ABC transporters of the wheat pathogen Mycosphaerella graminicola function as protectants against biotic and xenobiotic toxic compounds

Molecular Genetics and Genomics

Volumn 269, Issue 4, 2003, Pages 499-507

  Zwiers, L H ^a   Stergiopoulos, I ^a   Gielkens, M M C ^a,b   Goodall, S D ^a,c   De Waard, M A ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

ABC transporter; Antibiotic; Multidrug resistance; Mycosphaerella graminicola; Septoria tritici

Indexed keywords

ABC TRANSPORTER; AMPHOTERICIN B; ANTIBIOTIC AGENT; BERBERINE; CAMPTOTHECIN; CARBENDAZIM; COLCHICINE; CYCLOHEXIMIDE; DIACETOXYSCIRPENOL; ENILCONAZOLE; EUGENOL; FUNGICIDE; GENE PRODUCT; GRAMINE; HYGROMYCIN; MICONAZOLE; MYCOTOXIN; NEOMYCIN; OLIGOMYCIN; PHYTOALEXIN; PROBIOTIC AGENT; PROPICONAZOLE; PSORALEN; QUERCETIN; RESERPINE; RESORCINOL; RESVERATROL; THIRAM; TOMATINE; XENOBIOTIC AGENT;

ARTICLE; ATR2 GENE; BIOASSAY; DELETION MUTANT; ENZYME SPECIFICITY; FUNGAL CELL; FUSARIUM GRAMINEARUM; GENE; GENE DELETION; GENE DISRUPTION; MULTIDRUG RESISTANCE; NONHUMAN; PHYTOTOXICITY; PLANT DEFENSE; PLANT GENETICS; PLANT METABOLISM; PRIORITY JOURNAL; PROTECTION; SACCHAROMYCES CEREVISIAE; WHEAT;

ASCOMYCOTA; ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, FUNGAL; MUTATION; TRITICUM;

BURKHOLDERIA; BURKHOLDERIA CEPACIA; FUNGI; FUSARIUM; GIBBERELLA ZEAE; GRAMINICOLA; MYCOSPHAERELLA; MYCOSPHAERELLA GRAMINICOLA; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SEPTORIA; TRITICUM AESTIVUM; VITIS SP.;

EID: 0042661008     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-003-0855-x     Document Type: Article

References (43)

1. Andrade AC, Del Sorbo G, van Nistelrooy JGM, De Waard MA (2000) The ABC transporter AtrB from Aspergillus nidulans mediates resistance to all major classes of fungicides and some natural toxic compounds. Microbiology 146:1987-1997
2. Burkhead K, Schisler D, Slininger P (1994) Pyrrolnitrin production by biological control agent Pseudomonas cepacia B37w in culture and in colonized wounds of potatoes. Appl Environ Microbiol 60:2031-2039
3. Carmi R, Carmeli S, Levy E, Gough FJ (1994) (+)-(S)-dihydroaeruginoic acid, an inhibitor of Septoria tritici and other phytopathogenic fungi and bacteria, produced by Pseudomonas fluorescens. J Nat Prod 57:1200-5
4. Christensen PU, Davey J, Nielsen O (1997) The Schizosaccharomyces pombe mam1 gene encodes an ABC transporter mediating secretion of M-factor. Mol Gen Genet 255:226-236
5. De Waard MA (1997) Significance of ABC transporters in fungicide sensitivity and resistance. Pestic Sci 51:271-275
6. Decottignies A, Goffeau A (1997) Complete inventory of the yeast ABC proteins. Nat Genet 15:137-145
7. Decottignies A, Grant AM, Nichols JW, De Wet H, McIntosh DB, Goffeau A (1998) ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yorlp. J Biol Chem 273:12612-12622
8. Del Sorbo G, Schoonbeek H, De Waard MA (2000) Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genet Biol 30:1-15
9. Fleissner A, Copalla C, Weltring K-M (2002) An ABC Multidrug-Resistance transporter is necessary for tolerance of Gibberella pulicaris to phytoalexins and virulence on potato tubers. Mol Plant-Microbe Interact 15:102-108
10. Foote SJ, Thompson JK, Cowman AF, Kemp DJ (1989) Amplification of the multidrug resistance gene in some chloroquine-resistant isolates of P. falciparum. Cell 57:921-930
11. Frey M, Chomet P, Glawischnig E, Stettner C, Grun S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277:696-699
12. Gottesman MM, Pastan I (1993) Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 62:385-427
13. Higgins CF (2001) ABC transporters: physiology, structure and mechanism - an overview. Res Microbiol 152:205-210
14. Howell CR, Stipanovic RD (1979) Control of Rhizoctonia solani on cotton seedlings with Pseudomonas fluorescens and with an antibiotic produced by the bacterium. Phytopathology 69:480-482
15. Jeandet P, Bessis R, Sbaghi M, Meunier P (1995) Production of the phytoalexin resveratrol by grapes as a response to Botrytis attack under natural conditions. J Phytopathol 143:135-139
16. Kaur R, Bachhawat AK (1999) The yeast multidrug resistance pump, Pdr5p, confers reduced drug resistance in erg mutants of Saccharomyces cerevisiae. Microbiology 145:809-818
17. Kema GHJ, Van Silfhout CH (1997) Genetic variation for virulence and resistance in the wheat- Mycosphaerella graminicola pathosystem. III. Comparative seedling and adult plant experiments. Phytopathology 87:266-272
18. King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescein. J Lab Clin Med 44:301-307
19. Kolaczkowski M, Goffeau A (1997) Active efflux by multidrug transporters as one of the strategies to evade chemotherapy and novel practical implications of yeast pleiotropic drug resistance. Pharmacol Therapeut 76:219-242
20. Kolaczkowski M, Kolaczkowska A, Luczynski J, Witek S, Goffeau A (1998) In vivo characterization of the drug resistance profile of the major ABC transporters and other components of the yeast pleiotropic drug resistance network. Microb Drug Resist 4:143-158
21. Krishnamurthy SS, Prasad RU (1999) Membrane fluidity affects functions of Cdr1p, a multidrug ABC transporter of Candida albicans. FEMS Microbiol Lett 173:475-481
22. Levy E, Eyal Z, Carmely S, Kashman Y, Chet I (1989) Suppression of Septoria tritici and Puccinia recondita of wheat by an antibiotic-producing fluorescent pseudomonad. Plant Pathol 38:564-570
23. Mahe Y, Lemoine Y, Kuchler K (1996) The ATP binding cassette transporters Pdr5 and Snq2 of Saccharomyces cerevisiae can mediate transport of steroids in vivo. J Biol Chem 271:25167-25172
24. McGrath JP, Varshavsky A (1989) The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature 340:400-404
25. Melchers WJ, Verweij PE, Van den Hurk P, Van Belkum A, De Pauw BE, Hoogkamp Korstanje JA, Meis JF (1994) General primer-mediated PCR for detection of Aspergillus species. J Clin Microbiol 32:1710-1717
26. Muhitch MJ, McCormick SP, Alexander NJ, Hohn TM (2000) Transgenic expression of the TRI101 or PDR5 gene increases resistance of tobacco to the phytotoxic effects of the trichothecene 4,15-diacetoxyscirpenol. Plant Sci 157:201-207
27. Nishi K, Yoshida M, Nishimura M, Nishikawa M, Nishiyama M, Horinouchi S, Beppu T (1992) A leptomycin B resistance gene of Schizosaccharomyces pombe encodes a protein similar to the mammalian P-glycoproteins. Mol Microbiol 6:761-769
28. Payne AC, Grosjean-Cournoyer MC, Hollomon DW (1998) Transformation of the phytopathogen Mycosphaerella graminicola to carbendazim and hygromycin B resistance. Curr Genet 34:100-104
29. Rothenberg ML (1997) Topoisomerase I inhibitors: review and update. Ann Oncol 8:837-855
30. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual (2nd edn). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
31. Schoonbeek H, Del Sorbo G, De Waard MA (2001) The ABC transporter BcatrB affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil. Mol Plant-Microbe Interact 14:562-571
32. Schoonbeek H, Raaijmakers JM, De Waard MA (2002) Fungal ABC transporters and microbial interactions in natural environments. Mol Plant-Microbe Interact 15:1165-1172
33. Seitz LM (1992) Identification of 5-(2-oxoalkyl)resorcinols and 5-(2-oxoalkenyl)resorcinols in wheat and rye grains. J Agr Food Chem 40:1541-1546
34. Stergiopoulos I, Gielkens MMC, Goodall SD, Venema K, De Waard MA (2002a) Molecular cloning and characterisation of three new ABC transporter-encoding genes from the wheat pathogen Mycosphaerella graminicola. Gene 289:141-149
35. Stergiopoulos I, Zwiers L-H, De Waard MA (2002b) Secretion of natural and synthetic toxic compounds from filamentous fungi by membrane transporters of the ATP-binding cassette and major facilitator superfamily. Eur J Plant Pathol 108:719-734
36. Stergiopoulos I, Zwiers L-H, De Waard MA (2003) The ABC transporter MgAtr4 is a virulence factor of Mycosphaerella graminicola that affects colonization of substomatal cavities in wheat leaves. Mol Plant-Microbe Interact (in press)
37. Stermitz FR, Lorenz P, Tawara JN, Zenewicz LA, Lewis K (2000) Synergy in a medicinal plant: antimicrobial action of berberine potentiated by 5-methoxyhydnocarpin, a multidrug pump inhibitor. Proc Natl Acad Sci USA 97:1433-1437
38. Suzuki Y, Esumi Y, Hyakutake H, Kono Y, Sakurai A (1996) Isolation of 5-(8′Z-heptadecenyl)-resorcinol from etiolated rice seedlings as an antifungal agent. Phytochemistry 41:1485-1489
39. Urban M, Bhargava T, Hamer JE (1999) An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J 18:512-521
40. Wilkes MA, Marshall DR, Copeland L (1999) Hydroxamic acids in cereal roots inhibit the growth of take-all. Soil Biol Biochem 31:1831-1836
41. Zwiers L-H, De Waard MA (2000) Characterization of the ABC transporter genes MgAtr1 and MgAtr2 from the wheat pathogen Mycosphaerella graminicola. Fungal Genet Biol 30:115-125
42. Zwiers L-H, De Waard MA (2001) Efficient Agrobacterium tumefaciens -mediated gene disruption in the phytopathogen Mycosphaerella graminicola. Curr Genet 39:388-393
43. Zwiers L-H, Stergiopoulos I, Van Nistelrooy JGM, De Waard MA (2002) ABC transporters and azole susceptibility in laboratory strains of the wheat pathogen Mycosphaerella graminicola. Antimicrob Agents Chemother 46:3900-3906