The genome of Botrytis cinerea, a ubiquitous broad host range necrotroph

Genomics of Plant-Associated Fungi and Oomycetes: Dicot Pathogens

Volumn , Issue , 2014, Pages 19-44

  Hahn, Matthias ^a   Viaud, Muriel ^b   Van Kan, Jan ^c  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

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

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84929158839     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-662-44056-8_2     Document Type: Chapter

References (155)

1. Agger S, Lopez-Gallego F, Schmidt-Dannert C (2009) Diversity of sesquiterpene synthases in the basidiomycete Coprinus cinereus. Mol Microbiol 72:1181-1195
2. Aguileta G, Lengelle J, Chiapello H, Giraud T, Viaud M, Fournier E, Rodolphe F, Marthey S, Ducasse A, Gendrault A, Poulain J, Wincker P, Gout L (2012) Genes under positive selection in a model plant pathogenic fungus, Botrytis. Infect Genet Evol 12:987-996
3. Amoutzias GD, He Y, Lilley KS, van de Peer Y, Oliver SG (2012) Evaluation and properties of the budding yeast phosphoproteome. Mol Cell Proteom 11(M111):009555
4. Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP, Couloux A, Coutinho PM, de Vries RP, Dyer PS, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L, Lapalu N, Plummer KM, Pradier JM, Quévillon E, Sharon A, Simon A, ten Have A, Tudzynski B, Tudzynski P, Wincker P, Andrew M, Anthouard V, Beever RE, Beffa R, Benoit I, Bouzid O, Brault B, Chen Z, Choquer M, Collémare J, Cotton P, Danchin EG, Da Silva C, Gautier A, Giraud C, Giraud T, Gonzalez C, Grossetete S, Güldener U, Henrissat B, Howlett BJ, Kodira C, Kretschmer M, Lappartient A, Leroch M, Levis C, Mauceli E, Neuvéglise C, Oeser B, Pearson M, Poulain J, Poussereau N, Quesneville H, Rascle C, Schumacher J, Ségurens B, Sexton A, Silva E, Sirven C, Soanes DM, Talbot NJ, Templeton M, Yandava C, Yarden O, Zeng Q, Rollins JA, Lebrun MH, Dickman M (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7:e1002230
5. Andrew M, Barua R, Short SM, Kohn LM (2012) Evidence for a common toolbox based on necrotrophy in a fungal lineage spanning necrotrophs, biotrophs, endophytes, host generalists and specialists. PLoS ONE 7:e29943
6. Arbelet D, Malfatti P, Simond-Côte E, Fontaine T, Desquilbet L, Expert D, Kunz C, Soulié MC (2010) 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 23:1324-1334
7. Bayram O, Braus GH (2012) Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 36:1-24
8. Bayram Ö, Bayram ÖS, Ahmed YL, Maruyama J, Valerius O, Rizzoli SO, Ficner R, Irniger S, Braus GH (2012) The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet 8:e1002816
9. Billon-Grand G, Rascle C, Droux M, Rollins JA, Poussereau N (2010) pH modulation differs during sunflower cotyledon colonization by the two closely related necrotrophic fungi Botrytis cinerea and Sclerotinia sclerotiorum. Mol Plant Pathol 13:568-578
10. Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21-32
11. Brito N, Espino JJ, González C (2006) The endo-beta-1,4-xylanase Xyn11A is required for virulence in Botrytis cinerea. Mol Plant-Microbe Interact 19:25-32
12. Bushley KE, Turgeon BG (2010) Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol 10:26
13. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrateactive EnZymes database (CAZy): an expert resource for glycogenomics. Nucl Acids Res 37:D233-D238
14. Cettul E, Rekab D, Locci R, Firrao G (2008) Evolutionary analysis of endopolygalacturonase-encoding genes of Botrytis cinerea. Mol Plant Pathol 9:675-685
15. 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 64:85-100
16. Chitrampalam P, Inderbitzin P, Maruthachalam K, Wu BM, Subbarao KV (2013) The Sclerotinia sclerotiorum mating type locus (MAT) contains a 3.6-kb region that is inverted in every meiotic generation. PLoS ONE 8:e56895
17. Choquer M, Fournier E, Kunz C, Levis C, Pradier JM, Simon A, Viaud M (2007) Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol Lett 277:1-10
18. Ciuffetti LM, Manning VA, Pandelova I, Betts MF, Martinez JP (2010) Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol 187:911-919
19. Collado G, Aleu J, Hernandez-Galan R, Duran-Patron R (2000) Botrytis species: an intriguing source of metabolites with a wide range of biological activities. Structure, chemistry and bioactivity of metabolites isolated from Botrytis species. Curr Organ Chem 4:1261-1286
20. Colmenares AJ, Aleu J, Duran-Patron R, Collado IG, Hernandez-Galan R (2002) The putative role of botrydial and related metabolites in the infection mechanism of Botrytis cinerea. J Chem Ecol 28:997-1005
21. Cuesta Arenas Y, Kalkman E, Schouten A, Dieho M, Vredenbregt P, Uwumukiza B, Osés Ruiz M, van Kan JAL (2010) Functional analysis and mode of action of phytotoxic Nep1-like proteins of Botrytis cinerea. Physiol Mol Plant Pathol 74:376-386
22. Dalmais B, Schumacher J, Moraga J, Le Pêcheur P, Tudzynski B, Collado IG, Viaud M (2011) The Botrytis cinerea phytotoxin botcinic acid requires two polyketide synthases for production and has a redundant role in virulence. Mol Plant Pathol 12:564-579
23. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414-430
24. Debieu D, Bach J, Montesinos E, Fillinger S, Leroux P (2013) Role of sterol 3-ketoreductase sensitivity in susceptibility to the fungicide fenhexamid in Botrytis cinerea and other phytopathogenic fungi. Pest Manag Sci 69:642-651
25. Dickman MB, Park YK, Oltersdorf T, Li W, Clemente T, French R (2001) Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci USA 98:6957-6962
26. 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
27. Espino JJ, Gutierrez-Sanchez G, Brito N, Shah P, Orlando R, Gonzalez C (2010) The Botrytis cinerea early secretome. Proteomics 10:3020-3034
28. Faris JD, Zhang Z, Lu H, Lu SW, Reddy L, Cloutier S, Fellers JP, Meinhardt SW, Rasmussen JB, Xu SS, Oliver RP, Simons KJ, Friesen TL (2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci USA 107:13544-13549
29. Fernandez-Acero JF, Colby T, Harzen A, Cantoral JM, Schmidt J (2009) Proteomic analysis of the phytopathogenic fungus Botrytis cinerea during cellulose degradation. Proteomics 9:2892-2902
30. Fernandez-Acero JF, Colby T, Harzen A, Carbu M, Wieneke U, Cantoral JM, Schmidt J (2010) 2-DE proteomic approach to the Botrytis cinerea secretome induced with different carbon sources and plant-based elicitors. Proteomics 10:2270-2280
31. Fernández-Álvarez A, Elías-Villalobos A, Ibeas JI (2009) The O-mannosyltransferase PMT4 Is essential for normal appressorium formation and penetration in Ustilago maydis. Plant Cell 21:3397-3412
32. Fernández-Álvarez A, Marín-Menguiano M, Lanver D, Jiménez-Martín A, Elías-Villalobos A, Pérez-Pulido AJ, Kahmann R, Ibeas JI (2012) Identification of Omannosylated virulence factors in Ustilago maydis. PLoS Pathog 8:e1002563
33. 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
34. Fournier E, Giraud T, Loiseau A, Vautrin D, Estoup A, Solignac M, Cornuet JM, Brygoo Y (2002) Characterization of nine polymorphic microsatellite loci in the fungus Botrytis cinerea (Ascomycota). Mol Ecol Notes 2:253-255
35. Fournier E, Giraud T, Albertini C, Brygoo Y (2005) Partition of the Botrytis cinerea complex in France using multiple gene genealogies. Mycologia 97:1251-1267
36. Fournier E, Giraudn T (2008) Sympatric genetic differentiation of a generalist pathogenic fungus, Botrytis cinerea, on two different host plants, grapevine and bramble. J Evol Biol 21:122-132
37. Frías M, González C, Brito N (2011) BcSpl1, a ceratoplatanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytol 192:483-495
38. Frías M, Brito N, González C (2013) The Botrytis cinerea cerato-platanin BcSpl1 is a potent inducer of systemic acquired resistance (SAR) in tobacco and generates a wave of salicylic acid expanding from the site of application. Mol Plant Pathol 14:191-196
39. Giesbert S, Schumacher J, Kupas V, Espino J, Segmüller N, Haeuser-Hahn I, Schreier PH, Tudzynski P (2012) Identification of pathogenesis-associated genes by TDNA-mediated insertional mutagenesis in Botrytis cinerea: a type 2A phosphoprotein phosphatase and an SPT3 transcription factor have significant impact on virulence. Mol Plant-Microbe Interact 25:481-495
40. Gioti A, Simon A, Le Pêcheur P, Giraud C, Pradier JM, Viaud M, Levis C (2006) Expression profiling of Botrytis cinerea genes identifies three patterns of upregulation in planta and an FKBP12 protein affecting pathogenicity. J Mol Biol 358:372-386
41. 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
42. Giraud T, Fortini D, Levis C, Lamarque C, Leroux P, LoBuglio K, Brygoo Y (1999) Two sibling species of the Botrytis cinerea complex, transposa and vacuma, are found in sympatry on numerous host plants. Phytopathology 89:967-973
43. González M, Brito N, González C (2012) High abundance of Serine/Threonine-rich regions predicted to be hyper-O-glycosylated in the secretory proteins coded by eight fungal genomes. BMC Microbiol 12:213
44. Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751-757
45. González M, Brito N, Frias M, Gonzalez C (2013) Botrytis cinerea protein O-mannosyltransferases play critical roles in morphogenesis, growth, and virulence. PLos One 8(6):e65924
46. Gourgues M, Brunet-Simon A, Lebrun MH, Levis C (2004) The tetraspanin BcPls1 is required for appressorium-mediated penetration of Botrytis cinerea into host plant leaves. Mol Microbiol 51:619-629
47. Grant-Downton R, Terhem RA, Kapralov MV, Mehdi S, Rodriguez-Enriquez MJ, Gurr SJ, van Kan JAL, Dewey FM (2013) A novel Botrytis species is associated with a newly emergent foliar disease in cultivated Hemerocallis (Submitted for publication)
48. Han Y, Joosten HJ, Niu W, Zhao Z, Mariano PS, McCalman M, van Kan J, Schaap PJ, Dunaway- Mariano D (2007) Oxaloacetate hydrolase, the C-C bond lyase of oxalate secreting fungi. J Biol Chem 282:9581-9590
49. Hargreaves JA, Mansfield JW, Rossall S (1977) Changes in phytoalexin concentrations in tissues of the broad bean plant (Vicia faba L.) following inoculation with species of Botrytis. Physiol Plant Pathol 11:227-242
50. Harrison JG (1980) The production of toxins by Botrytis fabae in relation to growth of lesions on bean leaves at different humidities. Ann Appl Biol 95:63-72
51. ten Have A, Mulder W, Visser J, van Kan JAL (1998) The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol Plant-Microbe Interact 11:1009-1016
52. ten Have A, Espino JJ, Dekkers E, van Sluyter SC, Brito N, Kay J, González C, van Kan JA (2010) The Botrytis cinerea aspartic proteinase family. Fungal Genet Biol 47:53-65
53. Heller J, Meyer AJ, Tudzynski P (2012a) 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
54. Heller J, Ruhnke N, Espino JJ, Massaroli M, Collado IG, Tudzynski P (2012b) The mitogen-activated protein 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
55. Hoffmeister D, Keller NP (2007) Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24:393-416
56. Kars I, McCalman M, Wagemakers L, van Kan JA (2005a) Functional analysis of Botrytis cinerea pectin methylesterase genes by PCR-based targeted mutagenesis: Bcpme1 and Bcpme2 are dispensable for virulence of strain B05.10. Mol Plant Pathol 6:641-652
57. Kars I, Krooshof G, Wagemakers CAM, Joosten R, Benen JAE, van Kan JAL (2005b) Necrotising activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Plant J 43:213-225
58. Kerssies A, Bosker-van Zessen AI (1997) Variation in pathogenicity and DNA polymorphism among Botrytis cinerea isolates sampled inside and outside a glasshouse. Plant Dis 81:781-786
59. Krappmann S, Bayram Ö, Braus GH (2005) Deletion and allelic exchange of the Aspergillus fumigatus veA locus via a novel recyclable marker module. Eukaryot Cell 4:1298-1307
60. Kretschmer M, Hahn M (2008) Fungicide resistance and genetic diversity of Botrytis cinerea isolates from a vineyard in Germany. J Plant Dis Protect 115:214-219
61. Kretschmer M, Leroch M, Mosbach A, Walker AS, Fillinger S, Mernke D, Schoonbeek HJ, Pradier JM, Leroux P, De Waard MA, Hahn M (2009) Fungicidedriven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog 5:e1000696
62. 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
63. Kunz C, Vandelle E, Rolland S, Poinssot B, Bruel C, Cimerman A, Zotti C, Moreau E, Vedel R, Pugin A, Boccara M (2006) Characterization of a new, nonpathogenic mutant of Botrytis cinerea with impaired plant colonization capacity. New Phytol 170:537-550
64. Lanver D, Mendoza-Mendoza A, Brachmann A, Kahmann R (2010) Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell 22:2085-2101
65. Leroch M, Kleber A, Silva E, Coenen T, Koppenhöfer D, Shmaryahu A, Valenzuela PD, Hahn M (2013a) Transcriptome profiling of Botrytis cinerea conidial germination reveals upregulation of infection-related genes during the pre-penetration stage. Eukaryot Cell 12:614-626
66. Leroch M, Plesken C, Weber RW, Kauff F, Scalliet G, Hahn M (2013b) 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 79:159-167
67. Leroch M, Mernke D, Koppenhoefer D, Schneider P, Mosbach A, Doehlemann G, Hahn M (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
68. Li X, Kerrigan J, Chai W, Schnabel G (2012a) Botrytis caroliniana, a new species isolated from blackberry in South Carolina. Mycologia 104:650-658
69. Li B, Wang W, Zong Y, Qin G, Tian S (2012b) Exploring pathogenic mechanisms of Botrytis cinerea Secretome under different ambient pH based on comparative proteomic analysis. J Proteome Res 11:4249-4260
70. Liu W, Zhou X, Li G, Li L, Kong L, Wang C, Zhang H, Xu JR (2011a) Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog 7:e1001261
71. 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 phenylpyrroleresistance. Fungal Genet Biol 45:1062-1074
72. Liu W, Soulié MC, Perrino C, Fillinger S (2011b) The osmosensing signal transduction pathway from Botrytis cinerea regulates cell wall integrity and MAP kinase pathways control melanin biosynthesis with influence of light. Fungal Genet Biol 48:377-387
73. Manteau S, Abouna S, Lambert B, Legendre L (2003) Differential regulation by ambient pH of putative virulence factor secretion by the phytopathogenic fungus Botrytis cinerea. FEMS Microbiol Ecol. 43:359-366
74. Martinez F, Blancard D, Lecomte P, Levis C, Dubos B, Fermaud M (2003) Phenotypic differences between vacuma and transposa subpopulations of Botrytis cinerea. Eur J Plant Pathol 109:479-488
75. Martinez F, Dubos B, Fermaud M (2005) The role of saprotrophy and virulence in the population dynamics of Botrytis cinerea in vineyards. Phytopathology 95:692-700
76. Massaroli M, Moraga J, Bastos Borges K, Ramirez- Fernández J, Viaud M, González Collado I, Durán- Patrón R, Hernández-Galán R (2013) A shared biosynthetic pathway for botcinins and botrylactones revealed through gene deletions. Chem Bio 14:132-136
77. Mengiste T (2012) Plant immunity to necrotrophs. Annu Rev Phytopathol. 50:267-294
78. Michielse CB, Becker M, Heller J, Moraga J, Collado IG, Tudzynski P (2011) The Botrytis cinerea Reg1 protein, a putative transcriptional regulator, is required for pathogenicity, conidiogenesis, and the production of secondary metabolites. Mol Plant Microbe Interact 24:1074-1085
79. Morcx S, Kunz C, Choquer M, Assie S, Blondet E, Simond-Côte E, Gajek K, Chapeland-Leclerc F, Expert D, Soulie MC (2013) Disruption of Bcchs4, Bcchs6 or Bcchs7 chitin synthase genes in Botrytis cinerea and the essential role of class VI chitin synthase (Bcchs6). Fungal Genet Biol 52:1-8
80. Morschhäuser J (2010) Regulation of multidrug resistance in pathogenic fungi. Fungal Genet Biol 47:94-106
81. Mosbach A, Leroch M, Mendgen KW, Hahn M (2011) Lack of evidence for a role of hydrophobins in conferring surface hydrophobicity to conidia and hyphae of Botrytis cinerea. BMC Microbiol 11:10
82. Moyano C, Alfonso C, Gallegro J, Raposo R, Melgarejo P (2003) Comparison of RAPD and AFLP marker analysis as a means to study the genetic structure of Botrytis cinerea populations. Eur J Plant Pathol 109:515-522
83. Nielsen K, Yohalam DS (2001) Origin of a polyploidy Botrytis pathogen through interspecific hybridization between Botrytis aclada and Botrytis byssoidea. Mycologie 93:1064-1071
84. Nguyen QB, Itoh K, Van Vu B, Tosa Y, Nakayashiki H (2011) Simultaneous silencing of endo-b-1,4 xylanase genes reveals their roles in the virulence of Magnaporthe oryzae. Mol Microbiol 81:1008-1019
85. Noda J, Brito N, González C (2010) The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biol 10:38
86. Oliver RP, Solomon PS (2010) New developments in pathogenicity and virulence of necrotrophs. Curr Opin Plant Biol 13:415-419
87. Pihet M, Vandeputte P, Tronchin G, Renier G, Saulnier P, Georgeault S, Mallet R, Chabasse D, Symoens F, Bouchara JP (2009) Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol 9:177
88. Pinedo C, Wang CM, Pradier JM, Dalmais B, Choquer M, Le Pêcheur P, Morgant G, Collado IG, Cane DE, Viaud M (2008) Sesquiterpene synthase from the botrydial biosynthetic gene cluster of the phytopathogen Botrytis cinerea. ACS Chem Biol 3:791-801
89. 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
90. Quidde T, Osbourn AE, Tudzynski P (1998) Detoxification of a-tomatine by Botrytis cinerea. Physiol Mol Plant Pathol 52:151-165
91. RajaguruShaw P, Shaw M (2010) Genetic differentiation between hosts and locations in populations of latent Botrytis cinerea in southern England. Plant Pathol 59:1081-1090
92. Rampitsch C, Tinker NA, Subramaniam R, Barkow- Oesterreicher S, Laczko E (2012) Phosphoproteome profile of Fusarium graminearum grown in vitro under nonlimiting conditions. Proteomics 12:1002-1005
93. Reis H, Pfiffi S, Hahn M (2005) Molecular and functional characterization of a secreted lipase from Botrytis cinerea. Mol Plant Pathol 6:257-267
94. Rolke Y, Liu S, Quidde T, Williamson B, Schouten A, Weltring KM, Siewers V, Tenberge KB, Tudzynski B, Tudzynski P (2004) Functional analysis of H(2)O(2)-generating systems in Botrytis cinerea: the major Cu-Zn-superoxide dismutase (BCSOD1) contributes to virulence on French bean, whereas a glucose oxidase (BCGOD1) is dispensable. Mol Plant Pathol 5:17-27
95. Rossall S, Mansfield JW, Hutson RA (1980) Death of Botrytis cinerea and B. fabae following exposure to wyerone derivatives in vitro and during infection development in broad bean leaves. Physiol Plant Pathol 16:135-146
96. Rowe HC, Kliebenstein DJ (2007) Elevated genetic variation within virulence-associated Botrytis cinerea polygalacturonase loci. Mol Plant-Microbe Interact 20:1126-1137
97. Rowe HC, Walley JW, Corwin J, Chan EK, Dehesh K, Kliebenstein DJ (2010) Deficiencies in jasmonatemediated plant defense reveal quantitative variation in Botrytis cinerea pathogenesis. PLoS Pathog 6:e1000861
98. Rowe HC, Kliebenstein DJ (2010) All mold is not alike: the importance of intraspecific diversity in necrotrophic plant pathogens. PLOS Pathog 6:e1000759
99. Rui O, Hahn M (2007) 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 8:173-184
100. Saikia S, Nicholson MJ, Young C, Parker EJ, Scott B (2008) The genetic basis for indole-diterpene chemical diversity in filamentous fungi. Mycol Res 112:184-199
101. Schamber A, Leroch M, Diwo J, Mendgen K, Hahn M (2010) The role of mitogen-activated protein (MAP) kinase signalling components and the Ste12 transcription factor in germination and pathogenicity of Botrytis cinerea. Mol Plant Pathol 11:105-119
102. Schouten A, Wagemakers L, Stefanato FL, van der Kaaij RM, van Kan JA (2002) Resveratrol acts as a natural profungicide and induces self-intoxication by a specific laccase. Mol Microbiol 43:883-894
103. Schumacher J, Kokkelink L, Huesmann C, Jimenez-Teja D, Collado IG, Barakat R, Tudzynski P, Tudzynski B (2008a) The cAMP-dependent signaling pathway and its role in conidial germination, growth, and virulence of the gray mold Botrytis cinerea. Mol Plant-Microbe Interact 21:1443-1459
104. Schumacher J, Viaud M, Simon A, Tudzynski B (2008b) The Ga subunit BCG1, the phospholipase C (BcPLC1), and the calcineurin phosphatase coordinately regulate gene expression in the grey mold fungus Botrytis cinerea. Mol Microbiol 67:1027-1050
105. Schumacher J, de Larrinoa IF, Tudzynski B (2008c) 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
106. Schumacher J, Pradier JM, Simon A, Traeger S, Moraga J, González Collado I, Viaud M, Tudzynski B (2012) Natural variation in the VELVET gene bcvel1 affects virulence and light-dependent differentiation in Botrytis cinerea. PLoS One 7:e47840
107. 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
108. Schumacher J, Gautier A, Morgant G, Le Pêcheur P, Azeddine S, Fillinger S, Leroux P, Tudzynski B, Viaud M (2013) A functional bikaverin biosynthetic gene cluster in rare isolates of Botrytis cinerea is positively regulated by the Velvet complex PLoS One 8:e53729
109. Schulze Gronover C, Schorn C, Tudzynski B (2004) Identification of Botrytis cinerea genes up-regulated during infection and controlled by the Galpha subunit BCG1 using suppression subtractive hybridization (SSH). Mol Plant-Microbe Interact 17:537-546
110. Shah P, Gutierrez-Sanchez G, Orlando R, Bergmann C (2009) A proteomic study of pectin-degrading enzymes secreted by Botrytis cinerea grown in liquid culture. Proteomics 9:3126-3135
111. Shah P, Powell ALT, Orlando R, Bergmann C, Gutierrez-Sanchez G (2012) Proteomic analysis of ripening tomato fruit infected by Botrytis cinerea. J Proteome Res 11:2178-2192
112. Shipunov A, Newcombe G, Raghavendra AK, Anderson CL (2008) Hidden diversity of endophytic fungi in an invasive plant. Am J Bot 95:1096-1108
113. Siegmund U, Heller J, van Kan JA, Tudzynski P (2013) The NADPH oxidase complexes in Botrytis cinerea: Evidence for a close association with the ER and the tetraspanin Pls1. PLoS One 8:e55879
114. Shlezinger N, Minz A, Gur Y, Hatam I, Dagdas YF, Talbot NJ, Sharon A (2011a) Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PLoS Pathog 7:e1002185
115. Shlezinger N, Doron A, Sharon A (2011b) Apoptosis-like programmed cell death in the grey mould fungus Botrytis cinerea: genes and their role in pathogenicity. Biochem Soc Trans 39:1493-1498
116. Siewers V, Viaud M, Jimenez-Teja D, Collado IG, Gronover CS, Pradier JM, Tudzynski B, Tudzynski P (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
117. Siewers V, Kokkelink L, Smedsgaard J, Tudzynski P (2006) Identification of an abscisic acid gene cluster in the grey mold Botrytis cinerea. Appl Environ Microbiol 72:4619-4626
118. Simon A, Dalmais B, Morgant G, Viaud M (2013) Screening of a Botrytis cinerea one-hybrid library reveals a Cys2His2 transcription factor involved in the regulation of secondary metabolism gene clusters. Fung Genet Biol 52:9-19
119. Sowley ENK, Dewey FM, Shaw MW (2010) Persistent, symptomless, systemic, and seed-borne infection of lettuce by Botrytis cinerea. Eur J Plant Pathol 126:61-71
120. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stüber K, Loren Ver, van Themaat E, Brown JK, Butcher SA, Gurr SJ, Lebrun MH, Ridout CJ, Schulze-Lefert P, Talbot NJ, Ahmadinejad N, Ametz C, Barton GR, Benjdia M, Bidzinski P, Bindschedler LV, Both M, Brewer MT, Cadle-Davidson L, Cadle-Davidson MM, Collemare J, Cramer R, Frenkel O, Godfrey D, Harriman J, Hoede C, King BC, Klages S, Kleemann J, Knoll D, Koti PS, Kreplak J, López-Ruiz FJ, Lu X, Maekawa T, Mahanil S, Micali C, Milgroom MG, Montana G, Noir S, O'Connell RJ, Oberhaensli S, Parlange F, Pedersen C, Quesneville H, Reinhardt R, Rott M, Sacristán S, Schmidt SM, Schön M, Skamnioti P, Sommer H, Stephens A, Takahara H, Thordal-Christensen H, Vigouroux M, Wessling R, Wicker T, Panstruga R (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543-1546
121. Staats M, van Baarlen P, van Kan JA (2005) Molecular phylogeny of the plant pathogenic genus Botrytis and the evolution of host specificity. Mol Biol Evol 22:333-346
122. Staats M, van Baarlen P, Schouten A, van Kan JA, Bakker FT (2007a) Positive selection in phytotoxic protein-encoding genes of Botrytis species. Fungal Genet Biol 44:52-63
123. Staats M, van Baarlen P, Schouten A, van Kan JA (2007b) Functional analysis of NLP genes from Botrytis elliptica. Mol Plant Pathol 8:209-214
124. Staats M, van Kan JA (2012) Genome update of Botrytis cinerea strains B05.10 and T4. Eukaryot Cell 11:1413-1414
125. Stefanato FL, Abou-Mansour E, Buchala A, Kretschmer M, Mosbach A, Hahn M, Bochet CG, Métraux JP, Schoonbeek HJ (2009) The ABC transporter BcatrB from Botrytis cinerea exports camalexin and is a virulence factor on Arabidopsis thaliana. Plant J 58:499-510
126. Stergiopoulos I, Collemare J, Mehrabi R, de Wit PJGM (2013) Phytotoxic secondary metabolites and peptides produced by plant pathogenic Dothideomycete fungi. FEMS Microbiol Rev 37:67-93
127. Sutherland A, Auclair K, Vederas JC (2001) Recent advances in the biosynthetic studies of lovastatin. Curr Opin Drug Discov Devel 4:229-236
128. Tan K-C, Oliver RP, Solomon PS, Moffat CS (2010) Proteinaceaous necrotropic effectors in fungal virulence. Funct Plant Biol 37:907-912
129. Tan K-C, Ferguson-Hunt M, Rybak K, Waters ODC, Bond CS, Stukenbrock EH, Friesen TL, Faris JD, McDonald BA, Oliver RP (2012) Quantitative variation in effector activity of ToxA isoforms from Stagonospora nodorum and Pyrenophora tritici-repentis. Mol Plant-Microbe Interact 25:515-522
130. Tani H, Koshino H, Sakuno E, Cutler HG, Nakajima H (2006) Botcinins E and F and botcinolide from Botrytis cinerea and structural revision of botcinolides. J Nat Prod 69:722-725
131. 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
132. Temme N, Oeser B, Massaroli M, Heller J, Simon A, González Collado I, Viaud M, Tudzynski P (2012) BcAtf1- A global regulator controls various differentiation processes and phytotoxin production in Botrytis cinerea. Mol Plant Pathol 3:704-718
133. Tenberge KB (2004) Morphology and cellular organization in Botrytis interaction with plants. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds) Botrytis: biology, pathology and control. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 67-84
134. Valette-Collet O, Cimerman A, Reignault P, Levis C, Boccara M (2003) Disruption of Botrytis cinerea pectin methylesterase gene Bcpme1 reduces virulence on several host plants. Mol Plant-Microbe Interact 16:360-367
135. van Baarlen P, Staats M, van Kan JAL (2004) Induction of programmed cell death in lily by the fungal pathogen Botrytis elliptica. Mol Plant Pathol 5:559-574
136. van Baarlen P, Woltering EJ, Staats M, van Kan JAL (2007) Histochemical and genetic analysis of host and non-host interactions of Arabidopsis with three Botrytis species: an important role for cell death control. Mol Plant Pathol 8:41-54
137. van Kan JA (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247-253
138. Van Vu B, Itoh K, Nguyen QB, Tosa Y, Nakayashiki H (2012) Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Mol Plant-Microbe Interact 25:1135-1141
139. Viaud M, Brunet-Simon A, Brygoo Y, Pradier JM, Levis C (2003) Cyclophilin A and calcineurin functionsinvestigated by gene inactivation, cyclosporin A inhibition and cDNA arrays approaches in the phytopathogenic fungus Botrytis cinerea. Mol Microbiol 50:1451-1465
140. Viaud M, Fillinger S, Liu W, Polepalli JS, Le Pêcheur 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 19:1042-1050
141. Villen J, Gygi SP (2008) The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat Protoc 3:1630-1638
142. Vogt K, Bhabhra R, Rhodes JC, Askew DS (2005) Doxycycline-regulated gene expression in the opportunistic fungal pathogen Aspergillus fumigatus. BMC Microbiol 5:1
143. Walker AS, Gautier AL, Confais J, Martinho D, Viaud M, Le P, Cheur P, Dupont J, Fournier E (2011) Botrytis pseudocinerea, a new cryptic species causing gray mold in French vineyards in sympatry with Botrytis cinerea. Phytopathology 101:1433-1445
144. De Waard MA, Andrade AC, Hayashi K, Schoonbeek HJ, Stergiopoulos I, Zwiers LH (2006) Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Manag Sci 62:195-207
145. Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I, Huang HD, Jin H (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118-123
146. Williamson B, Tudzynski B, Tudzynski P, van Kan JAL (2007) Pathogen profile-Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561-580
147. Williams B, Kabbage M, Kim HJ, Britt R, Dickman MB (2011) Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog 7(6):e1002107
148. Windram O, Madhou P, McHattie S, Hill C, Hickman R, Cooke E, Jenkins DJ, Penfold CA, Baxter L, Breeze E, Kiddle SJ, Rhodes J, Atwell S, Kliebenstein DJ, Kim YS, Stegle O, Borgwardt K, Zhang C, Tabrett A, Legaie R, Moore J, Finkenstadt B, Wild DL, Mead A, Rand D, Beynon J, Ott S, Buchanan-Wollaston V, Denby KJ (2012) Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24:3530-3537
149. Wong Sak Hoi J, Dumas B (2010) Ste12 and Ste12-like proteins, fungal transcription factors regulating development and pathogenicity. Eukaryot Cell 9:480-485
150. Yin W, Keller NP (2011) Transcriptional regulatory elements in fungal secondary metabolism. J Microbiol 49:329-339
151. Yang Q, Yan L, Gu Q, Ma Z (2012) The mitogenactivated protein kinase kinase kinase BcOs4 is required for vegetative differentiation and pathogenicity in Botrytis cinerea. Appl Microbiol Biotechnol 96:481-492
152. Yan L, Yang Q, Jiang J, Michailides TJ, Ma Z (2011) Involvement of a putative response regulator Brrg-1 in the regulation of sporulation, sensitivity to fungicides, and osmotic stress in Botrytis cinerea. Appl Microbiol Biotechnol 90:215-226
153. Yan L, Yang Q, Sundin GW, Li H, Ma Z (2010) The mitogen-activated protein kinase kinase BOS5 is involved in regulating vegetative differentiation and virulence in Botrytis cinerea. Fungal Genet Biol 47:753-760
154. Zhang J, Wu MD, Li GQ, Yang L, Yu L, Jiang DH, Huang HC, Zhuang WY (2010a) Botrytis fabiopsis, a new species causing chocolate spot of broad bean in central China. Mycologia 102:1114-1126
155. Zhang J, Zhang L, Li GQ, Yang L, Jiang DH, Zhuang WY, Huang HC (2010b) Botrytis sinoallii: a new species of the grey mould pathogen on Allium crops in China. Mycoscience 5:421-431