The Transcription Factor BcLTF1 Regulates Virulence and Light Responses in the Necrotrophic Plant Pathogen Botrytis cinerea

PLoS Genetics

Volumn 10, Issue 1, 2014, Pages

  Schumacher, Julia ^a   Simon, Adeline ^b   Cohrs, Kim Christopher ^a   Viaud, Muriel ^b   Tudzynski, Paul ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

ASPERGILLUS NIDULANS; BOTRYTIS; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, FUNGAL; LIGHT; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; OXIDOREDUCTASES; PLANT DISEASES; PLANT PROTEINS; PLANTS; REACTIVE OXYGEN SPECIES; VIRULENCE;

EID: 84893779937     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004040     Document Type: Article

References (102)

1. Williamson B, Tudzynski B, Tudzynski P, van Kan JA, (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8: 561-580.
2. Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP, et al. (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7: e1002230.
3. Van Kan JA, (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11: 247-253.
4. Sharon A, Elad Y, Barakat R, Tudzynski P (2004) Phytohormones in Botrytis-plant interactions. In: Elad Y, Williamson B, Tudzynski P, Delen N, editors. Botrytis: biology, pathology, control. Kluwer, Dordrecht. pp. 163-179.
5. Choquer M, Fournier E, Kunz C, Levis C, Pradier JM, et al. (2007) Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol Lett 277: 1-10.
6. Tudzynski P, Kokkelink L (2009) Botrytis cinerea: Molecular aspects of a necrotrophic life style. In: Deising H, editor. The Mycota V, Plant Relationships, 2nd Edition. Springer-Verlag Berlin Heidelberg. pp. 29-50.
7. Siewers V, Viaud M, Jimenez-Teja D, Collado IG, Schulze Gronover C, et al. (2005) Functional analysis of the cytochrome P450 monooxygenase gene bcbot1 of Botrytis cinerea indicates that botrydial is a strain-specific virulence factor. Mol Plant-Microbe Interact 18: 602-612.
8. Pinedo C, Wang CM, Pradier JM, Dalmais B, Choquer M, et al. (2008) Sesquiterpene synthase from the botrydial biosynthetic gene cluster of the phytopathogen Botrytis cinerea. ACS Chem Biol 3: 791-801.
9. Dalmais B, Schumacher J, Moraga J, LePêcheur P, Tudzynski B, et al. (2011) The Botrytis cinerea phytotoxin botcinic acid requires two polyketide synthases for production and has a redundant role in virulence with botrydial. Mol Plant Pathol 12: 564-579.
10. Faretra F, Antonacci E, (1987) Production of apothecia of Botryotinia fuckeliana (de Bary) Whetz under controlled environmental conditions. Phytopathol Mediterr 26: 29-35.
11. Giraud T, Fortini D, Levis C, Leroux P, Brygoo Y, (1997) RFLP markers show genetic recombination in Botryotinia fuckeliana (Botrytis cinerea) and transposable elements reveal two sympatric species. Mol Biol Evol 14: 1177-1185.
12. Faretra F, Antonacci E, Pollastro S, (1988) Sexual behaviour and mating system of Botryotinia fuckeliana, teleomorph of Botrytis cinerea. J Gen Microbiol 134: 2543-2550.
13. Paul WRC, (1929) A comparative morphological and physiological study of a number of strains of Botrytis cinerea Pers. with special reference to their virulence. Trans Br Mycol Soc 14: 118-134.
14. Quidde T, Osbourn AE, Tudzynski P, (1998) Detoxification of α-tomatine by Botrytis cinerea. Physiol Mol Plant Pathol 52: 151-165.
15. Tan KK, Epton HAS, (1973) Effect of light on the growth and sporulation of Botrytis cinerea. Trans Br Mycol Soc 61: 147-157.
16. Tan KK, (1974) Blue-light inhibition of sporulation in Botrytis cinerea. J Gen Microbiol 82: 191-200.
17. Tan KK, (1975) Interaction of near-ultraviolet, blue, red, and far-red light in sporulation of Botrytis cinerea. Trans Br Mycol Soc 64: 215-222.
18. Schumacher J, Tudzynski P (2012) Morphogenesis and infection in Botrytis cinerea. In: Pérez-Martín J, Di Pietro A, editors. Topics in Current Genetics, Vol. Morphogenesis and Pathogenicity in Fungi. Springer-Verlag Berlin, Heidelberg. pp. 225-241.
19. Linden H, Ballario P, Macino G, (1997) Blue light regulation in Neurospora crassa. Fungal Genet Biol 22: 141-150.
20. Chen CH, Dunlap JC, Loros JJ, (2010) Neurospora illuminates fungal photoreception. Fungal Genet Biol 47: 922-929.
21. Shimura M, Ito Y, Ishii C, Yajima H, Linden H, et al. (1999) Characterization of a Neurospora crassa photolyase-deficient mutant generated by repeat induced point mutation of the phr gene. Fungal Genet Biol 28: 12-20.
22. Froehlich AC, Chen CH, Belden WJ, Madeti C, Roenneberg T, et al. (2010) Genetic and molecular characterization of a cryptochrome from the filamentous fungus Neurospora crassa. Eukaryot Cell 9: 738-750.
23. Bieszke JA, Braun EL, Bean LE, Kang S, Natvig DO, et al. (1999) The nop-1 gene of Neurospora crassa encodes a seven transmembrane helix retinal-binding protein homologous to archaeal rhodopsins. Proc Natl Acad Sci USA 96: 8034-8039.
24. Froehlich AC, Noh B, Vierstra RD, Loros J, Dunlap JC, (2005) Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot Cell 4: 2140-2152.
25. Adams TH, Wieser JK, Yu JH, (1998) Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 62: 35-54.
26. Han KH, (2009) Molecular Genetics of Emericella nidulans sexual development. Mycobiol 37: 171-182.
27. Bayram O, Biesemann C, Krappmann S, Galland P, Braus GH, (2008) More than a repair enzyme: Aspergillus nidulans photolyase-like CryA is a regulator of sexual development. Mol Biol Cell 19: 3254-3262.
28. Purschwitz J, Müller S, Kastner C, Schöser M, Haas H, et al. (2008) Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr Biol 18: 255-259.
29. Rodriguez-Romero J, Hedtke M, Kastner C, Müller S, Fischer R, (2010) Fungi, hidden in soil or up in the air: light makes a difference. Annu Rev Microbiol 64: 585-610.
30. Heller J, Ruhnke N, Espino J, Massaroli M, Collado IG, et al. (2012) The MAP kinase BcSak1 of Botrytis cinerea is required for pathogenic development and has broad regulatory functions beyond stress response. Mol Plant Microbe Interact 25: 802-816.
31. Schumacher J, Pradier JM, Simon A, Traeger S, Moraga J, et al. (2012) Natural variation in the VELVET gene bcvel1 affects virulence and light-dependent differentiation in Botrytis cinerea. PLoS One 7: e47840.
32. Schumacher J, Gautier A, Morgant G, Studt L, Ducrot PH, et al. (2013) A functional bikaverin biosynthesis gene cluster in rare strains of Botrytis cinerea is positively controlled by VELVET. PLoS One 8: e53729.
33. Han KH, Han KY, Yu JH, Chae KS, Jahng KY, et al. (2001) The nsdD gene encodes a putative GATA-type transcription factor necessary for sexual development of Aspergillus nidulans. Mol Microbiol 41: 299-309.
34. Grosse V, Krappmann S, (2008) The asexual pathogen Aspergillus fumigatus expresses functional determinants of Aspergillus nidulans sexual development. Eukaryot Cell 7: 1724-1732.
35. Szewczyk E, Krappmann S, (2010) Conserved regulators of mating are essential for Aspergillus fumigatus cleistothecium formation. Eukaryot Cell 9: 774-783.
36. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103: 10352-10357.
37. Chen CH, Ringelberg CS, Gross RH, Dunlap JC, Loros JJ, (2009) Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J 28: 1029-1042.
38. Nowrousian M, Teichert I, Masloff S, Kück U, (2012) Whole-genome sequencing of Sordaria macrospora mutants identifies developmental genes. G3 (Bethesda) 2: 261-270.
39. Giesbert S, Schumacher J, Kupas V, Espino J, Segmüller N, et al. (2012) Identification of pathogenesis-associated genes by T-DNA-mediated insertional mutagenesis in Botrytis cinerea: A type 2A phosphoprotein phosphatase and a SPT3 transcription factor have significant impact on virulence. Mol Plant Microbe Interact 25: 481-495.
40. Li M, Rollins JA, (2009) The development-specific protein (Ssp1) from Sclerotinia sclerotiorum is encoded by a novel gene expressed exclusively in sclerotium tissues. Mycologia 101: 34-43.
41. Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG, (2003) Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci USA 100: 15670-15675.
42. Loros JJ, Denome SA, Dunlap JC, (1989) Molecular cloning of genes under control of the circadian clock in Neurospora. Science 243: 385-388.
43. Leroch M, Mernke D, Koppenhoefer D, Schneider P, Mosbach A, et al. (2011) Living colors in the gray mold pathogen Botrytis cinerea: codon-optimized genes encoding green fluorescent protein and mCherry, which exhibit bright fluorescence. Appl Environ Microbiol 77: 2887-2897.
44. Govrin EM, Levine A, (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10: 751-757.
45. Heller J, Meyer AJ, Tudzynski P, (2012) Redox-sensitive GFP2: use of the genetically encoded biosensor of the redox status in the filamentous fungus Botrytis cinerea. Mol Plant Pathol 13: 935-947.
46. Subramanian A, Kuehn H, Gould J, Tamayo P, Mesirov JP, (2007) GSEA-P: a desktop application for Gene Set Enrichment Analysis. Bioinformatics 23: 3251-3253.
47. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, et al. (2003) PGC-1 alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273.
48. Smith KM, Sancar G, Dekhang R, Sullivan CM, Li S, et al. (2010) Transcription factors in light and circadian clock signaling networks revealed by genome-wide mapping of direct targets for Neurospora white collar complex. Eukaryot Cell 9: 1549-1556.
49. Christie JM, (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58: 21-45.
50. Simon A, Dalmais B, Morgant G, Viaud M, (2013) Screening of a Botrytis cinerea one-hybrid library reveals a Cys(2)His(2) transcription factor involved in the regulation of secondary metabolism gene clusters. Fungal Genet Biol 52: 9-19.
51. Hoffmeister D, Keller NP, (2007) Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24: 393-416.
52. Thewes S, Prado-Cabrero A, Prado MM, Tudzynski B, Avalos J, (2005) Characterization of a gene in the car cluster of Fusarium fujikuroi that codes for a protein of the carotenoid oxygenase family. Mol Genet Genomics 274: 217-228.
53. Prado-Cabrero A, Scherzinger D, Avalos J, Al-Babili S, (2007) Retinal biosynthesis in fungi: characterization of the carotenoid oxygenase CarX from Fusarium fujikuroi. Eukaryot Cell 6: 650-657.
54. Avalos J, Estrada AF, (2010) Regulation by light in Fusarium. Fungal Genet Biol 47: 930-938.
55. Heller J, Tudzynski P, (2011) Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu Rev Phytopathol 49: 369-390.
56. Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN, (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141: 357-366.
57. Van Aken O, Giraud E, Clifton R, Whelan J, (2009) Alternative oxidase: a target and regulator of stress responses. Physiol Plant 137: 354-361.
58. Volkov AN, Nicholls P, Worrall JA, (2011) The complex of cytochrome c and cytochrome c peroxidase: the end of the road? Biochim Biophys Acta 1807: 1482-1503.
59. Jarmuszkiewicz W, Woyda-Ploszczyca A, Antos-Krzeminska N, Sluse FE, (2010) Mitochondrial uncoupling proteins in unicellular eukaryotes. Biochim Biophys Acta 1797: 792-799.
60. Schumacher J, de Larrinoa IF, Tudzynski B, (2008) Calcineurin-responsive zinc finger transcription factor CRZ1 of Botrytis cinerea is required for growth, development, and full virulence on bean plants. Eukaryot Cell 7: 584-601.
61. Cary JW, Harris-Coward PY, Ehrlich KC, Mack BM, Kale SP, et al. (2012) NsdC and NsdD affect Aspergillus flavus morphogenesis and aflatoxin production. Eukaryot Cell 11: 1104-1111.
62. Urbasch I, (1985) Ultrastructural studies on the microconidia of Botrytis cinerea Pers. and their phialoconidial development. Phytopath Z 112: 229-237.
63. Jarvis WR (1977) Botryotinia and Botrytis Species: Taxonomy, Physiology and Pathogenicity. A Guide to the Literature. Canadian Department of Agriculture, Ottawa. pp. 38-39.
64. Ruger-Herreros C, Rodríguez-Romero J, Fernández-Barranco R, Olmedo M, Fischer R, et al. (2011) Regulation of conidiation by light in Aspergillus nidulans. Genetics 188: 809-822.
65. Fuller KK, Ringelberg CS, Loros JJ, Dunlap JC, (2013) The fungal pathogen Aspergillus fumigatus regulates growth, metabolism, and stress resistance in response to light. MBio 4: e00142-13.
66. Schumacher J, (2012) Tools for Botrytis cinerea: new expression vectors make the gray mold fungus more accessible to cell biology approaches. Fungal Genet Biol 49: 483-497.
67. Heintzen C, Loros JJ, Dunlap JC, (2001) The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 104: 453-464.
68. Schwerdtfeger C, Linden H, (2003) VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation. EMBO J 22: 4846-4855.
69. Doss RP, Deisenhofer J, Krug von Nidda HA, Soeldner AH, McGuire RP, (2003) Melanin in the extracellular matrix of germlings of Botrytis cinerea. Phytochemistry 63: 687-691.
70. Zeun R, Buchenauer H, (1985) Effect of tricyclazole on production and melanin contents of sclerotia of Botrytis cinerea. Phytopathol Z 112: 259-267.
71. Gao Q, Garcia-Pichel F, (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9: 791-802.
72. Strobel I, Breitenbach J, Scheckhuber CQ, Osiewacz HD, Sandmann G, (2009) Carotenoids and carotenogenic genes in Podospora anserina: engineering of the carotenoid composition extends the life span of the mycelium. Curr Genet 55: 175-184.
73. Schwarzländer M, Fricker MD, Müller C, Marty L, Brach T, et al. (2008) Confocal imaging of glutathione redox potential in living plant cells. J Microsc 231: 299-316.
74. Rhoads DM, Subbaiah CC, (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7: 177-194.
75. Duarte M, Videira A, (2009) Effects of mitochondrial complex III disruption in the respiratory chain of Neurospora crassa. Mol Microbiol 72: 246-258.
76. Sellem CH, Marsy S, Boivin A, Lemaire C, Sainsard-Chanet A, (2007) A mutation in the gene encoding cytochrome c1 leads to a decreased ROS content and to a long-lived phenotype in the filamentous fungus Podospora anserina. Fungal Genet Biol 44: 648-658.
77. Grahl N, Dinamarco TM, Willger SD, Goldman GH, Cramer RA, (2012) Aspergillus fumigatus mitochondrial electron transport chain mediates oxidative stress homeostasis, hypoxia responses and fungal pathogenesis. Mol Microbiol 84: 383-399.
78. Dufour E, Boulay J, Rincheval V, Sainsard-Chanet A, (2000) A causal link between respiration and senescence in Podospora anserina. Proc Natl Acad Sci USA 97: 4138-4143.
79. Magnani T, Soriani FM, Martins VP, Nascimento AM, Tudella VG, et al. (2007) Cloning and functional expression of the mitochondrial alternative oxidase of Aspergillus fumigatus and its induction by oxidative stress. FEMS Microbiol Lett 271: 230-238.
80. Honda Y, Hattori T, Kirimura K, (2012) Visual expression analysis of the responses of the alternative oxidase gene (aox1) to heat shock, oxidative, and osmotic stresses in conidia of citric acid-producing Aspergillus niger. J Biosci Bioeng 113: 338-342.
81. Yukioka H, Inagaki S, Tanaka R, Katoh K, Miki N, et al. (1998) Transcriptional activation of the alternative oxidase gene of the fungus Magnaporthe grisea by a respiratory-inhibiting fungicide and hydrogen peroxide. Biochim Biophys Acta 1442: 161-169.
82. Martins VP, Dinamarco TM, Soriani FM, Tudella VG, Oliveira SC, et al. (2011) Involvement of an alternative oxidase in oxidative stress and mycelium-to-yeast differentiation in Paracoccidioides brasiliensis. Eukaryot Cell 10: 237-248.
83. Borghouts C, Scheckhuber CQ, Stephan O, Osiewacz HD, (2002) Copper homeostasis and aging in the fungal model system Podospora anserina: differential expression of PaCtr3 encoding a copper transporter. Int J Biochem Cell Biol 34: 1355-1371.
84. Stumpferl SW, Stephan O, Osiewacz HD, (2004) Impact of a disruption of a pathway delivering copper to mitochondria on Podospora anserina metabolism and life span. Eukaryot Cell 3: 200-211.
85. Avila-Adame C, Köller W, (2002) Disruption of the alternative oxidase gene in Magnaporthe grisea and its impact on host infection. Mol Plant Microbe Interact 15: 493-500.
86. Magnani T, Soriani FM, Martins Vde P, Policarpo AC, Sorgi CA, et al. (2008) Silencing of mitochondrial alternative oxidase gene of Aspergillus fumigatus enhances reactive oxygen species production and killing of the fungus by macrophages. J Bioenerg Biomembr 40: 631-636.
87. Lorin S, Dufour E, Boulay J, Begel O, Marsy S, et al. (2001) Overexpression of the alternative oxidase restores senescence and fertility in a long-lived respiration-deficient mutant of Podospora anserina. Mol Microbiol 42: 1259-1267.
88. Scheckhuber CQ, Houthoofd K, Weil AC, Werner A, De Vreese A, et al. (2011) Alternative oxidase dependent respiration leads to an increased mitochondrial content in two long-lived mutants of the aging model Podospora anserina. PLoS One 6: e16620.
89. Schwarzländer M, Fricker MD, Sweetlove LJ, (2009) Monitoring the in vivo redox state of plant mitochondria: effect of respiratory inhibitors, abiotic stress and assessment of recovery from oxidative challenge. Biochim Biophys Acta 1787: 468-475.
90. Butow RA, Avadhani NG, (2004) Mitochondrial signaling: the retrograde response. Mol Cell 14: 1-15.
91. Staats M, van Kan JA, (2012) Genome update of Botrytis cinerea strains B05.10 and T4. Eukaryot Cell 11: 1413-1414.
92. Pontecorvo GV, Roper JA, Hemmons LM, MacDonald KD, Bufton AWJ, (1953) The genetics of Aspergillus nidulans. Adv Genet 5: 141-238.
93. Cenis JL, (1992) Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Res 20: 2380.
94. Siewers V, Smedsgaard J, Tudzynski P, (2004) The P450 monooxygenase BcABA1 is essential for abscisic acid biosynthesis in Botrytis cinerea. Appl Environ Microbiol 70: 3868-3876.
95. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
96. Temme N, Tudzynski P, (2009) Does Botrytis cinerea ignore H(2)O(2)-induced oxidative stress during infection? Characterization of Botrytis activator protein 1. Mol Plant Microbe Interact 22: 987-998.
97. Doehlemann G, Berndt P, Hahn M, (2006) Different signalling pathways involving a Galpha protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol Microbiol 59: 821-835.
98. Roca MG, Weichert M, Siegmund U, Tudzynski P, Fleissner A, (2012) Germling fusion via conidial anastomosis tubes in the grey mould Botrytis cinerea requires NADPH oxidase activity. Fungal Biol 116: 379-387.
99. Simon A, Biot E, (2010) ANAIS: Analysis of NimbleGen Arrays Interface. Bioinformatics 26: 2468-2469.
100. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
101. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
102. Sturn A, Quackenbush J, Trajanoski Z, (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18: 207-208.