The osmosensing signal transduction pathway from Botrytis cinerea regulates cell wall integrity and MAP kinase pathways control melanin biosynthesis with influence of light

Fungal Genetics and Biology

Volumn 48, Issue 4, 2011, Pages 377-387

  Liu, Weiwei ^a   Soulié, Marie Christine ^b   Perrino, Claude ^b   Fillinger, Sabine ^a  

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

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Botrytis; Cell wall integrity; Fungus; Gray mold; Light; MAP kinase; Melanin biosynthesis; Osmotic; Signal transduction

Indexed keywords

BETA 1,3 GLUCAN; CHITIN; MELANIN; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOGENIN; PROTEIN BOS1; PROTEIN HISTIDINE KINASE; PROTEIN HOG1; PROTEIN SAK1; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; BOTRYTIS CINEREA; CELL WALL; CONTROLLED STUDY; ENZYME MODIFICATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOSIS; PHENOTYPE; PHOTOSENSITIVITY; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WILD TYPE;

BOTRYTIS; CELL WALL; GENE DELETION; GENES, FUNGAL; LIGHT; MELANINS; OSMOTIC PRESSURE; PHOSPHOTRANSFERASES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

BOTRYOTINIA FUCKELIANA; BOTRYTIS; EUKARYOTA; FUNGI;

EID: 79952037878     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2010.12.004     Document Type: Article

References (83)

1. Alex L.A., et al. Hyphal development in Neurospora crassa: involvement of a two-component histidine kinase. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:3416-3421.
2. Arbelet D., et al. Disruption of the Bcchs3a chitin synthase gene in Botrytis cinerea is responsible for altered adhesion and overstimulation of host plant immunity. Mol. Plant-Microbe Interact. 2010, 23:1324-1334.
3. Bahn Y.-S. Master and commander in fungal pathogens: the two-component system and the HOG signaling pathway. Eukaryot. Cell 2008, 7:2017-2036.
4. Bahn Y.-S., et al. A unique fungal two-component system regulates stress responses, drug sensitivity, sexual development, and virulence of Cryptococcus neoformans. Mol. Biol. Cell 2006, 17:3122-3135.
5. Bahn Y.S., et al. Sensing the environment: lessons from fungi. Nat. Rev. Microbiol. 2007, 5:57-69.
6. Bayram Ö., et al. Spotlight on Aspergillus nidulans photosensory systems. Fungal Genet. Biol. 2010, 47:900-908.
7. Bell W., Wheeler M. Biosynthesis and functions of fungal melanins. Annu. Rev. Phytopathol. 1986, 24:411-451.
8. Bermejo C., et al. The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol. Biol. Cell 2008, 19:1113-1124.
9. Butler M.J., et al. Melanin synthesis by Sclerotinia sclerotiorum. Mycologia 2009, 101:296-304.
10. Büttner P., et al. Variations in ploidy among isolates of Botrytis cinerea: implications for genetic and molecular analyses. Curr. Genet. 1994, 25:445-450.
11. Cabib E. Differential inhibition of chitin synthetases 1 and 2 from Saccharomyces cerevisiae by polyoxin D and nikkomycins. Antimicrob. Agents Chemother. 1991, 35:170-173.
12. Casadevall A., et al. Melanin and virulence in Cryptococcus neoformans. Curr. Opin. Microbiol. 2000, 3:354-358.
13. Catlett N.L., et al. Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot. Cell 2003, 2:1151-1161.
14. Damveld R.A., et al. Expression of agsA, one of five 1,3-[alpha]-d-glucan synthase-encoding genes in Aspergillus niger, is induced in response to cell wall stress. Fungal Genet. Biol. 2005, 42:165-177.
15. de Jong J.C., et al. Glycerol generates turgor in rice blast. Nature (London) 1997, 389:244-245.
16. de Paula R.M., et al. A connection between MAPK pathways and circadian clocks. Cell Cycle 2008, 7:2630-2634.
17. Doehlemann G., et al. Different signalling pathways involving a Ga protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol. Microbiol. 2006, 59:821-835.
18. Doss R.P., et al. Melanin in the extracellular matrix of germlings of Botrytis cinerea. Phytochemistry 2003, 63:687-691.
19. Eliahu N., et al. Melanin biosynthesis in the maize pathogen Cochliobolus heterostrophus depends on two mitogen-activated protein kinases, Chk1 and Mps1, and the transcription factor Cmr1. Eukaryot. Cell 2007, 6:421-429.
20. Fuchs B.B., Mylonakis E. Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot. Cell 2009, 8:1616-1625.
21. Fujioka T., et al. MpkA-Dependent and -independent cell wall integrity signaling in Aspergillus nidulans. Eukaryot. Cell 2007, 6:1497-1510.
22. Garcia-Rodriguez L.J., et al. Cell integrity signaling activation in response to hyperosmotic shock in yeast. FEBS Lett. 2005, 579:6186-6190.
23. Govrin E.M., Levine A. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 2000, 10:751-757.
24. Gustin M.C., et al. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 1998, 62:1264-1300.
25. Hagiwara D., et al. Characterization of the NikA histidine kinase implicated in the phosphorelay signal transduction of Aspergillus nidulans, with special reference to fungicide responses. Biosci. Biotechnol. Biochem. 2007, 71:844-847.
26. Hahn J.S., Thiele D.J. Regulation of the Saccharomyces cerevisiae Slt2 kinase pathway by the stress-inducible Sdp1 dual specificity phosphatase. J. Biol. Chem. 2002, 277:21278-21284.
27. Hou Z., et al. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant-Microbe Interact. 2002, 15:1119-1127.
28. Howard R.J., Valent B. Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu. Rev. Microbiol. 1996, 50:491-512.
29. Hunter T., Plowman G.D. The protein kinases of budding yeast: six score and more. Trends Biochem. Sci. 1997, 22:18.
30. Idnurm A., et al. The Phycomyces madA gene encodes a blue-light photoreceptor for phototropism and other light responses. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:4546-4551.
31. Idnurm A., et al. A glimpse into the basis of vision in the kingdom Mycota. Fungal Genet. Biol. 2010, 47:881-892.
32. Igbaria A., et al. Distinct and combined roles of the MAP kinases of Cochliobolus heterostrophus in virulence and stress responses. Mol. Plant-Microbe Interact. 2008, 21:769-780.
33. Jones C.A., et al. The response regulator RRG-1 functions upstream of a MAPK pathway impacting asexual development, female fertility, osmotic stress, and fungicide resistance in Neurospora crassa. Mol. Biol. Cell 2007, E06-03-0226.
34. Kawasaki L., et al. SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol. Microbiol. 2002, 45:1153-1163.
35. Kihara J., et al. Expression of THR1, a 1,3,8-trihydroxynaphthalene reductase gene involved in melanin biosynthesis in the phytopathogenic fungus Bipolaris oryzae, is enhanced by near-ultraviolet radiation. Pigm. Cell Res. 2004, 17:15-23.
36. Kihara J., et al. Cloning, functional analysis and expression of a scytalone dehydratase gene (SCD1) involved in melanin biosynthesis of the phytopathogenic fungus Bipolaris oryzae. Curr. Genet. 2004, 45:197-204.
37. Kihara J., et al. Characterization of the BMR1 gene encoding a transcription factor for melanin biosynthesis genes in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol. Lett. 2008, 281:221-227.
38. Kim M.-K., et al. Inhibitory effect of nikkomycin Z on chitin synthases in Candida albicans. Yeast 2002, 19:341-349.
39. Kojima K., et al. The mitogen-activated protein kinase gene MAF1 is essential for the early differentiation phase of appressorium formation in Colletotrichum lagenarium. Mol. Plant-Microbe Interact. 2002, 15:1268-1276.
40. Kojima K., et al. Fungicide activity through activation of a fungal signalling pathway. Mol. Microbiol. 2004, 53:1785-1796.
41. Kuzniak E., Skłodowska M. Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 2005, 222:192-200.
42. Langfelder K., et al. Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet. Biol. 2003, 38:143-158.
43. Latgé J.P. The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 2007, 66:279-290.
44. Lenardon M.D., et al. Individual chitin synthase enzymes synthesize microfibrils of differing structure at specific locations in the Candida albicans cell wall. Mol. Microbiol. 2007, 66:1164-1173.
45. Lev S., et al. A mitogen-activated protein kinase of the corn leaf pathogen Cochliobolus heterostrophus is involved in conidiation, appressorium formation, and pathogenicity: diverse roles for mitogen-activated protein kinase homologs in foliar pathogens. PNAS 1999, 96:13542-13547.
46. Liu, W., 2008. Caractérisation de la cascade de signalisation osmotique "os" chez Botrytis cinerea. PhD, University of Paris-Sud XI, Orsay, France.
47. Liu W., et al. 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. 2008, 45:1062-1074.
48. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
49. Maeda H., Ishida N. Specificity of binding of hexopyranosyl polysaccharides with fluorescent brightener. J. Biochem. (Tokyo) 1967, 62:276-278.
50. Maeda T., et al. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 1994, 369:242-245.
51. Mayorga M.E., Gold S.E. A MAP kinase encoded by the ubc3 gene of Ustilago maydis is required for filamentous growth and full virulence. Mol. Microbiol. 1999, 34:485-497.
52. Mehrabi R., et al. MgSlt2, a cellular integrity MAP kinase gene of the fungal wheat pathogen Mycosphaerella graminicola, is dispensable for penetration but essential for invasive growth. Mol. Plant-Microbe Interact. 2006, 19:389-398.
53. Miskei M., et al. Annotation of stress-response proteins in the aspergilli. Fungal Genet. Biol. 2009, 46:S105-S120.
54. Moriwaki A., et al. Disruption of SRM1, a mitogen-activated protein kinase gene, affects sensitivity to osmotic and ultraviolet stressors in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol. Lett. 2006, 257:253-261.
55. Motoyama T., et al. A two-component histidine kinase of the rice blast fungus is involved in osmotic stress response and fungicide action. Fungal Genet. Biol. 2005, 42:200-212.
56. Motoyama T., et al. Involvement of putative response regulator genes of the rice blast fungus Magnaporthe oryzae in osmotic stress response, fungicide action, and pathogenicity. Curr. Genet. 2008, 54:185-195.
57. Müller P., et al. The MAP kinase Kpp2 regulates mating and pathogenic development in Ustilago maydis. Mol. Microbiol. 1999, 34:1007-1017.
58. Di Pietro A., et al. A MAP kinase of the vascular wilt fungus Fusarium oxysporum is essential for root penetration and pathogenesis. Mol. Microbiol. 2001, 39:1140-1152.
59. Pontecorvo G., et al. The genetics of Aspergillus nidulans. Adv. Genet. 1953, 5:141-239.
60. Posas F., et al. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell 1996, 86:865-875.
61. Rispail N., et al. Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet. Biol. 2009, 46:287-298.
62. Rui O., Hahn M. The Slt2-type MAP kinase Bmp3 of Botrytis cinerea is required for normal saprotrophic growth, conidiation, plant surface sensing and host tissue colonization. Mol. Plant Pathol. 2007, 8:173-184.
63. Schumacher M.M., et al. The osmotic-1 locus of Neurospora crassa encodes a putative histidine kinase similar to osmosensors of bacteria and yeast. Curr. Microbiol. 1997, 34:340-347.
64. Segmüller N., et al. BcSAK1, a stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot. Cell 2007, 6:211-221.
65. Soulié M.C., et al. Disruption of Botrytis cinerea class I chitin synthase gene Bcchs1 results in cell wall weakening and reduced virulence. Fungal Genet. Biol. 2003, 40:38-46.
66. Soulié M.-C., et al. Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a). Cell. Microbiol. 2006, 8:1310-1321.
67. Takano Y., et al. The Colletotrichum lagenarium MAP kinase gene CMK1 regulates diverse aspects of fungal pathogenesis. Mol. Plant-Microbe Interact. 2000, 13:374-383.
68. Tamas, M.J., Hohmann, S., 2003. The Osmotic Stress Response of Saccharomyces cerevisiae. Yeast Stress Responses.
69. Tan K.K. Red-far-red reversible photoreaction in the recovery from blue-light inhibition of sporulation in Botrytis cinerea. J. Gen. Microbiol. 1974, 201-202.
70. Thompson J.E., et al. The second naphthol reductase of fungal melanin biosynthesis in Magnaporthe grisea: tetrahydroxynaphthalene reductase. J. Biol. Chem. 2000, 275:34867-34872.
71. Tiedemann A. Evidence for a primary role of active oxygen species in induction of host cell death during infection of bean leaves with Botrytis cinerea. Physiol. Mol. Plant Pathol. 1997, 50:151-166.
72. Tsuji G., et al. Novel fungal transcriptional activators, Cmr1p of Colletotrichum lagenarium and pig1p of Magnaporthe grisea, contain Cys2His2 zinc finger and Zn(II)2Cys6 binuclear cluster DNA-binding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol. Microbiol. 2000, 38:940-954.
73. Valiante V., et al. The mitogen-activated protein kinase MpkA of Aspergillus fumigatus regulates cell wall signaling and oxidative stress response. Fungal Genet. Biol. 2008, 45:618-627.
74. Viaud M., et al. A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Mol. Plant-Microbe Interact. 2006, 19:1042.
75. Woloshuk C.P., et al. Melanin biosynthesis in Pyricularia oryzae: site of tricyclazole inhibition and pathogenicity of melanin deficient-mutants. Pestic. Biochem. Physiol. 1980, 14:256-264.
76. Wood P.J. Specificity in the interaction of direct dyes with polysaccharides. Carbohydr. Res. 1980, 81:271-287.
77. Xu J.R. Map kinases in fungal pathogens. Fungal Genet. Biol. 2000, 31:137-152.
78. Xu J.R., Hamer J.E. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 1996, 10:2696-2706.
79. Xu J.-R., et al. Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. PNAS 1998, 95:12713-12718.
80. Yoshimi A., et al. Group III histidine kinase is a positive regulator of Hog1-type mitogen-activated protein kinase in filamentous fungi. Eukaryot. Cell 2005, 4:1820-1828.
81. Zhang D., Miller M. Polyoxins and nikkomycins: progress in synthetic and biological studies. Curr. Pharm. Des. 1999, 5:73-99.
82. Zhang Y., et al. Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl. Environ. Microbiol. 2002, 68:532-538.
83. Zheng L., et al. The BMP1 gene is essential for pathogenicity in the gray mold fungus Botrytis cinerea. Mol. Plant-Microbe Interact. 2000, 13:724-732.