Functional and structural comparison of Pyrrolnitrin- and Iprodione-induced modifications in the class III histidine-kinase Bos1 of Botrytis cinerea

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Fillinger, Sabine ^a   Ajouz, Sakhr ^b   Nicot, Philippe C ^b   Leroux, Pierre ^a   Bardin, Marc ^b  

^a INRA Institut National de la Recherche Agronomique   (France)

^b INRA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BOS1 PROTEIN; HEPCIDIN; IPRODIONE; PROTEIN HISTIDINE KINASE; PYRROLNITRIN; UNCLASSIFIED DRUG;

ARTICLE; BOS1 GENE; BOTRYTIS CINEREA; ENZYME MODIFICATION; FUNGICIDAL ACTIVITY; FUNGICIDE RESISTANCE; FUNGUS GROWTH; GENE; GENE MUTATION; GENE SEQUENCE; HYDROPHOBICITY; LOSS OF FUNCTION MUTATION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC STRESS; PHENOTYPE; PROTEIN DOMAIN; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; AMINOIMIDAZOLE CARBOXAMIDE; ANTIFUNGAL AGENTS; BOTRYTIS; DRUG RESISTANCE, FUNGAL; HYDANTOINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; OSMOTIC PRESSURE; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PYRROLNITRIN;

EID: 84865058329     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042520     Document Type: Article

References (57)

1. Jarvis RW (1977) Botryotinia and Botrytis species: taxonomy, physiology, and pathogenicity. A guide to the literature. Ottawa, Canada: Canada Department of Agriculture. 195 p.
2. Leroux P (2004) Chemical control of Botrytis and its resistance to chemical fungicides. In: Elad Y, Williamson B, Tudzynski P, Delen N, editors. Botrytis: Biology, Pathology and Control. Dordrecht, The Netherlands: Kluwer Academic Press. pp. 195-222.
3. Myresiotis CK, Karaoglanidis GS, Tzavella-Monari K, (2007) Resistance of Botrytis cinerea isolates from vegetable crops to anilinopyrimidine, phenylpyrrole, hydroxyanilide, benzimidazole, and dicarboximide fungicides. Plant Disease 91: 407-413.
4. Duffy B, Schouten A, Raaijmakers JM, (2003) Pathogen self-defense: mechanisms to counteract microbial antagonism. Annual Review of Phytopathology 41: 501-538.
5. Elad Y, Stewart A (2004) Microbial control of Botrytis spp. In: Elad Y, Williamson B, Tudzynski P, Delen N, editors. Botrytis: Biology, Pathology and Control. Dordrecht, The Netherlands: Kluwer Academic Press. pp. 223-241.
6. Elmer PAG, Reglinski T, (2006) Biosuppression of Botrytis cinerea in grapes. Plant Pathology 55: 155-177.
7. Raaijmakers JM, Vlami M, de Souza JT, (2002) Antibiotic production by bacterial biocontrol agents. Antonie Van Leeuwenhoek International (Journal of General and Molecular Microbiology) 81: 537-547.
8. Arima K, Imanaka H, Kousaka M, Fukuta A, Tamura G, (1964) Pyrrolnitrin, a new antibiotic substance, produced by Pseudomonas. Agricultural and Biological Chemistry 28: 275-276.
9. Hammer PE, Burd W, Hill DS, Ligon JM, van Pee KH, (1999) Conservation of the pyrrolnitrin biosynthetic gene cluster among six pyrrolnitrin-producing strains. FEMS Microbiology Letters 180: 39-44.
10. Chernin L, Brandis A, Ismailov Z, Chet I, (1996) Pyrrolnitrin production by an Enterobacter agglomerans strain with a broad spectrum of antagonistic activity towards fungal and bacterial phytopathogens. Current Microbiology 32: 208-212.
11. Janisiewicz WJ, Roitman J, (1988) Biological control of blue mold and grey mold on apple and pear with Pseudomonas cepacia. Phytopathology 78: 1697-1700.
12. Ajouz S, Walker AS, Fabre F, Leroux P, Nicot PC, et al. (2011) Variability of Botrytis cinerea sensitivity to pyrrolnitrin, an antibiotic produced by biological control agents. BioControl 56: 353-363.
13. Ajouz S, Nicot PC, Bardin M, (2010) Adaptation to pyrrolnitrin in Botrytis cinerea and cost of resistance. Plant Pathology 59: 556-566.
14. Leroux P, Lanen C, Fritz R, (1992) Similarities in the antifungal activities of fenpiclonil, ipridione and tolclofos-methyl against Botrytis cinerea and Fusarium nivale. Pesticide Science 36: 255-261.
15. 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 Protection 18: 687-697.
16. Faretra F, Pollastro S, (1993) Isolation, characterization, and genetic analysis of laboratory mutants of Botryotinia fuckeliana resistant to the phenylpyrrole fungicide CGA 173506. Mycological Research 97: 620-624.
17. Ziogas BN, Markoglou AN, Spyropoulou V, (2005) Effect of phenylpyrrole-resistance mutations on ecological fitness of Botrytis cinerea and their genetical basis in Ustilago maydis. European Journal of Plant Pathology 113: 83-100.
18. 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: 1129-1135.
19. 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 Genetics and Biology 36: 187-198.
20. 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 Genetics and Biology 45: 1062-1074.
21. Oshima M, Fujimura M, Banno S, Hashimoto C, Motoyama T, et al. (2002) A point mutation in the two-component histidine kinase BcOS-1 gene confers dicarboximide resistance in field isolates of Botrytis cinerea. Phytopathology 92: 75-80.
22. Viaud M, Fillinger S, Liu W, Polepalli JS, Le Pecheur P, et al. (2006) A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Molecular Plant-Microbe Interactions 19: 1042-1050.
23. 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. Current Genetics 47: 234-243.
24. 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 Genetics and Biology 41: 102-108.
25. Kanetis L, Forster H, Jones CA, Borkovich KA, Adaskaveg JE, (2008) Characterization of genetic and biochemical mechanisms of fludioxonil and pyrimethanil resistance in field isolates of Penicillium digitatum. Phytopathology 98: 205-214.
26. Ma ZH, Luo Y, Michailides T, (2006) Molecular characterization of the two-component histidine kinase gene from Monilinia fructicola. Pest Management Science 62: 991-998.
27. Nathues E, Jorgens C, Lorenz N, Tudzynski P, (2007) The histidine kinase CpHK2 has impact on spore germination, oxidative stress and fungicide resistance, and virulence of the ergot fungus Claviceps purpurea. Molecular Plant Pathology 8: 653-665.
28. Okada A, Banno S, Ichiishi A, Kimura M, Yamaguchi I, et al. (2005) Pyrrolnitrin interferes with osmotic signal transduction in Neurospora crassa. Journal of Pesticide Science 30: 378-383.
29. Orth AB, Rzhetskaya M, Pell EJ, Tien M, (1995) A serine (threonine) protein kinase confers fungicide resistance in the phytopathogenic fungus Ustilago maydis. Applied And Environmental Microbiology 61: 2341-2345.
30. Pillonel C, Meyer T, (1997) Effect of phenylpyrroles on glycerol accumulation and protein kinase activity of Neurospora crassa. Pesticide Science 49: 229-236.
31. Catlett NL, Yoder OC, Turgeon BG, (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryotic Cell 2: 1151-1161.
32. Parkinson JS, (2010) Signaling Mechanisms of HAMP Domains in Chemoreceptors and Sensor Kinases. Annual Review of Microbiology 64: 101-122.
33. Aravind L, Ponting CP, (1999) The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett 176: 111-116.
34. Hulko M, Berndt F, Gruber M, Linder JU, Truffault V, et al. (2006) The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126: 929-940.
35. Airola MV, Watts KJ, Bilwes AM, Crane BR, (2010) Structure of Concatenated HAMP Domains Provides a Mechanism for Signal Transduction. Structure 18: 436-448.
36. Zhou Q, Ames P, Parkinson JS, (2009) Mutational analyses of HAMP helices suggest a dynamic bundle model of input-output signalling in chemoreceptors. Molecular Microbiology 73: 801-814.
37. Ferris HU, Dunin-Horkawicz S, Mondejar LG, Hulko M, Hantke K, et al. (2011) The mechanisms of HAMP-mediated signaling in transmembrane receptors. Structure 19: 378-385.
38. Watts KJ, Johnson MS, Taylor BL, (2008) Structure-function relationships in the HAMP and proximal signaling domains of the aerotaxis receptor Aer. Journal of Bacteriology 190: 2118-2127.
39. 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. Journal of Biological Chemistry 285: 12121-12132.
40. Ajouz S, Decognet V, Nicot PC, Bardin M, (2010) Microsatellite stability in the plant pathogen Botrytis cinerea after exposure to different selective pressures. Fungal Biology 114: 949-954.
41. Decognet V, Bardin M, Trottin-Caudal Y, Nicot PC, (2009) Rapid change in the genetic diversity of Botrytis cinerea populations after the introduction of strains in a tomato glasshouse. Phytopathology 99: 185-193.
42. Dellaporta SL, Wood J, Hicks JB, (1983) A plant DNA minipreparation: version 2. Plant Molecular Biology Reporter 1: 19-21.
43. Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, et al. (2011) Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7: e1002230.
44. Levis C, Fortini D, Brygoo Y, (1997) Transformation of Botrytis cinerea with the nitrate reductase gene (niaD) shows a high frequency of homologous recombination. Current Genetics 32: 157-162.
45. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
46. Zdobnov EM, Apweiler R, (2001) InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848.
47. Thompson JD, Gibson TJ, Higgins DG, (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2: Unit 2 3.
48. Kim KK, Yokota H, Kim S-H, (1999) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400: 787-792.
49. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797.
50. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25: 1605-1612.
51. Ajouz S, Bardin M, Nicot PC, El Maataoui M, (2011) Comparison of the development in planta of a pyrrolnitrin-resistant mutant of Botrytis cinerea and its sensitive wild-type parent isolate. European Journal of Plant Pathology 129: 31-42.
52. 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. European Journal of Plant Pathology 128: 171-184.
53. Finn RD, Clements J, Eddy SR, (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Research 39: W29-W37.
54. Dunin-Horkawicz S, Lupas AN, (2010) Comprehensive Analysis of HAMP Domains: Implications for Transmembrane Signal Transduction. Journal of Molecular Biology 397: 1156-1174.
55. Benkert P, Biasini M, Schwede T, (2011) Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics 27: 343-350.
56. Leroux P, Fritz R, Debieu D, Albertini C, Lanen C, et al. (2002) Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Management Science 58: 876-888.
57. Vignutelli A, Hilber-Bodmer M, Hilber UW, (2002) Genetic analysis of resistance to the phenylpyrrole fludioxonil and the dicarboximide vinclozolin in Botryotinia fuckeliana (Botrytis cinerea). Mycological Research 106: 329-335.