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Histidine Kinase Inhibitors

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Fungicide Resistance in Plant Pathogens

Abstract

Dicarboximides and phenylpyrroles have been mainly used to control diseases caused by fungal strains that belong to the genera Botrytis, Sclerotinia, Monilinia, and Alternaria. Both types of fungicides overactivate Hog-like mitogen-activated protein kinases in the osmotic signal transduction pathway and result in cell death. Cross-resistance among dicarboximides, phenylpyrroles, and aromatic hydrocarbons has been observed in most laboratory Botrytis cinerea-resistant mutants, which are generally hyperosmotic sensitive. However, such resistant strains have rarely been isolated from the fields. All dicarboximide-resistant field isolates contained point mutations in a putative osmosensor histidine kinase BcOS1/Daf1, did not show cross-resistance to phenylpyrroles, and were insensitive to osmotic stress. In contrast, Alternaria field-resistant strains carried various mutations, including null mutations, in their osmosensor histidine kinase genes. The introduction of several new fungicides against B. cinerea, such as anilinopyrimidine fungicides, fenhexamid, QoIs, and succinate dehydrogenase inhibitors, reduced the use of dicarboximides, thereby reducing the populations of dicarboximide-resistant strains. However, several types of multidrug resistance strains, in which efflux pumps are activated, have emerged. Gain-of-function mutations of the transcription factor Mrr1, which leads to an overexpression of the ATP-binding cassette transporter AtrB, confers reduced sensitivities to some fungicides, including fludioxonil and cyprodinil. In addition, strains that overexpress the major facilitator superfamily transporter mfsM2 by promoter rearrangements lead to reduced sensitivities to iprodione, fenhexamid, and cyprodinil. Therefore, in addition to target modifications of BcOS1, multidrug resistance caused by the overexpression of drug transporters is another resistance mechanism in B. cinerea against dicarboximides and phenylpyrroles.

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References

  • Abe K, Furukawa K, Fujioka T, Hagiwara D, Maeda H, Marui J, Mizutani O, Takahashi T, Yoshimi A, Yamagata Y, Gomi K, Hasegawa F (2009) Novel industrial applications of Aspergillus oryzae genomics. In: Machida M, Gomi K (eds) Aspergillus: molecular biology and genomics. Caister Academic Press, Washington, DC, pp 199–227

    Google Scholar 

  • Alberoni G, Collina M, Pancaldi D, Brunelli A (2005) Resistance to dicarboximide fungicides in Stemphylium vesicarium of Italian pear orchards. Eur J Plant Pathol 113(2):211–219

    Article  CAS  Google Scholar 

  • Alberoni G, Collina M, Lanen C, Leroux P, Brunelli A (2010) Field strains of Stemphylium vesicarium with a resistance to dicarboximide fungicides correlated with changes in a two-component histidine kinase. Eur J Plant Pathol 128:171–184

    Article  CAS  Google Scholar 

  • Alex LA, Borkovich KA, Simon MI (1996) Hyphal development in Neurospora crassa: involvement of a two-component histidine kinase. Proc Natl Acad Sci U S A 93(8):3416–3421

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Avenot H, Simoneau P, Iacomi-Vasilescu B, Bataille-Simoneau N (2005) Characterization of mutations in the two-component histidine kinase gene AbNIK1 from Alternaria brassicicola that confer high dicarboximide and phenylpyrrole resistance. Curr Genet 47(4):234–243

    Article  CAS  PubMed  Google Scholar 

  • Banno S, Noguchi R, Yamashita K, Fukumori F, Kimura M, Yamaguchi I, Fujimura M (2007) Roles of putative His-to-Asp signaling modules HPT-1 and RRG-2, on viability and sensitivity to osmotic and oxidative stresses in Neurospora crassa. Curr Genet 51(3):197–208

    Article  CAS  PubMed  Google Scholar 

  • Beever RE, Byrde RJW (1982) Resistance to the dicarboximide fungicides. In: Dekker J, Georgopoulos SG (eds) Fungicide resistance in crop protection. Pudoc, Wageningen, the Netherlands, pp 101–117

    Google Scholar 

  • Beever RE, Laracy EP, Pak HA (1989) Strains of Botrytis cinerea resistant to dicarboximide and benzimidazole fungicides in New Zealand vineyards. Plant Pathol 38(3):427–437

    Article  Google Scholar 

  • Catlett NL, Yoder OC, Turgeon BG (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot Cell 2(6):1151–1161

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chapeland F, Fritz R, Lanen C, Gredt M, Leroux P (1999) Inheritance and mechanisms of resistance to anilinopyrimidine fungicides in Botrytis cinerea (Botryotinia fuckeliana). Pestic Biochem Physiol 64(2):85–100

    Article  CAS  Google Scholar 

  • Cui W, Beever RE, Parkes SL, Weeds PL, Templeton MD (2002) An osmosensing histidine kinase mediates dicarboximide fungicide resistance in Botryotinia fuckeliana (Botrytis cinerea). Fungal Genet Biol 36(3):187–198

    Article  CAS  PubMed  Google Scholar 

  • Cui W, Beever RE, Parkes SL, Templeton MD (2004) Evolution of an osmosensing histidine kinase in field strains of Botryotinia fuckeliana (Botrytis cinerea) in response to dicarboximide fungicide usage. Phytopathology 94(10):1129–1135

    Article  CAS  PubMed  Google Scholar 

  • Dongo A, Bataille-Simoneau N, Campion C, Guillemette T, Hamon B, Iacomi-Vasilescu B, Katz L, Simoneau P (2009) The group III two-component histidine kinase of filamentous fungi is involved in the fungicidal activity of the bacterial polyketide ambruticin. Appl Environ Microbiol 75(1):127–134

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dry IB, Yuan KH, Hutton DG (2004) Dicarboximide resistance in field isolates of Alternaria alternata is mediated by a mutation in a two-component histidine kinase gene. Fungal Genet Biol 41(1):102–108

    Article  CAS  PubMed  Google Scholar 

  • Duan Y, Ge C, Liu S, Wang J, Zhou M (2013) A two-component histidine kinase Shk1 controls stress response, sclerotial formation and fungicide resistance in Sclerotinia sclerotiorum. Mol Plant Pathol 14(7):708–718

    Article  CAS  PubMed  Google Scholar 

  • Edlich W, Lyr H (1995) Mechanism of action of dicarboximide fungicides. In: Lyr H (ed) Modern selective fungicides: properties, applications, and mechanisms of action. Spektrum Akademischer Verlag, New York, pp 119–131

    Google Scholar 

  • Faretra F, Pollastro S (1991) Genetic basis of resistance to benzimidazole and dicarboximide fungicides in Botryotinia fuckeliana (Botrytis cinerea). Mycol Res 95(8):943–951

    Article  CAS  Google Scholar 

  • Fillinger S, Ajouz S, Nicot PC, Leroux P, Bardin M (2012) Functional and structural comparison of pyrrolnitrin- and iprodione-induced modifications in the class III histidine-kinase Bos1 of Botrytis cinerea. PLoS One 7(8), e42520

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fujimura M, Ochiai N, Ichiishi A, Usami R, Horikoshi K, Yamaguchi I (2000) Sensitivity to phenylpyrrole fungicides and abnormal glycerol accumulation in os and cut mutant strains of Neurospora crassa. J Pestic Sci 25:31–35

    Article  CAS  Google Scholar 

  • Fujimura M, Ochiai N, Oshima M, Motoyama T, Ichiishi A, Usami R, Horikoshi K, Yamaguchi I (2003) Putative homologs of SSK22 MAPKK kinase and PBS2 MAPK kinase of Saccharomyces cerevisiae encoded by os-4 and os-5 genes for osmotic sensitivity and fungicide resistance in Neurospora crassa. Biosci Biotechnol Biochem 67(1):186–191

    Article  CAS  PubMed  Google Scholar 

  • Fujinami A, Ozaki T, Nodera K, Tanaka K (1971) Studies on biological activity of cyclic imide compounds. Part II. Antimicrobial activity of 1-phenylpyrrolidine-2,5-diones and related compounds. Agric Biol Chem 35:1707–1719

    Article  CAS  Google Scholar 

  • Furukawa K, Katsuno Y, Urao T, Yabe T, Yamada-Okabe T, Yamada-Okabe H, Yamagata Y, Abe K, Nakajima T (2002) Isolation and functional analysis of a gene, tcsB, encoding a transmembrane hybrid-type histidine kinase from Aspergillus nidulans. Appl Environ Microbiol 68(11):5304–5310

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Furukawa K, Hoshi Y, Maeda T, Nakajima T, Abe K (2005) Aspergillus nidulans HOG pathway is activated only by two-component signalling pathway in response to osmotic stress. Mol Microbiol 56(5):1246–1261

    Article  CAS  PubMed  Google Scholar 

  • Gehmann K, Nyfeler R, Leadbeater A, Nevill D, Sozzi D (1990) CGA 173506: a new phenylpyrrole fungicide for broad-spectrum disease control. In: Proceedings of the Brighton crop protection conference pests diseases 2. British Crop Protection Council, Farnham, pp 339–406

    Google Scholar 

  • Grabke A, Fernandez-Ortuno D, Amiri A, Li X, Peres NA, Smith P, Schnabel G (2014) Characterization of iprodione resistance in Botrytis cinerea from strawberry and blackberry. Phytopathology 104(4):396–402

    Article  CAS  PubMed  Google Scholar 

  • Grindle M, Temple W (1982) Fungicide resistance of os mutants of Neurospora crassa. Neurospora Newsl 29:16–17

    Google Scholar 

  • Hisada Y, Kawase Y (1977) Morphological studies of antifungal action of N-(3′, 5′-dichlorophenyl)-1, 2-dimethylcyclopropane-1, 2-dicarboximide on Botrytis cinerea. Ann Phytopathol Soc Jpn 43:151–158

    Article  Google Scholar 

  • Hisada Y, Kato T, Kawase Y (1978) Mechanism of antifungal action of procymidone in Botrytis cinerea. Ann Phytopathol Soc Jpn 44(4):509–518

    Article  Google Scholar 

  • Hutton DG (1988) The appearance of dicarboximide resistance in Alternaria alternata in passionfruit in south-east Queensland. Australas Plant Pathol 17(2):34–36

    Article  Google Scholar 

  • Iacomi-Vasilescu B, Bataille-Simoneau N, Campion C, Dongo A, Laurent E, Serandat I, Hamon B, Simoneau P (2008) Effect of null mutations in the AbNIK1 gene on saprophytic and parasitic fitness of Alternaria brassicicola isolates highly resistant to dicarboximide fungicides. Plant Pathol 57:937–947

    Article  CAS  Google Scholar 

  • Izumitsu K, Yoshimi A, Tanaka C (2007) Two-component response regulators Ssk1p and Skn7p additively regulate high-osmolarity adaptation and fungicide sensitivity in Cochliobolus heterostrophus. Eukaryot Cell 6(2):171–181

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Izumitsu K, Yoshimi A, Hamada S, Morita A, Saitoh Y, Tanaka C (2009) Dic2 and Dic3 loci confer osmotic adaptation and fungicidal sensitivity independent of the HOG pathway in Cochliobolus heterostrophus. Mycol Res 113(Pt 10):1208–1215

    Article  CAS  PubMed  Google Scholar 

  • Jespers ABK, De Waard MA (1995) Effect of fenpiclonil on phosphorylation of glucose in Fusarium sulphureum. Pestic Sci 44(2):167–175

    Article  CAS  Google Scholar 

  • Jespers ABK, Davidse LC, Dewaard MA (1993) Biochemical effects of the phenylpyrrole fungicide fenpiclonil in Fusarium sulphureum (Schlecht). Pestic Biochem Physiol 45(2):116–129

    Article  CAS  Google Scholar 

  • Jones CA, Greer-Phillips SE, Borkovich KA (2007) The response regulator RRG-1 functions upstream of a mitogen-activated protein kinase pathway impacting asexual development, female fertility, osmotic stress, and fungicide resistance in Neurospora crassa. Mol Biol Cell 18(6):2123–2136

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kamei M, Takahashi M, Banno S, Ichiishi A, Fukumori F, Fujimura M (2013) Regulation and physiological function of MAP kinase and cAMP-PKA pathways. In: Kasbekar D, McCluskey K (eds) Neurospora: genomics and molecular biology. Horizon Scientific Press/Caister Academic Press, Norwich, pp 171–192

    Google Scholar 

  • Kojima K, Takano Y, Yoshimi A, Tanaka C, Kikuchi T, Okuno T (2004) Fungicide activity through activation of a fungal signalling pathway. Mol Microbiol 53(6):1785–1796

    Article  CAS  PubMed  Google Scholar 

  • Kretschmer M, Leroch M, Mosbach A, Walker AS, Fillinger S, Mernke D, Schoonbeek HJ, Pradier JM, Leroux P, De Waard MA, Hahn M (2009) Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog 5(12):e1000696

    Article  PubMed Central  PubMed  Google Scholar 

  • Leroch M, Plesken C, Weber RW, Kauff F, Scalliet G, Hahn M (2013) Gray mold populations in German strawberry fields are resistant to multiple fungicides and dominated by a novel clade closely related to Botrytis cinerea. Appl Environ Microbiol 79(1):159–167

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leroux P, Clerjeau M (1985) Resistance of Botrytis cinerea Pers. and Plasmopara viticola (Berk. & Curt.) Berl. and de Toni to fungicides in French vineyards. Crop Prot 4:137–160

    Article  CAS  Google Scholar 

  • Leroux P, Lanen C, Fritz R (1992) Similarities in the antifungal activities of fenpiclonil, iprodione and tolclofos-methyl against Botrytis cinerea and Fusarium nivale. Pestic Sci 36:255–261

    Article  CAS  Google Scholar 

  • Leroux P, Chapeland F, Desbrosses D, Gredt M (1999) Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards. Crop Prot 18(10):687–697

    Article  CAS  Google Scholar 

  • Leroux P, Fritz R, Debieu D, Albertini C, Lanen C, Bach J, Gredt M, Chapeland F (2002) Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Manag Sci 58(9):876–888

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Leroux P, Fillinger S (2008) The HOG1-like MAP kinase Sak1 of Botrytis cinerea is negatively regulated by the upstream histidine kinase Bos1 and is not involved in dicarboximide- and phenylpyrrole-resistance. Fungal Genet Biol 45(7):1062–1074

    Article  CAS  PubMed  Google Scholar 

  • Locke T, Fletcher JT (1988) Incidence of benomyl and iprodione resistance in isolates of Botrytis cinerea in tomato crops in England and Wales in 1986. Plant Pathol 37(3):381–384

    Article  CAS  Google Scholar 

  • Luo Y, Yang J, Zhu M, Yan J, Mo M, Zhqng K (2008) Characterization of mutations in AlHK1 gene from Alternaria longipes: implication of limited function of two-component histidine kinase on conferring dicarboximide resistance. J Microbiol Biotechnol 18(1):15–22

    CAS  PubMed  Google Scholar 

  • Luo YY, Yang JK, Zhu ML, Liu CJ, Li HY, Lu ZB, Pan WZ, Zhang ZH, Bi W, Zhang KQ (2013) The group III two-component histidine kinase AlHK1 is involved in fungicides resistance, osmosensitivity, spore production and impacts negatively pathogenicity in Alternaria longipes. Curr Microbiol 64(5):449–456

    Article  Google Scholar 

  • Ma Z, Luo Y, Michailides T (2006) Molecular characterization of the two-component histidine kinase gene from Monilinia fructicola. Pest Manag Sci 62(10):991–998

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Yan L, Luo Y, Michailides TJ (2007) Sequence variation in the two-component histidine kinase gene of Botrytis cinerea associated with resistance to dicarboximide fungicides. Pestic Biochem Physiol 88(3):300–306

    Article  CAS  Google Scholar 

  • Maeda T, Wurgler-Murphy SM, Saito H (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369(6477):242–245

    Article  CAS  PubMed  Google Scholar 

  • Mays L (1969) Isolation, characterization, and genetic analysis of osmotic mutants of Neurospora crassa. Genetics 63:781–794

    PubMed Central  CAS  PubMed  Google Scholar 

  • Meena N, Kaur H, Mondal AK (2010) Interactions among HAMP domain repeats act as an osmosensing molecular switch in group III hybrid histidine kinases from fungi. J Biol Chem 285(16):12121–12132

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mernke D, Dahm S, Walker AS, Laleve A, Fillinger S, Leroch M, Hahn M (2011) Two promoter rearrangements in a drug efflux transporter gene are responsible for the appearance and spread of multidrug resistance phenotype MDR2 in Botrytis cinerea isolates in French and German vineyards. Phytopathology 101(10):1176–1183

    Article  CAS  PubMed  Google Scholar 

  • Motoyama T, Kadokura K, Ohira T, Ichiishi A, Fujimura M, Yamaguchi I, Kudo T (2005a) A two-component histidine kinase of the rice blast fungus is involved in osmotic stress response and fungicide action. Fungal Genet Biol 42(3):200–212

    Article  CAS  PubMed  Google Scholar 

  • Motoyama T, Ohira T, Kadokura K, Ichiishi A, Fujimura M, Yamaguchi I, Kudo T (2005b) An Os-1 family histidine kinase from a filamentous fungus confers fungicide-sensitivity to yeast. Curr Genet 47(5):298–306

    Article  CAS  PubMed  Google Scholar 

  • Noguchi R, Banno S, Ichikawa R, Fukumori F, Ichiishi A, Kimura M, Yamaguchi I, Fujimura M (2007) Identification of OS-2 MAP kinase-dependent genes induced in response to osmotic stress, antifungal agent fludioxonil, and heat shock in Neurospora crassa. Fungal Genet Biol 44(3):208–218

    Article  CAS  PubMed  Google Scholar 

  • Ochiai N, Fujimura M, Oshima M, Motoyama T, Ichiishi A, Yamada-Okabe H, Yamaguchi I (2002) Effects of iprodione and fludioxonil on glycerol synthesis and hyphal development in Candida albicans. Biosci Biotechnol Biochem 66(10):2209–2215

    Article  CAS  PubMed  Google Scholar 

  • Ochiai N, Tokai T, Nishiuchi T, Takahashi-Ando N, Fujimura M, Kimura M (2007) Involvement of the osmosensor histidine kinase and osmotic stress-activated protein kinases in the regulation of secondary metabolism in Fusarium graminearum. Biochem Biophys Res Commun 363(3):639–644

    Article  CAS  PubMed  Google Scholar 

  • Okada A, Banno S, Ichiishi A, Kimura M, Yamaguchi I, Fujimura M (2005) Pyrrolnitrin interferes with osmotic signal transduction pathway in Neurospora crassa. J Pestic Sci 30:378–383

    Article  CAS  Google Scholar 

  • Orth AB, Rzhetskaya M, Pell EJ, Tien M (1995) A serine (threonine) protein kinase confers fungicide resistance in the phytopathogenic fungus Ustilago maydis. Appl Environ Microbiol 61(6):2341–2345

    PubMed Central  CAS  PubMed  Google Scholar 

  • Oshima M, Fujimura M, Banno S, Hashimoto C, Motoyama T, Ichiishi A, Yamaguchi I (2002) A point mutation in the two-component histidine kinase BcOS-1 gene confers dicarboximide resistance in field isolates of Botrytis cinerea. Phytopathology 92(1):75–80

    Article  CAS  PubMed  Google Scholar 

  • Oshima M, Banno S, Okada K, Takeuchi T, Kimura M, Ichiishi A, Yamaguchi I, Fujimura M (2006) Survey of mutations of a histidine kinase gene BcOS1 in dicarboximide-resistant field isolates of Botrytis cinerea. J Gen Plant Pathol 72(1):65–73

    Article  CAS  Google Scholar 

  • Pillonel C, Meyer T (1997) Effect of phenylpyrroles on glycerol accumulation and protein kinase activity of Neurospora crassa. Pestic Sci 49(3):229–236

    Article  CAS  Google Scholar 

  • Pommer E, Lorenz G (1995) Dicarboximide fungicides. In: Lyr H (ed) Modern selective fungicides – properties, applications, mechanisms of action. Gustav Fischer Verlag, New York, pp 99–118

    Google Scholar 

  • Ramesh MA, Laidlaw RD, Durrenberger F, Orth AB, Kronstad JW (2001) The cAMP signal transduction pathway mediates resistance to dicarboximide and aromatic hydrocarbon fungicides in Ustilago maydis. Fungal Genet Biol 32(3):183–193

    Article  CAS  PubMed  Google Scholar 

  • Raposo R, Gomez V, Urrutia T, Melgarejo P (2000) Fitness of Botrytis cinerea associated with dicarboximide resistance. Phytopathology 90(11):1246–1249

    Article  CAS  PubMed  Google Scholar 

  • Schaller GE, Shiu SH, Armitage JP (2011) Two-component systems and their co-option for eukaryotic signal transduction. Curr Biol 21(9):R320–R330

    Article  CAS  PubMed  Google Scholar 

  • Schumacher MM, Enderlin CS, Selitrennikoff CP (1997) The osmotic-1 locus of Neurospora crassa encodes a putative histidine kinase similar to osmosensors of bacteria and yeast. Curr Microbiol 34(6):340–347

    Article  CAS  PubMed  Google Scholar 

  • Segmuller N, Ellendorf U, Tudzynski B, Tudzynski P (2007) BcSAK1, a stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot Cell 6(2):211–221

    Article  PubMed Central  PubMed  Google Scholar 

  • Van Thuat N, Schafer W, Bormann J (2012) The stress-activated protein kinase FgOS-2 is a key regulator in the life cycle of the cereal pathogen Fusarium graminearum. Mol Plant Microbe Interact 25(9):1142–1156

    Article  PubMed  Google Scholar 

  • Viaud M, Fillinger S, Liu W, Polepalli JS, Le Pecheur P, Kunduru AR, Leroux P, Legendre L (2006) A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Mol Plant Microbe Interact 19(9):1042–1050

    Article  CAS  PubMed  Google Scholar 

  • Walker AS, Micoud A, Remuson F, Grosman J, Gredt M, Leroux P (2013) French vineyards provide information that opens ways for effective resistance management of Botrytis cinerea (grey mould). Pest Manag Sci 69(6):667–678

    Article  CAS  PubMed  Google Scholar 

  • Watanabe S, Yamashita K, Ochiai N, Fukumori F, Ichiishi A, Kimura M, Fujimura M (2007) OS-2 mitogen activated protein kinase regulates the clock-controlled gene ccg-1 in Neurospora crassa. Biosci Biotechnol Biochem 71(11):2856–2859

    Article  CAS  PubMed  Google Scholar 

  • Yamashita K, Shiozawa A, Banno S, Fukumori F, Ichiishi A, Kimura M, Fujimura M (2007) Involvement of OS-2 MAP kinase in regulation of the large-subunit catalases CAT-1 and CAT-3 in Neurospora crassa. Genes Genet Syst 82(4):301–310

    Article  CAS  PubMed  Google Scholar 

  • Yamashita K, Shiozawa A, Watanabe S, Fukumori F, Kimura M, Fujimura M (2008) ATF-1 transcription factor regulates the expression of ccg-1 and cat-1 genes in response to fludioxonil under OS-2 MAP kinase in Neurospora crassa. Fungal Genet Biol 45(12):1562–1569

    Article  CAS  PubMed  Google Scholar 

  • Yoshimi A, Tsuda M, Tanaka C (2004) Cloning and characterization of the histidine kinase gene Dic1 from Cochliobolus heterostrophus that confers dicarboximide resistance and osmotic adaptation. Mol Genet Genomics 271(2):228–236

    Article  CAS  PubMed  Google Scholar 

  • Yoshimi A, Kojima K, Takano Y, Tanaka C (2005) Group III histidine kinase is a positive regulator of Hog1-type mitogen-activated protein kinase in filamentous fungi. Eukaryot Cell 4(11):1820–1828

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang Y, Lamm R, Pillonel C, Lam S, Xu JR (2002) Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl Environ Microbiol 68(2):532–538

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Faculty of Life Sciences, Toyo University, Ora, Gunma, 374-0193, Japan

    Makoto Fujimura, Shinpei Banno, Akihiko Ichiishi & Fumiyasu Fukumori

  2. Yamanashi Experiment Station, Japan Plant Protection Association, Minami, Yamanashi, 405-0042, Japan

    Shinpei Banno

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  1. Makoto Fujimura
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  2. Shinpei Banno
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  3. Akihiko Ichiishi
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  4. Fumiyasu Fukumori
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Correspondence to Makoto Fujimura .

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  1. Kibi International University, Minami-Awaji, Hyogo, Japan

    Hideo Ishii

  2. Bristol, United Kingdom

    Derek William Hollomon

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Fujimura, M., Banno, S., Ichiishi, A., Fukumori, F. (2015). Histidine Kinase Inhibitors. In: Ishii, H., Hollomon, D. (eds) Fungicide Resistance in Plant Pathogens. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55642-8_12

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