Essential letters in the fungal alphabet: ABC and MFS transporters and their roles in survival and pathogenicity

Advances in Genetics

Volumn 85, Issue , 2014, Pages 201-253

  Perlin, Michael H ^a   Andrews, Jared ^a   Toh, Su San ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

ABC, MFS, sugar, and oligopeptide transporters; Efflux transporters; Fungal multidrug resistance; Pathogenic fungi

Indexed keywords

ABC TRANSPORTER; CARRIER PROTEIN; FUNGAL PROTEIN;

ANTIFUNGAL RESISTANCE; CHEMISTRY; CLASSIFICATION; DRUG EFFECTS; FUNGUS; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY;

ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, FUNGAL; ENVIRONMENTAL MICROBIOLOGY; FUNGAL PROTEINS; FUNGI; MEMBRANE TRANSPORT PROTEINS;

EID: 84901460286     PISSN: 00652660     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800271-1.00004-4     Document Type: Chapter

References (121)

1. Alexander N.J., McCormick S.P., Hohn T.M. TRI12, a trichothecene efflux pump from Fusarium sporotrichioides: Gene isolation and expression in yeast. Molecular Genetics and Genomics 1999, 261:977-984. 10.1007/s004380051046.
2. Amnuaykanjanasin A., Daub M.E. The ABC transporter ATR1 is necessary for efflux of the toxin cercosporin in the fungus Cercosporin nicotianae. Fungal Genetics and Biology 2009, 46:146-158. 10.1016/j.fgb.2008.11.007.
3. Andrade A.C., Del Sorbo G., Van Nistelrooy J.G., Waard M.A. The ABC transporter AtrB from Aspergillus nidulans mediates resistance to all major classes of fungicides and some natural toxic compounds. Microbiology 2000, 146:1987-1997.
4. Becker J.M., Henry L.K., Jiang W., Koltin Y. Reduced virulence of Candida albicans mutants affected in multidrug resistance. Infection and Immunity 1995, 63:4515-4518. 10.1111/j.1365-2958.2005.04576.x.
5. Biswas K., Morschhäuser J. The Mep2p ammonium permease controls nitrogen starvation-induced filamentous growth in Candida albicans. Molecular Microbiology 2005, 56:649-669. 10.1111/j.1365-2958.2005.04576.x.
6. Brown D.W., McCormick S.P., Alexander N.J., Proctor R.H., Desjardins A.E. A genetic and biochemical approach to study trichothecene diversity in Fusarium sporotrichioides and Fusarium graminearum. Fungal Genetics and Biology 2001, 32:121-133. 10.1006/fgbi.2001.1256.
7. Brown V., Sexton J.A., Johnston M. A glucose sensor in Candida albicans. Eukaryotic Cell 2006, 5:1726-1737.
8. Cannon R.D., Lamping E. Efflux-mediated antifungal drug resistance. Clinical Microbiological Reviews 2009, 22:291-321. 10.1128/CMR.00051-08.
9. Cardoza R.E., Malmierca M.G., Hermosa M.R., Alexander N.J., McCormick S.P., Proctor R.H., et al. Identification of loci and functional characterization of trichothecene biosynthesis genes in filamentous fungi of the genus Trichoderma. Applied and Environmental Microbiology 2011, 77:4867-4877. 10.1128/AEM.00595-11.
10. Casadevall A., Fang F.C., Pirofski L.-a Microbial virulence as an emergent property: Consequences and opportunities. PLoS Pathogens 2011, 7:e1002136. 10.1371/journal.ppat.1002136.
11. Chague F., Maor R., Sharon A. CgOpt1 a putative oligopeptide transporter from Colletotrichum gloeosporioides that is involved in responses to auxin and pathogenicity. BMC Microbiology 2009, 9:173-184. 10.1186/1471-2180-9-173.
12. Choquer M., Lee M.H., Bau H.J., Chung K.R. Deletion of a MFS transporter-like gene in Cercospora nicotianae reduces cercosporin toxin accumulation and fungal virulence. FEBS Letters 2007, 581:489-494.
13. Coleman J.J., Mylonakis E. Efflux in fungi: la pièce de résistance. PLoS Pathogens 2009, 5:e1000486. PMID:19557154. 10.1371/journal.ppat.1000486.
14. Coleman J.J., White G.J., Rodriguez-Carres M., Vanetten H.D. An ABC transporter and a cytochrome P450 of Nectria haematococca MPVI are virulence factors on pea and are the major tolerance mechanisms to the phytoalexin pisatin. Molecular Plant Microbe Interactions 2011, 24:368-376. 10.1094/MPMI-09-10-0198.
15. Damon C., Vallon L., Zimmermann S., Haider M.Z., Galeote V., Dequin S., et al. A novel family of oligopeptide transporters identified by functional metatranscriptomics of soil eukaryotes. ISME Journal 2011, 5:1871-1880. 10.1038/ismej.2011.67.
16. Daub M.E., Herrero S., Chung K.-R. Photoactivated perylenequinone toxins in fungal pathogenesis of plants. FEMS Microbiology Letters 2005, 252:197-206. 10.1016/j.femsle.2005.08.033.
17. Daub M.E., Herrero S., Chung K.-R. Reactive oxygen species in plant pathogenesis: The role of perylenequinone photosensitizers. Antioxidant & Redox Signaling 2013, 19:270-289. 10.1089/ars.2012.5080.
18. Davis M.M., Alvarez F.J., Ryman K., Holm Å.A., Ljungdahl P.O., Engström Y. Wild-type Drosophila melanogaster as a model host to analyze nitrogen source dependent virulence of Candida albicans. PLoS One 2011, 6:e27434. Epub 2011 Nov 14. 10.1371/journal.pone.0027434.
19. Decottignies A., Goffeau A. A complete inventory of the yeast ABC proteins. Nature Genetics 1997, 15:137-145. 10.1038/ng0297-137.
20. Doidy J., Grace E., Kühn C., Simon-Plas F., Casieri L., Wipf D. Sugar transporters in plants and in their interactions with fungi. Trends in Plant Sciences 2012, 17:413-422. 10.1016/j.tplants.2012.03.00.
21. Dreesen T.D., Johnson D.H., Henikoff S. The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes. Molecular and Cellular Biology 1988, 8:5206-5215.
22. Dunkel N., Hertlein T., Franz R., Reuß O., Sasse C., Schäfer T., et al. Roles of different peptide transporters in nutrient acquisition in Candida albicans. Eukaryotic Cell 2013, 12:520-528. Epub 2013 Feb 2. 10.1128/EC.00008-13.
23. Ehrenhofer-Murray A.E., Wurgler F.E., Sengstag C. The Saccharomyces cerevisiae SGE1 gene product: A novel drug-resistance protein within the major facilitator superfamily. Molecular and General Genetics 1994, 244:287-294.
24. Fernandez J., Wright J.D., Hartline D., Quispe C.F., Madayiputhiya N., Wilson R.A. Principles of carbon catabolite repression in the rice blast fungus: Tps1, Nmr1-3, and a MATE-family pump regulate glucose metabolism during infection. PLoS Genetics 2012, 8:e1002673. 10.1371/journal.pgen.1002673.
25. Fleissner A., Sopalla C., Weltring K.M. An ATP-binding cassette multidrug-resistance transporter is necessary for tolerance of Gibberella pulicaris to phytoalexins and virulence on potato tubers. Molecular Plant Microbe Interactions 2002, 15:102-108. 2002.15.2.102. 10.1094/MPMI.
26. Gaur M., Choudhury D., Prasad R. Complete inventory of ABC proteins in human pathogenic yeast, Candida albicans. Journal of Molecular Microbiology and Biotechnology 2005, 9:3-15. 10.1159/000088141.
27. Gaur M., Puri N., Manoharlal R., Rai V., Mukhopadhayay G., Choudhury D., Prasad R. MFS transportome of the human pathogenic yeast Candida albicans. BMC Genomics 2008, 9:579.
28. Goffeau A., Park J., Paulsen I.T., Jonniaux J.L., Dinh T., Mordant P., et al. Multidrug-resistant transport proteins in yeast: Complete inventory and phylogenetic characterization of yeast open reading frames with the major facilitator superfamily. Yeast 1997, 13:43-54. 1<43::AID-YEA56>3.0.CO;2-J. 10.1002/(SICI)1097-0061(199701)13.
29. Gomolplitinant M., Saier M.H. Evolution of the oligopeptide transporter family. Journal of Membrane Biology 2011, 240:89-110. Epub 2011 Feb 24. 10.1007/s00232-011-9347-9.
30. Gompel-Klein P., Brendel M. Allelism of SNQ1 and ATR1, genes of the yeast Saccharomyces cerevisiae required for controlling sensitivity to 4-nitroquinoline-N-oxide and aminotriazole. Current Genetics 1990, 18:93-96.
31. Grigoriev I.V., Cullen D., Goodwin S.B., Hibbett D., Jeffries T.W., Kubicek C.P., et al. Fueling the future with fungal genomics. Mycology 2011, 2:192-209.
32. Grigoriev I.V., Nordberg H., Shabalov I., Aerts A., Cantor M., Goodstein D., et al. The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Research 2012, 40:D26-D32.
33. Gulshan K., Moye-Rowley W.S. Multidrug resistance in fungi. Eukaryotic Cell 2007, 6:1933-1942. 10.1128/EC.00254-07.
34. Gupta A., Chatoo B.B. Functional analysis of a novel ABC transporter ABC4 from Magnaporthe grisea. FEMS Microbiology Letters 2008, 278:22-28. 10.1111/j.1574-6968.2007.00937.x.
35. Haas H., Eisendle M., Turgeon B.G. Siderophores in fungal physiology and virulence. Annual Reviews of Phytopathology 2008, 46:149-187. 10.1146/annurev.phyto.45.062806.094338.
36. Hayashi K., Schoonbeek H.J., De Waard M.A. Bcmfs1, a novel major facilitator superfamily transporter from Botrytis cinerea, provides tolerance towards the natural toxic compounds camptothecin and cercosporin and towards fungicides. Applied and Environmental Microbiology 2002, 68:4996-5004. 10.1128/AEM.68.10.4996-5004.2002.
37. Helber N., Wippel K., Sauer N., Schaarschmidt S., Hause B., Requena N. A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp. is crucial for the symbiotic relationship with plants. Plant Cell 2011, 23:3812-3823. PMID:21972259. 10.1105/tpc.111.089813.
38. Ismail Y., McCormick S., Hijri M. A fungal symbiont of plant-roots modulates mycotoxin gene expression in the pathogen Fusarium sambucinum. PLoS ONE 2011, 6:e17990. 10.1371/journal.pone.0017990.
39. Katinka M.D., Duprat S., Cornillot E., Méténier G., Thomarat F., Prensier G., et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 2001, 414:450-453. 10.1038/35106579.
40. Kiel J.A., Veenhuis M., van der Klei I.J. PEX genes in fungal genomes: Common, rare or redundant. Traffic 2006, 7:1291-1303. 10.1111/j.1600-0854.2006.00479.x.
41. Kim Y., Park S.-Y., Kim D., Choi J., Lee Y.-H., Lee J.-H., et al. Genome-scale analysis of ABC transporter genes and characterization of the ABCC type transporter genes in Magnaporthe oryzae. Genomics 2013, 101:354-361. 10.1016/j.ygeno.2013.04.003.
42. Kovalchuk A., Driesen A.J. Phylogenetic analysis of fungal ABC transporters. BMC Genomics 2010, 11:177. 10.1186/1471-2164-11-177.
43. Kovalchuk A., Lee Y.H., Asiegbu F.O. Diversity and evolution of ABC proteins in basidiomycetes. Mycologia 2013, 13-001. 10.3852/13-001.
44. Kragl C., Schrettl M., Abt B., Sarg B., Lindner H.H., Haas H. EstB-mediated hydrolysis of the siderophore triacetylfusarinine C optimizes iron uptake of Aspergillus fumigatus. Eukaryotic Cell 2007, 6:1278-1285. 10.1128/EC.00066-07.
45. Kretschmer M., Leroch M., Mosbach A., Walker A.S., Fillinger S., Mernke D., et al. Fungicide-driven evolution and molecular basis of mutidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PloS Pathogens 2009, 5:e1000696. 10.1371/journal.ppat.1000696.
46. Kriel J., Haesendonckx S., Rubio-Texeira M., Van Zeebroeck G., Thevelein J.M. From transporter to transceptor: Signaling from transporters provokes re-evaluation of complex trafficking and regulatory controls: Endocytic internalization and intracellular trafficking of nutrient transceptors may, at least in part, be governed by their signaling function. BioEssays 2011, 33:870-879. Epub 2011 Sep 13. 10.1002/bies.201100100.
47. Kuchler K., Sterne R.E., Thorner J. Saccharomyces cerevisiae STE6 gene product: A novel pathway for protein export in eukaryotic cells. EMBO Journal 1989, 8:3973-3984.
48. Lamping E., Baret P.V., Holmes A.R., Monk B.C., Goffeau A., Cannon R.D. Fungal PDR transporters: Phylogeny, topology, motifs, function. Fungal Genetics and Biology 2010, 47:127-142. 10.1016/j.fgb.2009.10.007.
49. Lamping E., Cannon R.D. Use of a yeast-based membrane protein expression technology to overexpress drug resistance efflux pumps. Methods in Molecular Biology 2010, 666:219-250. 10.1007/978-1-60761-820-1_15.
50. Leandro M.J., Fonseca C., Gonçalves P. Hexose and pentose transport in ascomycetous yeasts: An overview. FEMS Yeast Research 2009, 9:511-525. 10.1111/j.1567-1364.2009.00509.x.
51. Lee T., Han Y.K., Kim K.H., Yun S.H., Lee Y.W. Tri13 and Tri7 determine deoxynivalenol- and nivalenol-producing chemotypes of Gibberella zeae. Applied and Environmental Microbiology 2002, 68:2148-2154. 10.1128/AEM.68.5.2148-2154.2002.
52. Lengeler K.B., Davidson R.C., D'souza C., Harashima T., Shen W.C., Wang P., et al. Signal transduction cascades regulating fungal development and virulence. Microbiology and Molecular Biology Reviews 2000, 64:746-785. 10.1128/MMBR.64.4.746-785.2000.
53. Lingner U., Münch S., Deising H.B., Sauer N. Hexose transporters of a hemibiotrophic plant pathogen: Functional variations and regulatory differences at different stages of infection. The Journal of Biological Chemistry 2011, 286:20913-20922. 10.1074/jbc.M110.213678.
54. Liu H.Y., Chiang Y.C., Pan J., Chen J., Salvadore C., Audino D.C., Badarinarayana V., Palaniswamy V., Anderson B., Denis C.L. Characterization of CAF4 and CAF16 reveals a functional connection between the CCR4-NOT complex and a subset of SRB proteins of the RNA polymerase II holoenzyme. Journal of Biological Chemistry 2001, 276:7541-7548.
55. Liu M., Liu J., Wang W.M. Isolation and functional analysis of Thmfs1, the first major facilitator superfamily transporter from the biocontrol fungus Trichoderma harzianum. Biotechnology Letters 2012, 34:1857-1862. 10.1007/s10529-012-0972-x.
56. Lodish H., Berk A., Zipursky L., Matsudaira P., Baltimore D., Darnell J. Molecular Cell Biology 2000, W. H. Freeman, New York, (Chapter 15). 4th ed.
57. Malmierca M.G., Cardoza R.E., Alexander N.J., McCormick S.P., Collado I.G., Hermosa R., et al. Relevance of trichothecenes in fungal physiology: Disruption of tri5 in Trichoderma arundinaceum. Fungal Genetics and Biology 2013, 53:22-33. 2013.02.001. Epub 2013 Feb 27. 10.1016/j.fgb.
58. Manzoor H., Kelloniemi J., Chiltz A., Wendehenne D., Pugin A., Poinssot B., et al. Involvement of the glutamate receptor AtGLR3.3 in plant defense signaling and resistance to Hyaloperonospora arabidopsidis. Plant Journal 2013, 76:466-480. Epub 2013 Sep 19. 10.1111/tpj.12311.
59. Markowitz V.M., Chen I.-M.A., Palaniappan K., Chu K., Szeto E., Pillay M., et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Research 2012, 40:D123-D129.
60. Markowitz V.M., Chen I.-M.A., Chu K., Szeto E., Palaniappan K., Grechkin Y., et al. IMG/M: The integrated metagenomes data management and comparative analysis system. Nucleic Acids Research 2012, 40:D123-D129. 10.1093/nar/gkr975.
61. Maranhão F.C., Paião F.G., Fachin A.L., Martinez-Rossi N.M. Membrane transporter proteins are involved in Trichophyton rubrum pathogenesis. Journal of Medical Microbiology 2009, 58:163-168. 10.1099/jmm.0.002907-0.
62. Maruthachalam K., Klosterman S.J., Kang S., Hayes R.J., Subbarao K.V. Identification of pathogenicity-related genes in the vascular wilt fungus Verticillium dahliae by Agrobacterium tumefaciens-mediated T-DNA insertional mutagenesis. Molecular Biotechnology 2011, 49:209-221. 10.1007/s12033-011-9392-8.
63. McCormick S.P., Alexander N.J. Fusarium Tri8 encodes a trichothecene C-3 esterase. Applied and Environmental Microbiology 2002, 68:2959-2964. 10.1128/AEM.68.6.2959-2964.2002.
64. Menke J., Dong Y., Kistler H.C. Fusarium graminearum Tri12p influences virulence to wheat and trichothecene accumulation. Molecular Plant Microbe Interactions 2012, 25:1408-1418. 10.1094/MPMI-04-12-0081-R.
65. do Nascimento A.M., Goldman M.H., Goldman G.H. Molecular characterization of ABC transporter-encoding genes in Aspergillus nidulans. Genetics and Molecular Research 2002, 1:337-349.
66. do Nascimento A.M., Goldman G.H., Park S., Marras S.A., Delmas G., Oza U., et al. Multiple resistance mechanisms among Aspergillus fumigatus mutants with high-level resistance to itraconazole. Antimicrobial Agents and Chemotherapy 2003, 47:1719-1726.
67. Nasmith C.G., Walkowiak S., Wang L., Leung W.W., Gong Y., Johnston A., et al. Tri6 is a global transcription regulator in the phytopathogen Fusarium graminearum. PLoS Pathogens 2011, 7:e1002266. 10.1371/journal.ppat.1002266.
68. Newstead S., Drew D., Cameron A.D., Postis V.L., Xia X., Fowler P.W., et al. Crystal structure of a prokaryotic homologue of the mammalian oligopeptide-proton symporters, PepT1 and PepT2. EMBO Journal 2011, 30:417-426. Epub 2010 Dec 3. 10.1038/emboj.2010.309.
69. Niimi M., Wada S., Tanabe K., Kaneko A., Takano Y., Umeyama T., et al. Functional analysis of fungal drug efflux transporters by heterologous expression in Saccharomyces cerevisiae. Japanese Journal of Infectious Diseases 2005, 58:1-7.
70. Niimi M. Characterization of the multi-drug efflux Systems of pathogenic fungi using functional hyperexpression in Saccharomyces cerevisiae. Japanese Journal of Medical Mycology 2010, 51:79-87.
71. Nourani A., Wesolowski-Louvel M., Delaveau T., Jacq C., Delahodde A. Multiple-drug-resistance phenomenon in the yeast Saccharomyces cerevisiae: Involvement of two hexose transporters. Molecular and Cellular Biology 1997, 17:5453-5460.
72. Oh D.-C., Scott J.J., Currie C.R., Clardy J. Mycangimycin, a polyene peroxide from a mutualist Streptomyces sp. Organic Letters 2009, 11:633-636. 10.1021/ol802709x.
73. Özcan S., Dover J., Johnston M. Glucose sensing and signaling by two glucose receptors in the yeast Saccharomyces cerevisiae. EMBO Journal 1998, 17:2566-2573.
74. Pao S.S., Paulsen I.T., Saier M.H. Major facilitator superfamily. Microbiology and Molecular Biology Reviews 1998, 62:1-34. Review. PMID:9529885.
75. Parrent J.L., James T.Y., Vasaitis R., Taylor A.F. Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evolutionary Biology 2009, 9:148. 10.1186/1471-2148-9-148.
76. Pasrija R., Banerjee D., Prasad R. Structure and function analysis of CaMdr1p, a major facilitator superfamily antifungal efflux transporter protein of Candida albicans: Identification of amino acid residues critical for drug/H+ transport. Eukaryotic Cell 2007, 6:443-453.
77. Pedras M.S.C., Minic Z. Differential protein expression in response to the phytoalexin brassinin allows the identification of molecular targets in the phytopathogenic fungus Alternaria brassicicola. Molecular Plant Pathology 2012, 13:483-493.
78. Peplow A.W., Tag A.G., Garifullina G.F., Beremand M.N. Identification of new genes positively regulated by Tri10 and a regulatory network for trichothecene mycotoxin production. Applied and Environmental Microbiology 2003, 69:2731-2736. 10.1128/AEM.69.5.2731-2736.2003.
79. Periyannan S., Moore J., Ayliffe M., Bansal U., Wang X., Huang L., et al. The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 2013, 341:786-788. Epub 2013 Jun 27. 10.1126/science.1239028.
80. Prates R.A., Kato I.T., Ribeiro M.S., Tegos G.P., Hamblin M.R. Influence of multidrug efflux systems on methylene blue-mediated photodynamic inactivation of Candida albicans. Journal of Antimicrobial Chemotherapy 2011, 66:1525-1532. 10.1093/jac/dkr160.
81. Punta M., Coggill P.C., Eberhardt R.Y., Mistry J., Tate J., Boursnell C., et al. The Pfam protein families database. Nucleic Acids Research 2012, 40(Database issue):D290-D301. Epub 2011 Nov 29. 10.1093/nar/gkr1065.
82. Ravichandra N.G. Fundamentals of Plant Pathology 2013, Ghosh, PHI Learning Private Limited, Delhi.
83. Reddy V.S., Shlykov M.A., Castillo R., Sun E.I., Saier M.H. The major facilitator superfamily (MFS). FEBS Journal 2012, 279:2022-2035. Revisted, Epub 2012 May 8. Erratum in: FEBS Journal 2013 Aug; 280(16): 3975. 10.1111/j.1742-4658.2012.08588.x.
84. Reimann S., Deising H.B. Inhibition of efflux transporter-mediated fungicide resistance in Pyrenophora tritici-repentis by a derivative of natural 4'-hydroxyflavone and potentiation of fungicide activity. Applied and Environmental Microbiology 2005, 71:3269-3275. 10.1128/AEM.71.6.3269-3275.2005.
85. Ricardo S., Lehmann R. An ABC transporter controls export of a Drosophila germ cell attractant. Science 2009, 323:943-946. 10.1126/science.1166239.
86. Roohparvar R., De Waard M.A., Kema G.H., Zwiers L.H. MgMfs1, a major facilitator superfamily transporter from the fungal wheat pathogen Mycosphaerella graminicola, is a strong protectant against natural toxic compounds and fungicides. Fungal Genetics and Biology 2007, 44:378-388. 10.1016/j.fgb.2006.09.007.
87. Rutherford J.C., Lin X., Nielsen K., Heitman J. Amt2 permease is required to induce ammonium-responsive invasive growth and mating in Cryptococcus neoformans. Eukaryotic Cell 2008, 7:237-246. Epub 2007 Nov 30. 10.1128/EC.00079-07.
88. Saier M.H., Tran C.V., Barabote R.D. TCDB: The Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Research 2006, 34:D181-D186. 10.1093/nar/gkj001.
89. Sanguinetti M., Posteraro B., La Sorda M., Torelli R., Fiori B., Santangelo R., et al. Role of AFR1, an ABC transporter-encoding gene, in the in vivo response to fluconazole and virulence of Cryptococcus neoformans. Infection and Immunity 2006, 74:1352-1359.
90. Schaarschmidt S., Roitsch T., Hause B. Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. Journal of Experimental Botany 2006, 57:4015-4023. Epub 2006 Oct 18.
91. Schoonbeek H.J., Del Sorbo G., De Waard M.A. The ABC transporter BcatrG affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpliclonil. Molecular Plant Microbe Interactions 2001, 14:562-571.
92. Schuller C., Bauer B.E., Kuchler K. Inventory and evolution of fungal ABC protein genes. ABC proteins: from bacteria to man 2003, Elsevier. I.B. Holland, S.P.C. Cole, K. Kuchler, C.F. Higgins (Eds.).
93. Shalchian-Tabrizi K., Minge M.A., Espelund M., Orr R., Ruden T., Jakobsen K.S., et al. Multigene phylogeny of choanozoa and the origin of animals. PLoS ONE 2008, 3:e2098. 10.1371/journal.pone.0002098.
94. Silva L.V., Sanguinetti M., Vandeputte P., Torelli R., Rochat B., Sanglard D. Milbemycins: More than efflux inhibitors for fungal pathogens. Antimicrobial Agents and Chemotherapy 2013, 57:873-886. Epub 2012 Dec 3. 10.1128/AAC.02040-12.
95. Sipos G., Kuchler K. Fungal ATP-binding cassette (ABC) transporters in drug resistance & detoxification. Current Drug Targets 2006, 7:471-481.
96. Slaven J.W., Anderson M.J., Sanglard D., Dixon G.K., Bille J., Roberts I.S., et al. Increased expression of a novel Aspergillus fumigatus ABC transporter gene, atrF, in the presence of itraconazole in an itraconazole resistant clinical isolate. Fungal Genetics and Biology 2002, 36:199-206. 10.1016/S1087-1845(02)00016-6.
97. Smith D.G., Garcia-Pedrajas M.D., Gold S.E., Perlin M.H. Isolation and characterization from pathogenic fungi of genes encoding ammonium permeases and their roles in dimorphism. Molecular Microbiology 2003, 50:259-275. 10.1046/j.1365-2958.2003.03680.x.
98. Solcan N., Kwok J., Fowler P.W., Cameron A.D. Alternating access mechanism in the POT family of oligopeptide transporters. The EMBO Journal 2012, 31:3411-3421. 10.1038/emboj.2012.157.
99. Sun C.B., Suresh A., Deng Y.Z., Naqvi N.I. A multidrug resistance transporter in Magnaporthe is required for host penetration and for survival during oxidative stress. Plant Cell 2006, 18:3686-3705. Epub 2006 Dec 22. 10.1105/tpc.105.037861.
100. Sutherland R., Viljoen A., Myburg A.A., Van den Berg N. Pathogenicity associated genes in Fusarium oxysporum f. sp. cubense race 4. South African Journal of Sciences 2013, 109. Art. #0023, 10 pages. 10.1590/sajs.2013/20120023.
101. Tag A.G., Garifullina G.F., Peplow A.W., Ake C., Phillips T.D., Hohn T.M., et al. A novel regulatory gene, Tri10, controls trichothecene toxin production and gene expression. Applied and Environmental Microbiology 2001, 67:5294-5302. 10.1128/AEM.67.11.5294-5302.2001.
102. Thomazella D.P., Teixeira P.J., Oliveira H.C., Saviani E.E., Rincones J., Toni I.M., et al. The hemibiotrophic cacao pathogen Moniliophthora perniciosa depends on a mitochondrial alternative oxidase for biotrophic development. New Phytologist 2012, 194:1025-1034. Epub 2012 Mar 23. 10.1111/j.1469-8137.2012.04119.x.
103. Tian C., Beeson W.T., Iavarone A.T., Sun J., Marletta M.A., Cate J.H.D., et al. Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proceedings of the National Academy of Sciences 2009, 106:22157-22162.
104. Tijerino A., Cardoza R.E., Moraga J., Malmierca M.G., Vicente F., Aleu J., et al. Overexpression of the trichodiene synthase gene tri5 increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genetics and Biology 2011, 48:285-296. Epub 2010 Dec 7. 10.1016/j.fgb.2010.11.012.
105. Urban M., Bhargava T., Hamer J.E. An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO Journal 1999, 18:512-521. 10.1093/emboj/18.3.512.
106. Vargas W.A., Martín J.M., Rech G.E., Rivera L.P., Benito E.P., Díaz-Mínguez J.M., et al. Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotrichum graminicola in maize. Plant Physiology 2012, 158:1342-1358. Epub 2012 Jan 12. 10.1104/pp.111.190397.
107. von Dohren H. A survey of nonribosomal peptide synthetase (NRPS) genes in Aspergillus nidulans. Fungal Genetics and Biology 2009, 46:S45-S52. 10.1016/j.fgb.2008.08.008.
108. Wada S., Tanabe K., Yamazaki A., Niimi M., Uehara Y., Niimi K., et al. Phosphorylation of Candida glabrata ATP-binding cassette transporter Cdr1p regulates drug efflux activity and ATPase stability. Journal of Biological Chemistry 2005, 280:94-103. 10.1074/jbc.M408252200.
109. Wahl R., Wippel K., Goos S., Kämper J., Sauer N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biology 2010, 8:e1000303. 10.1371/journal.pbio.1000303.
110. Ward T.J., Bielawski J.P., Kistler H.C., Sullivan E., O'Donnell K. Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin cluster of phytopathogenic Fusarium. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:9278-9283. 10.1073/pnas.142307199.
111. Weber R.W.S., Entrop A.-P. Multiple fungicide resistance in Botrytis: A growing problem in German soft-fruit production. Fungicides - Beneficial and Harmful Aspects 2011, ISBN: 978-953-307-451-1, InTech, 10.5772/27199. Available from. http://www.intechopen.com/books/fungicides-beneficial-and-harmful-aspects/multiple-fungicide-resistance-in-botrytis-a-growing-problem-in-german-soft-fruit-production, N. Thajuddin (Ed.).
112. Wenzel J.J., Piehler A., Kaminski W.E. ABC A-subclass proteins: Gatekeepers of cellular phosphor- and sphingolipid transport. Frontiers in Biosciences 2007, 12:3177-3193. 10.2741/2305.
113. Wiles A.M., Cai H., Naider F., Becker J.M. Nutrient regulation of oligopeptide transport in Saccharomyces cerevisiae. Microbiology 2006, 152:3133-3145. 10.1099/mic.0.29055-0.
114. Wipf D., Ludewig U., Tegeder M., Rentsch D., Koch W., Frommer W.B. Conservation of amino acid transporters in fungi, plants and animals. Trends in Biochemical Science 2002, 27:139-147. 10.1016/S0968-0004(01)02054-0.
115. Wood N.J., Alizadeh T., Richardson D.J., Ferguson S.J., Moir J.W.B. Two domains of a dual-function NarK protein are required for nitrate uptake, the first step of denitrification in Paracoccus pantotrophus. Molecular Microbiology 2002, 44:157-170. 10.1046/j.1365-2958.2002.02859.x.
116. Wuchiyama J., Kimura M., Yamaguchi I. A trichothecene efflux pump encoded by Tri102 in the biosynthesis gene cluster of Fusarium graminearum. Journal of Antibiotics (Tokyo) 2000, 53:196-200. 10.1046/j.1365-2958.2002.02859.x.
117. Yin Y., He X., Szewczyk P., Nguyen T., Chang G. Structure of the multidrug transporter EmrD from Escherichia coli. Science 2006, 312:741-744.
118. Yoshida Y. Cytochrome P450 of fungi: Primary target for azole antifungal agents. Current Topics in Medical Mycology 1988, 2:388-418. 10.1007/978-1-4612-3730-3_11.
119. Young L., Leonhard K., Tatsuta T., Trowsdale J., Langer T. Role of the ABC transporter Mdl1 in peptide export from mitochondria. Science 2001, 291:2135-2138. 10.1126/science.1056957.
120. Zuccaro A., Lahrmann U., Güldener U., Langen G., Pfiffi S., Biedenkopf D., et al. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathogens 2011, 7:e1002290. Epub 2011 Oct 13. 10.1371/journal.ppat.1002290.
121. Zwiers L.H., Stergiopoulos I., Gielkens M.M., Goodall S.D., De Waard M.A. ABC transporters of the wheat pathogen Mycosphaerella graminicola function as protectants against biotic and xenobiotic toxic compounds. Molecular Genetics and Genomics 2003, 269:499-507. 10.1007/s00438-003-0855-x.