ABCC Transporter Gene MoABC-R1 Is Associated with Pyraclostrobin Tolerance in Magnaporthe oryzae
Abstract
:1. Introduction
2. Materials and Methods
2.1. Primers Used in This Study
2.2. Fungal Cultivation
2.3. Conidia Production
2.4. Mycelia Collection
2.5. Vegetative Growth Rates
2.6. Feature and Function Prediction for MoABC-R1
2.7. Generation of MoABC-R1 Disrupted Mutants
2.8. Generation of MoABC-R1 Complement Strains
2.9. Appressorium Formation Assay
2.10. Fungicide and Salt Stress Sensitivity Assay
2.11. MoABC-R1 Response to Fungicide and Salt Stress
2.12. Pathogenicity Assay
3. Results
3.1. MoABC-R1 Is Required for Fungicide Tolerance in M. oryzae
3.2. MoABC-R1 Encodes a Multidrug Tolerance Protein: ABCC Transporter
3.3. MoABC-R1 Is Not Essential for Inorganic Salt Transportation
3.4. MoABC-R1 Plays a Critical Role in the Pathogenesis of M. oryzae
3.5. The Significance of MoABC-R1 in Fungicide-Based Rice Blast Control
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Schoonbeek, H.; Del, S.G.; De Waard, M.A. The ABC transporter BcatrB affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil. Mol. Plant Microbe Interact. 2001, 14, 562–571. [Google Scholar] [CrossRef]
- Zwiers, L.H.; De Waard, M.A. Characterization of the ABC transporter genes MgAtr1 and MgAtr2 from the wheat pathogen Mycosphaerella graminicola. Fungal Genet. Biol. 2000, 30, 115–125. [Google Scholar] [CrossRef] [PubMed]
- Nakaune, R.; Hamamoto, H.; Imada, J.; Akutsu, K.; Hibi, T. A novel ABC transporter gene, PMR5, is involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Mol. Genet. Genom. 2002, 267, 179–185. [Google Scholar] [CrossRef] [PubMed]
- Miura, H.; Katagiri, M.; Yamaguchi, T.; Uesugi, Y.; Ito, H. Mode of Occurrence of Kasugamycin Resistant Rice Blast Fungus. Ann. Phytopathol. Soc. Japan 1976, 42, 117–123. [Google Scholar] [CrossRef]
- Stergiopoulos, I.; Zwiers, L.; De Waard, M.A. 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. 2002, 108, 719–734. [Google Scholar] [CrossRef]
- Grasso, V.; Palermo, S.; Sierotzki, H.; Garibaldi, A.; Gisi, U. Cytochrome b gene structure and consequences for resistance to Qo inhibitor fungicides in plant pathogens. Pest Manag. Sci. 2006, 62, 465–472. [Google Scholar] [CrossRef]
- Wang, Z.Q.; Meng, F.Z.; Zhang, M.M.; Yin, L.F.; Yin, W.X.; Lin, Y.; Hsiang, T.; Peng, Y.L.; Wang, Z.H.; Luo, C.X. A Putative Zn2Cys6 Transcription Factor Is Associated with Isoprothiolane Resistance in Magnaporthe oryzae. Front. Microbiol. 2018, 9, 2608. [Google Scholar] [CrossRef]
- Gisi, U.; Sierotzki, H.; Cook, A.; McCaffery, A. Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Manag. Sci. 2002, 58, 859–867. [Google Scholar] [CrossRef]
- Fernandez-Ortuno, D.; Tores, J.A.; de Vicente, A.; Perez-Garcia, A. Mechanisms of resistance to QoI fungicides in phytopathogenic fungi. Int. Microbiol. 2008, 11, 1–9. [Google Scholar]
- Avila Adame, C.; Koller, W. Characterization of spontaneous mutants of Magnaporthe grisea expressing stable resistance to the Qo-inhibiting fungicide azoxystrobin. Curr. Genet. 2003, 42, 332–338. [Google Scholar] [CrossRef]
- Liu, P.; Wang, H.; Zhou, Y.; Meng, Q.; Si, N.; Hao, J.J.; Liu, X. Evaluation of fungicides enestroburin and SYP1620 on their inhibitory activities to fungi and oomycetes and systemic translocation in plants. Pestic Biochem. Physiol. 2014, 112, 19–25. [Google Scholar] [CrossRef] [PubMed]
- Vincelli, P.; Dixon, E. Resistance to QoI (Strobilurin-like) Fungicides in Isolates of Pyricularia grisea from Perennial Ryegrass. Plant Dis. 2002, 86, 235–240. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.; Dixon, E.W.; Vincelli, P.; Farman, M.L. Field Resistance to Strobilurin (Q(o)I) Fungicides in Pyricularia grisea Caused by Mutations in the Mitochondrial Cytochrome b Gene. Phytopathology 2003, 93, 891–900. [Google Scholar] [CrossRef] [PubMed]
- Avila-Adame, C.; Koller, W. Disruption of the alternative oxidase gene in Magnaporthe grisea and its impact on host infection. Mol. Plant Microbe Interact. 2002, 15, 493–500. [Google Scholar] [CrossRef]
- Frenkel, O.; Cadle-Davidson, L.; Wilcox, W.F.; Milgroom, M.G. Mechanisms of Resistance to an Azole Fungicide in the Grapevine Powdery Mildew Fungus, Erysiphe necator. Phytopathology 2015, 105, 370–377. [Google Scholar] [CrossRef]
- de Waard, M.A.; Andrade, A.C.; Hayashi, K.; Schoonbeek, H.J.; Stergiopoulos, I.; Zwiers, L.H. Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Manag. Sci. 2006, 62, 195–207. [Google Scholar] [CrossRef]
- Sipos, G.; Kuchler, K. Fungal ATP-binding cassette (ABC) transporters in drug resistance & detoxification. Curr. Drug Targets 2006, 7, 471–481. [Google Scholar]
- Ma, Z.; Michailides, T.J. Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Prot. 2005, 24, 853–863. [Google Scholar] [CrossRef]
- Rees, D.C.; Johnson, E.; Lewinson, O. ABC transporters: The power to change. Nat. Rev. Mol. Cell Biol. 2009, 10, 218–227. [Google Scholar] [CrossRef]
- Yin, Y.; Wang, Z.; Cheng, D.; Chen, X.; Chen, Y.; Ma, Z. The ATP-binding protein FgArb1 is essential for penetration, infectious and normal growth of Fusarium graminearum. New Phytol. 2018, 219, 1447–1466. [Google Scholar] [CrossRef]
- Jones, P.M.; George, A.M. The ABC transporter structure and mechanism: Perspectives on recent research. Cell. Mol. Life Sci. 2004, 61, 682–699. [Google Scholar] [CrossRef] [PubMed]
- Wright, J.; Muench, S.P.; Goldman, A.; Baker, A. Substrate polyspecificity and conformational relevance in ABC transporters: New insights from structural studies. Biochem. Soc. Trans. 2018, 46, 1475–1484. [Google Scholar] [CrossRef] [PubMed]
- Beis, K.; Rebuffat, S. Multifaceted ABC transporters associated to microcin and bacteriocin export. Res. Microbiol. 2019, 170, 399–406. [Google Scholar] [CrossRef]
- Moussatova, A.; Kandt, C.; O’Mara, M.L.; Tieleman, D.P. ATP-binding cassette transporters in Escherichia coli. Biochim. Biophys. Acta 2008, 1778, 1757–1771. [Google Scholar] [CrossRef] [PubMed]
- Jones, P.M.; O’Mara, M.L.; George, A.M. ABC transporters: A riddle wrapped in a mystery inside an enigma. Trends Biochem. Sci. 2009, 34, 520–531. [Google Scholar] [CrossRef] [PubMed]
- Lefevre, F.; Boutry, M. Towards Identification of the Substrates of ATP-Binding Cassette Transporters. Plant Physiol. 2018, 178, 18–39. [Google Scholar] [CrossRef]
- Szollosi, D.; Rose-Sperling, D.; Hellmich, U.A.; Stockner, T. Comparison of mechanistic transport cycle models of ABC exporters. Biochim. Biophys. Acta Biomembr. 2018, 1860, 818–832. [Google Scholar] [CrossRef]
- Ford, R.C.; Beis, K. Learning the ABCs one at a time: Structure and mechanism of ABC transporters. Biochem. Soc. Trans. 2019, 47, 23–36. [Google Scholar] [CrossRef]
- Quazi, F.; Lenevich, S.; Molday, R.S. ABCA4 is an N-retinylidene-phosphatidylethanolamine and phosphatidylethanolamine importer. Nat. Commun. 2012, 3, 925. [Google Scholar] [CrossRef]
- Deeley, R.G.; Westlake, C.; Cole, S.P. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol. Rev. 2006, 86, 849–899. [Google Scholar] [CrossRef]
- Tanaka, K.J.; Song, S.; Mason, K.; Pinkett, H.W. Selective substrate uptake: The role of ATP-binding cassette (ABC) importers in pathogenesis. Biochim. Biophys. Acta Biomembr. 2018, 1860, 868–877. [Google Scholar] [CrossRef] [PubMed]
- Srikant, S.; Gaudet, R. Mechanics and pharmacology of substrate selection and transport by eukaryotic ABC exporters. Nat. Struct. Mol. Biol. 2019, 26, 792–801. [Google Scholar] [CrossRef] [PubMed]
- Aravind, L.; Walker, D.R.; Koonin, E.V. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res. 1999, 27, 1223–1242. [Google Scholar] [CrossRef] [PubMed]
- Khandelwal, N.K.; Kaemmer, P.; Forster, T.M.; Singh, A.; Coste, A.T.; Andes, D.R.; Hube, B.; Sanglard, D.; Chauhan, N.; Kaur, R.; et al. Pleiotropic effects of the vacuolar ABC transporter MLT1 of Candida albicans on cell function and virulence. Biochem. J. 2016, 473, 1537–1552. [Google Scholar] [CrossRef]
- Huang, H.; Lu-Bo, Y.; Haddad, G.G. A Drosophila ABC transporter regulates lifespan. PLoS Genet. 2014, 10, e1004844. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Qi, P.F.; Zhang, Y.Z.; Liu, C.H.; Zhu, J.; Chen, Q.; Guo, Z.R.; Wang, Y.; Xu, B.J.; Zheng, T.; Jiang, Y.F.; et al. Fusarium graminearum ATP-Binding Cassette Transporter Gene FgABCC9 Is Required for Its Transportation of Salicylic Acid, Fungicide Resistance, Mycelial Growth and Pathogenicity towards Wheat. Int. J. Mol. Sci. 2018, 19, 2351. [Google Scholar] [CrossRef]
- Gottesman, M.M.; Fojo, T.; Bates, S.E. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat. Rev. Cancer 2002, 2, 48–58. [Google Scholar] [CrossRef]
- Gottesman, M.M. Mechanisms of cancer drug resistance. Annu. Rev. Med. 2002, 53, 615–627. [Google Scholar] [CrossRef]
- Kretschmer, M.; Leroch, M.; Mosbach, A.; Walker, A.S.; Fillinger, S.; Mernke, D.; Schoonbeek, H.J.; Pradier, J.M.; Leroux, P.; De Waard, M.A.; et al. Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog. 2009, 5, e1000696. [Google Scholar] [CrossRef]
- Abou, A.G.; Tryono, R.; Doll, K.; Karlovsky, P.; Deising, H.B.; Wirsel, S.G. Identification of ABC transporter genes of Fusarium graminearum with roles in azole tolerance and/or virulence. PLoS ONE 2013, 8, e79042. [Google Scholar]
- Kim, S.; Park, S.Y.; Kim, H.; Kim, D.; Lee, S.W.; Kim, H.T.; Lee, J.H.; Choi, W. Isolation and Characterization of the Colletotrichum acutatum ABC Transporter CaABC1. Plant Pathol. J. 2014, 30, 375–383. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.; Park, S.Y.; Kim, D.; Choi, J.; Lee, Y.H.; Lee, J.H.; Choi, W. Genome-scale analysis of ABC transporter genes and characterization of the ABCC type transporter genes in Magnaporthe oryzae. Genomics 2013, 101, 354–361. [Google Scholar] [CrossRef] [PubMed]
- Urban, M.; Bhargava, T.; Hamer, J.E. An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J. 1999, 18, 512–521. [Google Scholar] [CrossRef]
- Gupta, A.; Chattoo, B.B. Functional analysis of a novel ABC transporter ABC4 from Magnaporthe grisea. FEMS Microbiol. Lett. 2008, 278, 22–28. [Google Scholar] [CrossRef]
- Young, J.L.; Kyosuke, Y.; Hiroshi, H.; Ryoji, N. A Novel ABC Transporter Gene ABC2 Involved in Multidrug Susceptibility but not Pathogenicity in Rice Blast Fungus, Magnaporthe grisea. Pestic Biochem. Physiol. 2005, 81, 13–23. [Google Scholar]
- Patkar, R.N.; Xue, Y.K.; Shui, G.; Wenk, M.R.; Naqvi, N.I. Abc3-mediated efflux of an endogenous digoxin-like steroidal glycoside by Magnaporthe oryzae is necessary for host invasion during blast disease. PLoS Pathog. 2012, 8, e1002888. [Google Scholar] [CrossRef] [PubMed]
- Zhou, X.; Li, G.; Xu, J.R. Efficient approaches for generating GFP fusion and epitope-tagging constructs in filamentous fungi. Methods Mol. Biol. 2011, 722, 199–212. [Google Scholar]
- Schwappach, B.; Zerangue, N.; Jan, Y.N.; Jan, L.Y. Molecular basis for K (ATP) assembly: Transmembrane interactions mediate association of a K+ channel with an ABC transporter. Neuron 2000, 26, 155–167. [Google Scholar] [CrossRef]
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Hu, P.; Liu, Y.; Zhu, X.; Kang, H. ABCC Transporter Gene MoABC-R1 Is Associated with Pyraclostrobin Tolerance in Magnaporthe oryzae. J. Fungi 2023, 9, 917. https://doi.org/10.3390/jof9090917
Hu P, Liu Y, Zhu X, Kang H. ABCC Transporter Gene MoABC-R1 Is Associated with Pyraclostrobin Tolerance in Magnaporthe oryzae. Journal of Fungi. 2023; 9(9):917. https://doi.org/10.3390/jof9090917
Chicago/Turabian StyleHu, Pei, Yanchen Liu, Xiaoli Zhu, and Houxiang Kang. 2023. "ABCC Transporter Gene MoABC-R1 Is Associated with Pyraclostrobin Tolerance in Magnaporthe oryzae" Journal of Fungi 9, no. 9: 917. https://doi.org/10.3390/jof9090917