An ATP-binding cassette pleiotropic drug transporter protein is required for xenobiotic tolerance and antagonism in the fungal biocontrol agent Clonostachys rosea

Molecular Plant-Microbe Interactions

Volumn 27, Issue 7, 2014, Pages 725-732

  Dubey, Mukesh K ^a   Jensen, Dan Funck ^a   Karlsson, Magnus ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; FUNGAL PROTEIN; XENOBIOTIC AGENT;

ARTICLE; ASCOMYCETES; CHEMISTRY; FUSARIUM; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; PHYSIOLOGY;

ASCOMYCOTA; ATP-BINDING CASSETTE TRANSPORTERS; FUNGAL PROTEINS; FUSARIUM; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENETIC COMPLEMENTATION TEST; XENOBIOTICS;

EID: 84901715107     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-12-13-0365-R     Document Type: Article

References (52)

1. Andersson, M. A., Mikkola, R., Raulio, M., Kredics, L., Maijala, P., and Salkinoja-Salonen, M. S. 2009. Acrebol, a novel toxic peptaibol produced by an Acremonium exuviarum indoor isolate. J. Appl. Microbiol. 106:909-923.
2. Bae, H., Roberts, D. P., Lim, H.-S., Strem, M. D., Park, S.-C., Ryu, C.-M., Melnick, R. L., and Bailey, B. A. 2011. Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol. Plant-Microbe Interact. 24:336-351.
3. Biemans-Oldehinkel, E., Doeven, M. K., and Poolman, B. 2006. ABC transporter architecture and regulatory roles of accessory domains. FEBS (Fed. Eur. Biochem. Soc.) Lett. 580:1023-1035. (Pubitemid 43186038)
4. Chatterton, S., Jayaraman, J., and Punja, Z. K. 2008. Colonization of cucumber plants by the biocontrol fungus Clonostachys rosea f. catenulata. Biol. Control 46:267-278.
5. Coleman, J. J., and Mylonakis, E. 2009. Efflux in fungi: La Piece de Resistance. PLoS Pathog. 5:e1000486. Published online.
6. Coleman, J. J., White, G. J., Rodriguez-Carres, M., and VanEtten, H. D. 2011. 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. Mol. Plant-Microbe Interact. 24:368-376.
7. Del Sorbo, G., Schoonbeek, H., and De Waard, M. A. 2000. Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genet. Biol. 30:1-15. (Pubitemid 30666583)
8. de Waard, M. A., Andrade, A. C., Hayashi, K., Schoonbeek, H. J., Stergiopoulos, I., and Zwiers, L. H. 2006. Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Manag. Sci. 62:195-207.
9. Druzhinina, I. S., Seidl-Seiboth, V., Herrera-Estrella, A., Horwitz, B. A., Kenerley, C. M., Monte, E., Mukherjee, P. K., Zeilinger, S., Grigoriev, I. V., and Kubicek, C. 2011. Trichoderma: The genomics of opportunistic success. Nat. Rev. Microbiol. 9:749-759.
10. Dubey, M. K., Ubhayasekera, W., Sandgren, M., Jensen, D. F., and Karlsson, M. 2012. Disruption of the Eng18B ENGase gene in the fungal biocontrol agent Trichoderma atroviride affects growth, conidiation and antagonistic ability. PLoS ONE 7:e36152. Published online.
11. Dubey, M. K., Broberg, A., Sooriyaarachchi, S., Ubhayasekera, W., Jensen, D. F., and Karlsson, M. 2013a. The glyoxylate cycle is involved in pleotropic phenotypes, antagonism and induction of plant defence responses in the fungal biocontrol agent Trichoderma atroviride. Fungal Genet. Biol. 58-59:33-41.
12. Dubey, M. K, Broberg, A., Jensen D. F., and Karlsson M. 2013b. Role of the methylcitrate cycle in growth, antagonism and induction of systemic defence responses in the fungal biocontrol agent Trichoderma atroviride. Microbiology 159:2492-2500.
13. Fleissner, A., Sopalla, C., and Weltring, K.-M. 2002. An ATP-binding cassette multidrug-resistance transporter is necessary for tolerance of Gibberella pulicaris to phytoalexins and virulence on potato tubers. Mol. Plant-Microbe Interact. 15:102-108. (Pubitemid 34186393)
14. Gupta, A., and Chattoo, B. B. 2008. Functional analysis of a novel ABC transporter ABC4 from Magnaporthe grisea. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 278:22-28. (Pubitemid 350215876)
15. Jensen, B., Knudsen, I. M. B., Madsen, M., and Jensen, D. F. 2004. Biopriming of infected carrot seed with an antagonist, Clonostachys rosea, selected for control of seedborne Alternaria spp. Phytopathology 94:551-560. (Pubitemid 38681963)
16. Jensen, D. F., Knudsen, I. M. B., Lübeck, M., Mamarabadi, M., Hockenhull, J., and Jensen B. 2007. Development of a biocontrol agent for plant disease control with special emphasis on the near commercial fungal antagonist Clonostachys rosea strain IK726. Aust. Plant Pathol. 36:95-101. (Pubitemid 46364632)
17. Jensen, B., Knudsen I. M. B., Jensen, D. F., Andersen, B., Nielsen, K. F., Thrane, U., and Larsen, J. 2011. Importance of microbial pest control agents and their metabolites in relation to the natural microbiota on strawberry. Pesticides Research no. 1282011, Danish Environmental Protection Agency, Aarhus, Denmark.
18. Karimi, M., De Meyer, B., and Hilson, P. 2005. Modular cloning in plant cells. Trends Plant Sci. 10:103-105. (Pubitemid 40323292)
19. Knudsen, I. M. B., Hockenhul, J., and Jensen, D. F. 1995. Biocontrol of seedling diseases caused by Fusarium culmorum and Bipolaris sorokiniana: Effects of selected fungal antagonists on growth and yield components. Plant Pathol. 44:467-477. (Pubitemid 26454903)
20. Kosawang, C. 2013. Three-way interaction between Fusarium species, their plant hosts and biocontrol organisms. PhD thesis. Faculty of Science, University of Copenhagen, Denmark.
21. Kosawang, C., Karlsson, M., Jensen, D. F, Dilokpimol, A., and Collinge, D. B. 2014. Transcriptomic profiling to identify genes involved in Fusarium mycotoxin deoxynivalenol and zearalenone tolerance in the mycoparasitic fungus Clonostachys rosea. BMC Genomics 15:55.
22. Kovalchuk, A., and Driessen, A. J. M. 2010. Phylogenetic analysis of fungal ABC transporters. BMC Genomics 11:177.
23. Kretschmer, M., Leroch, M., Mosbach, A., Walker, A. S., Fillinger, S., Mernke, D., Schoonbeek, H., Pradier, J. M., Leroux, P., de Waard, M. A., and Hahn, M. 2009. Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog. 5, e1000696. Published online.
24. Lamping, E., Baret, P. V., Holmes, A. R., Monk, B. C., Goffeau, A., and Cannon, R. D. 2010. Fungal PDR transporters: Phylogeny, topology, motifs and function. Fungal Genet. Biol. 47:127-142.
25. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. (Pubitemid 350162903)
26. Letunic, I., Doerks, T., and Bork, P. 2009. SMART 6: Recent updates and new developments. Nucleic Acids Res. 37:D229-D232.
27. Li, G. Q., Huang, H. C., Acharya, S. N., and Erickson R. S. 2004. Biological control of blossom blight of alfalfa caused by Botrytis cinerea under environmentally controlled and field conditions. Plant Dis. 88:1246-1251. (Pubitemid 39437987)
28. Lübeck, M., Knudsen, I. M. B., Jensen, B., Thrane, U., Janvier, C., and Jensen, D. F. 2002. GUS and GFP transformation of the biocontrol strain Clonostachys rosea IK726 and the use of these marker genes in ecological studies. Mycol. Res. 106:818-826.
29. Luongo, L. Galli, M., Corazza, L., Meekes, E. T. M., De Haas, B. H., Plas, L. V., and Köhl, J. 2005. Potential of fungal antagonists for biocontrol of Fusarium spp. in wheat and maize through competition in crop debris. Biocontrol Sci. Techn. 15:229-242. (Pubitemid 40856375)
30. Macedo, P. E. F., Maffia, L. A., Cota, L. V., Lourenco, V., and Mizubuti, E. S. G. 2012. Sensitivity of four isolates of Clonostachys rosea to pesticides used in the strawberry crop in Brazil. J. Pestic. Sci. 37:333-337.
31. Mamarabadi, M., Jensen, B., Jensen, D. F., and Lübeck, M. 2008. Realtime RT-PCR expression analysis of chitinase and endoglucanase genes in the three-way interaction between the biocontrol strain Clonostachys rosea IK726, Botrytis cinerea and strawberry. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 285:101-110. (Pubitemid 352000222)
32. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Lu, F., Marchler, G. H., Mullokandov, M., Omelchenko, M. V., Robertson, C. L., Song, J. S., Thanki, N., Yamashita, R. A., Zhang, D., Zhang, N., Zheng, C., and Bryant, S. H. 2011. CDD: A Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39:D225-229.
33. Nygren, C. M. R., Eberhardt, U., Karlsson, M., Parrent, J. L., Lindahl, B. D., and Taylor, A. F. S. 2008. Growth on nitrate and occurrence of nitrate reductase-encoding genes in a phylogenetically diverse range of ectomycorrhizal fungi. New Phytol. 180:875-889.
34. Paul, S., Diekema D., and Moye-Rowley W. S. 2013. Contributions of Aspergillus fumigatus ATP-binding cassette transporter proteins to drug resistance and virulence. Eukaryot. Cell 12:1619-1628.
35. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. 2011. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786.
36. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:2001-2007.
37. Roberti, R., Badiali, F., Pisi, A., Pancaldi, D., and Cesari, A. 2006. Sensitivity of Clonostachys rosea and Trichoderma spp. as potential biocontrol agents to pesticides. J. Phytopathol. 154:100-109
38. Roberti, R., Veronesi, A., Cesaria, A., Casconeb, A., Berardinob, I. D., Bertinib, J., Caruso, C. 2008. Induction of PR proteins and resistance by the biocontrol agent Clonostachys rosea in wheat plants infected with Fusarium culmorum. Plant Sci. 175:339-347.
39. Rodriguez, M. A., Cabrera, G., Gozzo, F. C., Eberlin, M. N., and Godeas, A. 2011. Clonostachys rosea BAFC3874 as a Sclerotinia sclerotiorum antagonist: Mechanisms involved and potential as a biocontrol agent. J. Appl. Microbiol. 110:1177-1186.
40. Ruocco, M., Lanzuise, S., Vinale, F., Marra, R., Turra, D., Woo, S. L., and Lorito, M. 2009. Identification of a new biocontrol gene in Trichoderma atroviride: The role of an ABC transporter membrane pump in the interaction with different plant-pathogenic fungi. Mol. Plant-Microbe Interact. 22:291-301.
41. Schouten, A., Maksimova, O., Cuesta-Arenas, Y., van den Berg, G., and Raaijmakers, J. M. 2008. Involvement of the ABC transporter BcAtrB and the laccase BcLCC2 in defence of Botrytis cinerea against the broad-spectrum antibiotic 2,4-diacetylphloroglucinol. Environ. Microbiol. 10:1145-1157. (Pubitemid 351499233)
42. Sharom, F. J. 2008. ABC multidrug transporters: Structure, function and role in chemoresistance. Pharmacogenomics 9:105-127. (Pubitemid 351560534)
43. Song, T. T., Ying, S. H., and Feng, M. G. 2012. High resistance of Isaria fumosorosea to carbendazim arises from the overexpression of an ABC transporter (ifT1) rather than tubulin mutation. J. Appl. Microbiol. 112:175-184.
44. Song, T. T., Zhao, J., Ying, S. H., and Feng, M. G. 2013. Differential contributions of five ABC transporters to mutidrug resistance, antioxidation and virulence of Beauveria bassiana, an entomopathogenic fungus. PLoS ONE 8:62179. Published online.
45. Sun, C. B., Suresh, A., Deng, Y. Z., and Naqvi, N. I. 2006. A multidrug resistance transporter in Magnaporthe is required for host penetration and for survival during oxidative stress. Plant Cell 18:3686-3705. (Pubitemid 46464921)
46. Takahashi-Ando, N., Kimura, M., Kakeya, H., Osada, H., and Yamaguchi, I. 2002. A novel lactonohydrolase responsible for the detoxification of zearalenone: Enzyme purification and gene cloning. Biochem. J. 365:1-6 (Pubitemid 34756133)
47. Toledo, A. V., Virla, E., Humber, R. A., Paradell, S. L., and Lastra, C. C. 2006. First record of Clonostachys rosea (Ascomycota: Hypocreales) as an entomopathogenic fungus of Oncometopia tucumana and Sonesimia grossa (Hemiptera: Cicadellidae) in Argentina. J. Invertebr. Pathol. 92:7-10.
48. Tzelpis, G. D., and Lagopodi, L. A. 2011. Interaction between Clonostachys rosea IK726 and Pseudomonas chlororaphis PCL 1391 against tomato foot and root rot caused by Fusarium oxysporium f. sp. radicis lycopersici. IOBC/wprs Bulletin 63:75-79.
49. Tzelepis, G. D., Melin, P., Jensen, D. F., Stenlid, J., and Karlsson, M. 2012. Functional analysis of glycoside hydrolase family 18 and 20 genes in Neurospora crassa. Fungal Genet. Biol. 49:717-730.
50. Urban, M., Bhargava, T., and Hamer, J. E. 1999. An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO (Eur. Mol. Biol. Organ.) J. 18:512-521. (Pubitemid 29057236)
51. Utermark, J., and Karlovsky, P. 2008. Genetic transformation of filamentous fungi by Agrobacterium tumefaciens. Nat. Protoc. doi:10.1038/nprot.2008.83. Published online.
52. Zhang, L., Yang, J., Niu, Q., Zhao, X., Ye, F., Liang, L., and Zhang, K. Q. 2008. Investigation on the infection mechanism of the fungus Clonostachys rosea against nematodes using the green fluorescent protein. Appl. Microbiol. Biotechnol. 78:983-990.