasche J, Gudmestad NC (2011) Competitive parasitic fitness of mefenoxam-sensitive and -resistant isolates of Phytophthora erythroseptica under fungicide selection pressure. Plant Dis 95:691–696

    Article  CAS  Google Scholar 

  • Chen L, Wang Q, Lu X, Zhu S, Liu X (2011) Semidominant mutations in CesA3 leading to resistance to CAA fungicides in Phytophthora capsici. Phytopathology 101:S34 (abstract)

    Article  CAS  Google Scholar 

  • Chen L, Zhu S, Lu X, Pang Z, Cai M, Liu X (2012) Assessing the risk that Phytophthora melonis can develop a point mutation (V1109L) in CesA3 conferring resistance to carboxylic acid amide fungicides. PLoS ONE 7(7), e42069. doi:10.1371/journal.pone.0042069

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cohen Y, Rubin E, Hadad T, Gotlieb D, Sierotzki H, Gisi U (2007) Sensitivity of Phytophthora infestans to mandipropamid and the effect of enforced selection pressure in the field. Plant Pathol 56:836–842

    Article  CAS  Google Scholar 

  • Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR, Etherington GJ, Deahl KL, Farrer RA, Gilroy EM, Goss EM, Grünwald NJ, Hein I, MacLean D, McNicol JW, Randall E, Oliva RF, Pel MA, Shaw DS, Squires JN, Taylor MC, Vleeshouwers VGAA, Birch PRJ, Lees AK, Kamoun S (2012) Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathog 8(10), e1002940. doi:10.1371/journal.ppat.1002940

    Article  PubMed Central  PubMed  Google Scholar 

  • Corio-Costet MF, Martinez F, Delmotte F, Douence L, Richart-Cervera S, Chen WJ (2008) Resistance of Plasmopara viticola to QoI fungicides: origin and diversity. In: Dehne HW, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds V, Proceedings 15th international Reinhardsbrunn symposium. DPG Selbstverlag, Braunschweig, pp 107–112

    Google Scholar 

  • Crute IR, Harrison JM (1988) Studies on the inheritance of resistance to metalaxyl in Bremia lactucae and on the stability and fitness of field isolates. Plant Pathol 37:231–250

    Article  CAS  Google Scholar 

  • Crute IR, Gordon PL, Moss NA (1994) Variation for response to phenylamides in UK populations of Bremia lactucae (lettuce downy mildew) and Peronospora parasitica (brassica downy mildew). In: Heaney S, Slawson D, Hollomon DW, Smith M, Russell PE, Parry DW (eds) Fungicide resistance. British Crop Protection Council, Surrey, pp 155–162

    Google Scholar 

  • Csinos AS, Bertrand PF (1994) Distribution of Phytophthora parasitica var. nicotianae races and their sensitivity to metalaxyl in Georgia. Plant Dis 78:471–474

    Article  CAS  Google Scholar 

  • Dagget SS, Goetz E, Therrien CD (1993) Phenotypic changes in populations of Phytophthora infestans from eastern Germany. Phytopathology 83:319–323

    Article  Google Scholar 

  • Davidse LC (1988) Phenylamide fungicides: mechanism of action and resistance. In: Delp CJ (ed) Fungicide resistance in North America. APS Press, St Paul, pp 63–65

    Google Scholar 

  • Davidse LC (1995) Phenylamide fungicides: biochemical action and resistance. In: Lyr H (ed) Modern selective fungicides, 2nd edn. Gustav Fischer, Jena, pp 347–354

    Google Scholar 

  • Degli-Esposti M, De Fries S, Crimi M, Ghelli A, Patarnello T, Meyer A (1993) Mitochondrial cytochrome b: evolution and structure of the protein. Biochim Biophys Acta 1143:243–271

    Article  CAS  Google Scholar 

  • Di Rago JP, Coppée JY, Colson AM (1989) Molecular basis for resistance to myxothiazol, mucidin (strobilurin A) and stigmatellin. J Biol Chem 264:14543–14548

    PubMed  Google Scholar 

  • Dunn AR, Milgroom MG, Meitz JC, McLeod A, Fry WE, McGrath MT, Dillard HR, Smart CD (2010) Population structure and resistance to mefenoxam of Phytophthora capsici in New York State. Plant Dis 94:1461–1468

    Article  Google Scholar 

  • Fabritius AL, Shattock RC, Judelson HS (1997) Genetic analysis of metalaxyl insensitivity loci in Phytophthora infestans using linked DNA markers. Phytopathology 87:1034–1040

    Article  CAS  PubMed  Google Scholar 

  • Falloon RE, Follas GB, Butler RC, Goulden DS (2000) Resistance in Peronospora viciae to phenylamide fungicides: reduced efficacy of seed treatments of pea (Pisum sativum) and assessment of alternatives. Crop Prot 19:313–325

    Article  CAS  Google Scholar 

  • Fisher DJ, Hayes AL (1982) Mode of action of the fungicides furalaxyl, metalaxyl and ofurace. Pestic Sci 13:330–339

    Article  CAS  Google Scholar 

  • FRAC (2014) Several documents on www.frac.info

  • French-Monar RD, Jones JB, Roberts PD (2006) Characterization of Phytophthora capsici associated with roots of weeds on Florida vegetable farms. Plant Dis 90:345–350

    Article  CAS  Google Scholar 

  • Fry WE, Goodwin SB, Dyer AT, Matuszak JM, Drenth A, Tooley PW, Sujkowski LS, Koh YJ, Cohen BA, Spielman LJ, Deahl KL, Inglis DA, Sandlan KP (1993) Historical and recent migrations of Phytophthora infestans: chronology, pathways, and implications. Plant Dis 84:731–735

    Google Scholar 

  • Gallup CA, Ivors KL, Greene MD, Lannon KR, Shew HD (2009) Population structure of Phytophthora nicotianae, the causal agent of black shank, in North Carolina tobacco fields. North Carolina State University, Raleigh

    Google Scholar 

  • Geier BM, Schägger H, Brandt U, Colson AM, von Jagow G (1992) Point mutation in cytochrome b of yeast ubihydroquinone-cytochrome-oxidoreductase causing myxothiazol resistance and facilitated dissociation of the iron-sulfur subunit. Eur J Biochem 208:375–380

    Article  CAS  PubMed  Google Scholar 

  • Gisi U (2002) Chemical control of downy mildews. In: Spencer PTN, Gisi U, Lebeda A (eds) Advances in downy mildew research. Kluwer Academic Publishers, Dordrecht, pp 119–159

    Chapter  Google Scholar 

  • Gisi U (2014) Assessment of selection and resistance risk for DMI fungicides in Aspergillus fumigatus in agriculture and medicine: a critical review. Pest Manag Sci 70:352–364

    Article  CAS  PubMed  Google Scholar 

  • Gisi U, Cohen Y (1996) Resistance to phenylamide fungicides: a case study with Phytophthora infestans involving mating type and race structure. Annu Rev Phytopathol 34:549–572

    Article  CAS  PubMed  Google Scholar 

  • Gisi U, Sierotzki H (2008) Fungicide mode of action and resistance in downy mildews. Eur J Plant Pathol 122:157–167

    Article  CAS  Google Scholar 

  • Gisi U, Sierotzki H, Cook A, Mc Caffery A (2002) Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides, Pest Manag Sci 58:859-867

    Google Scholar 

  • Gisi U, Waldner M, Kraus N, Dubuis PH, Sierotzki H (2007) Inheritance of resistance to carboxylic acid amide (CAA) fungicides in Plasmopara viticola. Plant Pathol 56:199–208

    Article  CAS  Google Scholar 

  • Gisi U, Walder F, Resheat-Eini Z, Edel D, Sierotzki H (2011) Change of genotype, sensitivity and aggressiveness in Phytophthora infestans isolates collected in European countries in 1997, 2006 and 2007. J Phytopathol 159:223–232

    Article  Google Scholar 

  • Gisi U, Lamberth C, Mehl A, Seitz T (2012) Carboxylic Acid Amide (CAA) fungicides. In: Krämer W, Schirmer U, Jeschke P, Witschel M (eds) Modern crop protection compounds, 2nd edn. Wiley-VCH, Weinheim, pp 807–830

    Chapter  Google Scholar 

  • Goodwin SB, Smart CD, Sandrock RW, Deahl KL, Punja ZK, Fry WE (1998) Genetic change within populations of Phytophthora infestans in the United States and Canada during 1994 to 1996: role of migration and recombination. Phytopathology 85:478–479

    Google Scholar 

  • Grasso V, Palermo S, Sierotzki H, Garibaldi A, Gisi U (2006) Cytochrome b gene structure and consequences for resistance to QoI fungicides in plant pathogens. Pest Manag Sci 62:465–472

    Article  CAS  PubMed  Google Scholar 

  • Grönberg L, Andersson B, Yuen J (2012) Can weed hosts increase aggressiveness of Phytophthora infestans on potato? Phytopathology 102:429–433

    Article  PubMed  Google Scholar 

  • Gullino ML, Gilardi G, Tinivella F, Garibaldi A (2004) Observations on the behaviour of different populations of Plasmopara viticola resistant to QoI fungicides in Italian vineyards. Phytopathol Medit 43:341–350

    CAS  Google Scholar 

  • Hamed BH, Gisi U (2013) Generation of pathogenic F1 progeny from crosses of Phytophthora infestans isolates differing in ploidy. Plant Pathol 62:708–718

    Article  CAS  Google Scholar 

  • Heaney SP, Hall AA, Davies SA, Olaya G (2000) Resistance to fungicides in the QoI-STAR cross-resistance group: current perspectives. Proc Brighton Crop Protect Conf 2:755–762

    Google Scholar 

  • Hermann D, Gisi U (2012) Fungicide resistance in Oomycetes with special reference to Phytophthora infestans and phenylamides. In: Thind TS (ed) Fungicide resistance in crop protection. CAB International, Oxfordshire, pp 133–140

    Chapter  Google Scholar 

  • Hermann D, McKenzie D, Cohen Y, Gisi U (2015) Phenylamides: market trends and resistance evolution for important Oomycete pathogens 35 years after the first product introduction. In: Stevenson KL, Wyenandt CA, McGrath ML (eds) Fungicide resistance development in North America. APS Press, St. Paul (in press)

    Google Scholar 

  • Hu J, Hong C, Stromberg EL, Moorman GW (2010) Mefenoxam sensitivity in Phytophthora cinnamomi isolates. Plant Dis 94:39–44

    Article  CAS  Google Scholar 

  • Hu CH, Perez FG, Donahoo R, McLeod A, Myers K, Ivors K, Secor G, Roberts PD, Deahl KL, Fry WE, Ristaino JB (2012) Recent genotypes of Phytophthora infestans in the Eastern United States reveal clonal populations and reappearance of mefenoxam sensitivity. Plant Dis 96:1323–1330

    Article  Google Scholar 

  • Ishii H, Fraaije BA, Sugiyama T, Noguchi K, Nishimura K, Takeda T, Amano T, Hollomon DW (2001) Occurrence and molecular characterization of strobilurin resistance in cucumber powdery mildew and downy mildew. Phytopathology 91:1166–1171

    Article  CAS  PubMed  Google Scholar 

  • Ishii H, Sugiyama T, Nishimura K, Ishikawa Y (2002) Strobilurin resistance in cucumber pathogens: persistence and molecular diagnosis of resistance. In: Dehne HW, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds III, Proceedings 13th international Reinhardsbrunn symposium. Agro Concept, Bonn, pp 149–159

    Google Scholar 

  • Judelson HS (1997) Expression and inheritance of sexual preference and selfing propensity in Phytophthora infestans. Fungal Genet Biol 21:188–197

    Article  Google Scholar 

  • Judelson HS, Roberts S (1999) Multiple loci determining insensitivity to phenylamide fungicides on Phytophthora infestans. Phytopathology 89:754–760

    Article  CAS  PubMed  Google Scholar 

  • Kadish D, Cohen Y (1992) Overseasoning of metalaxyl-sensitive and metalaxyl-resistant isolates of Phytophthora infestans in potato tubers. Phytopathology 82:887–889

    Article  CAS  Google Scholar 

  • Kadish D, Grinberger M, Cohen Y (1990) Fitness of metalaxyl-sensitive and metalaxyl-resistant isolates of Phytophthora infestans on susceptible and resistant potato cultivars. Phytopathology 80:200–205

    Article  Google Scholar 

  • Keinath AP (2007) Sensitivity of populations of Phytophthora capsici from South Carolina to mefenoxam, dimethomorph, zoxamide, and cymoxanil. Plant Dis 91:743–748

    Article  CAS  Google Scholar 

  • Kuck KH, Leadbeater AJ, Gisi U (2012) FRAC mode of action classification and resistance risk of fungicides. In: Krämer W, Schirmer U, Jeschke P, Witschel M (eds) Modern crop protection compounds, 2nd edn. Wiley-VCH, Weinheim, pp 539–557

    Chapter  Google Scholar 

  • Lamour KH, Hausbeck MK (2000) Mefenoxam insensitivity and the sexual stage of Phytophthora capsici in Michigan cucurbit fields. Phytopathology 90:396–400

    Article  CAS  PubMed  Google Scholar 

  • Lebeda A, Cohen Y (2012) Fungicide resistance in Pseudoperonospora cubensis, the causal pathogen of cucurbit downy mildew. In: Thind TS (ed) Fungicide resistance in crop protection: risk and management. CABI, Wallingford, pp 44–63

    Chapter  Google Scholar 

  • Lebreton L, Lucas JM, Andrivon D (1999) Aggressiveness and competitive fitness of Phytophthora infestans isolates collected from potato and tomato in France. Phytopathology 89:679–686

    Article  CAS  PubMed  Google Scholar 

  • Lees AK, Wattier R, Shaw DS, Sullivan L, Williams NA, Cooke DEL (2006) Novel microsatellite markers for the analysis of Phytophthora infestans populations. Plant Pathol 55:311–319

    Article  CAS  Google Scholar 

  • Li Y, Cooke DEL, Jacobsen E, van der Lee T (2013) Efficient multiplex simple sequence repeat genotyping of the oomycete plant pathogen Phytophthora infestans. J Microbiol Methods 92:316–322

    Article  CAS  PubMed  Google Scholar 

  • Lu XH, Hausbeck MK, Liu XL, Hao JJ (2011) Wild type sensitivity and mutation analysis for resistance risk to fluopicolide in Phytophthora capsici. Plant Dis 95:1535–1541

    Article  Google Scholar 

  • Lu XH, Davis RM, Livingston S, Nunez J, Hao J (2012) Fungicide sensitivity of Pythium spp. associated with cavity spot of carrot in California and Michigan. Plant Dis 96:384–388

    Article  CAS  Google Scholar 

  • Lucas JA, Greer G, Oudemans PV, Coffey MD (1990) Fungicide sensitivity in somatic hybrids of Phytophthora capsici by protoplast fusion. Physiol Mol Plant Pathol 36:175–187

    Article  CAS  Google Scholar 

  • McGrath MT (2012) Challenge of fungicide resistance and anti-resistance strategies in managing vegetable diseases in the USA. In: Thind ST (ed) Fungicide resistance in crop protection: risk and management. CABI, Wallingford, pp 191–207

    Chapter  Google Scholar 

  • Montarry J, Corbiere R, Andrivon D (2007) Is there a trade-off between aggressiveness and overwinter survival in Phytophthora infestans? Funct Ecol 21:603–610

    Article  Google Scholar 

  • Moorman GW, Kang S, Geiser DM, Kim SH (2002) Identification and characterization of Pythium species associated with greenhouse floral crops in Pennsylvania. Plant Dis 86:1227–1231

    Article  Google Scholar 

  • Müller U, Gisi U (2012) Newest aspects of nucleic acid synthesis inhibitors: metalaxyl-M. In: Krämer W, Schirmer U, Jeschke P, Witschel M (eds) Modern crop protection compounds, 2nd edn. Wiley-VCH, Weinheim, pp 901–908

    Chapter  Google Scholar 

  • Olaya G, Cleere S, Stanger C, Burbidge J, Hall A, Windass J (2003) A novel potential target site and QoI fungicide resistance mechanism in Pythium aphanidermatum. Phytopathology 93(6) Supplement: S67 (abstract)

    Google Scholar 

  • Pang Z, Shao J, Chen L, Lu X, Hu J, Qin Z, Liu X (2013) Resistance to the novel fungicide pyrimorph in Phytophthora capsici: risk assessment and detection of point mutations in CesA3 that confer resistance. PLoS ONE 8(2), e56513. doi:10.1371/journal.pone.0056513

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Parkunan V, Johnson CS, Bowman BC, Hong CX (2010) Population structure, mating type, and mefenoxam sensitivity of Phytophthora nicotianae in Virginia tobacco fields. Plant Dis 94:1361–1365

    Article  Google Scholar 

  • Parra G, Ristaino JB (2001) Resistance to mefenoxam and metalaxyl among field isolates of Phytophthora capsici causing Phytophthora blight of bell pepper. Plant Dis 85:1069–1075

    Article  CAS  Google Scholar 

  • Phillips McDougall (2012) AgriReference reports, release 6.0, product directory V13, www.phillipsmcdougall.com

  • Porter LD, Miller JS, Nolte P, Price WJ (2007) In vitro somatic growth and reproduction of phenylamide-resistant and -sensitive isolates of Phytophthora erythroseptica from infected potato tubers in Idaho. Plant Pathol 56:492–499

    Article  CAS  Google Scholar 

  • Randall E, Young V, Sierotzki H, Scalliet G, Birch PRJ, Cooke DEL, Csukai M, Whisson SC (2014) Sequence diversity in the large subunit of RNA polymerase I contributes to mefenoxam insensitivity in Phytophthora infestans. Mol Plant Pathol. doi:10.1111/mpp.12124

    PubMed  Google Scholar 

  • Reuveni M, Eyal H, Cohen Y (1980) Development of resistance to metalaxyl in Pseudoperonospora cubensis. Plant Dis 64:1108–1109

    Article  Google Scholar 

  • Rubin A(E), Gotlieb D, Gisi U, Cohen Y (2008) Mutagenesis of Phytophthora infestans for resistance against carboxylic acid amide and phenylamide fungicides. Plant Dis 92:675–683

    Article  CAS  Google Scholar 

  • Scherer E, Gisi U (2006) Characterization of genotype and mating type in European isolates of Plasmopara viticola. J Phytopathol 154:489–495

    Article  CAS  Google Scholar 

  • Schwinn F, Staub T (1995) Oomycete fungicides: phenylamides and other fungicides against Oomycetes. In: Lyr H (ed) Modern selective fungicides, 2nd edn. Gustav Fischer, Jena, pp 323–346

    Google Scholar 

  • Shattock RC (1986) Inheritance of metalaxyl resistance in the potato late blight fungus. In: Proceedings Brighton crop protection conference, vol 2. British Crop Protection Council, Thornton Heath, Surrey, pp 555–560

    Google Scholar 

  • Shattock RC (1988) Studies on inheritance of resistance to metalaxyl in Phytophthora infestans. Plant Pathol 37:4–11

    Article  CAS  Google Scholar 

  • Shaw DS, Shattock RC (1991) Genetics of Phytophthora infestans: the Mendelian approach. In: Lucas JA, Shattock RC, Shaw DS, Cooke LR (eds) Phytophthora. Cambridge University Press, Cambridge, UK, pp 218–230

    Google Scholar 

  • Sierotzki H, Parisi S, Steinfeld U, Tenzer I, Poirey S, Gisi U (2000a) Mode of resistance to respiration inhibitors at the cytochrome bc1 enzyme complex of Mycosphaerella fijiensis field isolates. Pest Manag Sci 56:833–841

    Article  CAS  Google Scholar 

  • Sierotzki H, Wullschleger J, Gisi U (2000b) Point-mutation in cytochrome b gene conferring resistance to strobilurin fungicides in Erysiphe graminis f.sp. tritici field isolates. Pestic Biochem Physiol 68:107–112

    Article  CAS  Google Scholar 

  • Sierotzki H, Kraus N, Assemat P, Stanger C, Cleere S, Windass J, Gisi U (2005) Evolution of resistance to QoI fungicides in Plasmopara viticola populations in Europe. In: Dehne HW, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds IV, Proceedings 14th international Reinhardsbrunn symposium. BCPC, Alton, pp 73–80

    Google Scholar 

  • Sierotzki H, Kraus N, Pepin S, Fernandes N, Gisi U (2008) Dynamics of QoI resistance in Plasmopara viticola. In: Dehne HW, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds V, Proceedings 15th international Reinhardsbrunn symposium. DPG Selbstverlag, Braunschweig, pp 151–157

    Google Scholar 

  • Sierotzki H, Blum M, Olaya G, Waldner-Zulauf M, Wullschleger J, Cohen Y, Gisi U (2011) Sensitivity to CAA fungicides and frequency of mutations in cellulose synthase (CesA3) gene of oomycete pathogen populations. In: Dehne HW, Deising HB, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds VI, Proceedings 16th international Reinhardsbrunn symposium. DPG Selbstverlag, Braunschweig, pp 103–110

    Google Scholar 

  • Staub T (1994) Early experiences with phenylamide resistance and lessons for continued successful use. In: Heaney S, Slawson D, Hollomon DW, Smith M, Russell PE, Parry DW (eds) Fungicide resistance. British Crop Protection Council, Farnham, pp 131–138

    Google Scholar 

  • Staub T, Sozzi D (1981) Résistance au métalaxyl en pratique et les consequences pour son utilisation. Phytiatr Phytopharm 30:283–291 (in French)

    Google Scholar 

  • Takeda T, Kawagoe Y, Uchida K, Fuji M, Amano T (1999) The appearance of resistant isolates to strobilurins. Ann Phytopathol Soc Jpn 65:655 (Japanese abstract)

    Google Scholar 

  • Taylor RJ, Salas B, Secor GA, Rivera V, Gudmestad NC (2002) Sensitivity of North American isolates of Phytophthora erythroseptica and Pythium ultimum to mefenoxam (metalaxyl). Plant Dis 86:797–802

    Article  CAS  Google Scholar 

  • Taylor RJ, Pasche JS, Gudmestad NC (2006) Biological significance of mefenoxam resistance in Phytophthora erythroseptica and its implications for the management of pink rot of potato. Plant Dis 90:927–934

    Article  CAS  Google Scholar 

  • Taylor RJ, Pasche JS, Gudmestad NC (2011) Effect of application method and rate on residual efficacy of mefenoxam and phosphorous acid fungicides in the control of pink rot of potato. Plant Dis 95:997–1006

    Article  CAS  Google Scholar 

  • Toffolatti SL, Vercesi A (2012) QoI resistance in Plasmopara viticola in Italy: evolution and management strategies. In: Thind TS (ed) Fungicide resistance in crop protection. CAB International, Oxfordshire, pp 172–183

    Chapter  Google Scholar 

  • Toffolatti SL, Serrati L, Sierotzki H, Gisi U, Vercesi A (2007) Assessment of QoI resistance in Plasmopara viticola oospores. Pest Manag Sci 63:194–201

    Article  CAS  PubMed  Google Scholar 

  • Toffolatti SL, Serrati L, Vercesi A (2011) CAA, phenylamide and QoI resistance assessment in Plasmopara viticola oospores. In: Dehne HW, Deising HB, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds VI, Proceedings 16th international Reinhardsbrunn symposium. DPG Selbstverlag, Braunschweig, pp 267–272

    Google Scholar 

  • Whisson SC, Fonné-Pfister R, Csukai M (2011) Molecular approaches to elucidate pathways and sites of fungicide resistance in Oomycetes. In: Dehne HW, Deising HB, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds VI, Proceedings 16th international Reinhardsbrunn symposium. DPG Selbstverlag, Braunschweig, pp 91–102

    Google Scholar 

  • Wicks TG, Hall B, Pezzanati P (1994) Fungicidal control of metalaxyl-insensitive strains of Bremia lactucae on lettuce. Crop Prot 13:617–624

    Article  CAS  Google Scholar 

  • Widmark AK, Andersson B, Cassel-Lundhagen A, Sandström M, Yuen JE (2007) Phytophthora infestans in a single field in southwest Sweden early in spring: symptoms, spatial distribution and genotypic variation. Plant Pathol 56:573–579

    Article  CAS  Google Scholar 

  • Yuen JE, Andersson B (2013) What is the evidence for sexual reproduction of Phytophthora infestans in Europe? Plant Pathol 62:485–491

    Article  Google Scholar 

  • Zhu SS, Liu XL, Wang Y, Wu XH, Liu PF, Li JQ, Yuan SK, Si NG (2007) Resistance of Pseudoperonospora cubensis to flumorph on cucumber in plastic houses. Plant Pathol 56:967–975

    Article  CAS  Google Scholar 

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Correspondence to Ulrich Gisi .

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Gisi, U., Sierotzki, H. (2015). Oomycete Fungicides: Phenylamides, Quinone Outside Inhibitors, and Carboxylic Acid Amides. In: Ishii, H., Hollomon, D. (eds) Fungicide Resistance in Plant Pathogens. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55642-8_10

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