1887

Abstract

Cercosporin is a non-host-selective, photoactivated polyketide toxin produced by many phytopathogenic species, which plays a crucial role during pathogenesis on host plants. Upon illumination, cercosporin converts oxygen molecules to toxic superoxide and singlet oxygen that damage various cellular components and induce lipid peroxidation and electrolyte leakage. Three genes (, and ) encoding putative FAD/FMN- or NADPH-dependent oxidoreductases in the cercosporin toxin biosynthetic pathway of were functionally analysed. Replacement of each gene via double recombination was utilized to create null mutant strains that were completely impaired in cercosporin production as a consequence of specific interruption at the , or locus. Expression of , , , and was drastically reduced or nearly abolished when , or was disrupted. Production of cercosporin was revived when a functional gene cassette was introduced into the respective mutants. All , and null mutants retained wild-type levels of resistance against toxicity of cercosporin or singlet-oxygen-generating compounds, indicating that none of the genes plays a role in self-protection.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/007294-0
2007-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/8/2781.html?itemId=/content/journal/micro/10.1099/mic.0.2007/007294-0&mimeType=html&fmt=ahah

References

  1. Alexander N. J., McCormick S. P., Hohn T. M. 1999; TRI12, a trichothecene efflux pump from Fusarium sporotrichioides : gene isolation and expression in yeast. Mol Gen Genet 261:977–984
    [Google Scholar]
  2. August P. R., Flickinger M. C., Sherman D. H. 1994; Cloning and analysis of a locus ( mcr ) involved in mitomycin C resistance in Streptomyces lavendulae . J Bacteriol 176:4448–4454
    [Google Scholar]
  3. Bell P. E., Nau C. D., Brown J. T., Konisky J., Kadner R. J. 1990; Genetic suppression demonstrates interaction of TonB protein with outer membrane transport proteins in Escherichia coli . J Bacteriol 172:3826–3829
    [Google Scholar]
  4. Callahan T. M., Rose M. S., Meade M. J., Ehrenshaft M., Upchurch R. G. 1999; CFP, the putative cercosporin transporter of Cercospora kikuchii , is required for wild type cercosporin production, resistance, and virulence on soybean. Mol Plant Microbe Interact 12:901–910
    [Google Scholar]
  5. Chen H., Lee M.-H., Daub M. E., Chung K.-R. 2007; Molecular analysis of the cercosporin biosynthetic gene cluster in Cercospora nicotianae . Mol Microbiol 64:755–770
    [Google Scholar]
  6. Choquer M., Dekkers K. A., Chen H.-Q., Ueng P. P., Daub M. E., Chung K.-R. 2005; The CTB1 gene encoding a fungal polyketide synthase is required for cercosporin biosynthesis and fungal virulence of Cercospora nicotianae . Mol Plant Microbe Interact 18:468–476
    [Google Scholar]
  7. Choquer M., Lee M. H., Bau H. J., Chung K. R. 2007; Deletion of a MFS transporter-like gene in Cercospora nicotianae reduces cercosporin toxin accumulation and fungal virulence. FEBS Lett 581:489–494
    [Google Scholar]
  8. Chung K.-R. 2003; Involvement of calcium/calmodulin signaling in cercosporin toxin biosynthesis by Cercospora nicotianae . Appl Environ Microbiol 69:1187–1196
    [Google Scholar]
  9. Chung K.-R., Jenns A. E., Ehrenshaft M., Daub M. E. 1999; A novel gene required for cercosporin toxin resistance in the fungus, Cercospora nicotianae . Mol Gen Genet 262:382–389
    [Google Scholar]
  10. Chung K.-R., Shilts T., Li W., Timmer L. W. 2002; Engineering a genetic transformation system for Colletotrichum acutatum , the causal fungus of lime anthracnose and postbloom fruit drop. FEMS Microbiol Lett 213:33–39
    [Google Scholar]
  11. Chung K.-R., Daub M. E., Kuchler K., Schüller C. 2003a; The CRG1 gene required for resistance to the singlet oxygen-generating cercosporin toxin in Cercospora nicotianae encodes a putative fungal transcription factor. Biochem Biophys Res Commun 302:302–310
    [Google Scholar]
  12. Chung K.-R., Ehrenshaft M., Wetzel D. K., Daub M. E. 2003b; Cercosporin- deficient mutants by plasmid tagging in the asexual fungus Cercospora nicotianae . Mol Genet Genomics 270:103–113
    [Google Scholar]
  13. Daub M. E. 1982; Peroxidation of tobacco membrane lipids by the photosensitizing toxin, cercosporin. Plant Physiol 69:1361–1364
    [Google Scholar]
  14. Daub M. E., Briggs S. P. 1983; Changes in tobacco cell membrane composition and structure caused by the fungal toxin, cercosporin. Plant Physiol 71:763–766
    [Google Scholar]
  15. Daub M. E., Ehrenshaft M. 2000; The photoactivated Cercospora toxin cercosporin: contributions to plant disease and fundamental biology. Annu Rev Phytopathol 38:461–490
    [Google Scholar]
  16. Daub M. E., Hangarter R. P. 1983; Production of singlet oxygen and superoxide by the fungal toxin, cercosporin. Plant Physiol 73:855–857
    [Google Scholar]
  17. Daub M. E., Leisman G. B., Clark R. A., Bowden E. F. 1992; Reduced detoxification as a mechanism of fungal resistance to singlet-oxygen-generating photosensitizers. Proc Natl Acad Sci U S A 89:9588–9592
    [Google Scholar]
  18. Daub M. E., Li M., Bilski P., Chignell C. F. 2000; Dihydrocercosporin singlet oxygen production and subcellular localization: a possible defense against cercosporin phototoxicity in Cercospora . Photochem Photobiol 71:135–140
    [Google Scholar]
  19. Daub M. E., Herrero S., Chung K.-R. 2005; Photoactivated perylenequinone toxins in fungal pathogenesis of plants. FEMS Microbiol Lett 252:197–206
    [Google Scholar]
  20. Dekkers K. L., You B.-J., Gowda V. S., Liao H.-L., Lee M.-H., Bau H.-J., Ueng P. P., Chung K.-R. 2007; The Cercospora nicotianae gene encoding dual O -methyltransferase and FAD-dependent monooxygenase domains mediates cercosporin toxin biosynthesis. Fungal Genet Biol 44:444–454
    [Google Scholar]
  21. Ehrenshaft M., Upchurch R. G. 1991; Isolation of light-enhanced cDNAs of Cercospora kikuchii . Appl Environ Microbiol 57:2671–2676
    [Google Scholar]
  22. Ehrenshaft M., Jenns A. E., Chung K.-R., Daub M. E. 1998; SOR1 , a gene required for photosensitizer and singlet oxygen resistance in Cercospora fungi, is highly conserved in divergent organisms. Mol Cell 1:603–609
    [Google Scholar]
  23. Ehrenshaft M., Bilski P., Li M. Y., Chignell C. F., Daub M. E. 1999; A highly conserved sequence is a novel gene involved in de novo vitamin B6 biosynthesis. Proc Natl Acad Sci U S A 96:9374–9378
    [Google Scholar]
  24. Goffeau A., Barrell B. G., Bussey H., Davis R. W., Dujon B., Feldmann H., Galibert F., Hoheisel J. D., Jacq C. other authors 1996; Life with 6000 genes. Science 274:546–547
    [Google Scholar]
  25. Huttner W. B. 1988; Tyrosine sulfation and the secretary pathway. Annu Rev Physiol 50:363–376
    [Google Scholar]
  26. Jenns A. E., Daub M. E. 1995; Characterization of mutants of Cercospora nicotianae sensitive to the toxin cercosporin. Phytopathology 85:906–912
    [Google Scholar]
  27. Jenns A. E., Daub M. E., Upchurch R. G. 1989; Regulation of cercosporin accumulation in culture by medium and temperature manipulation. Phytopathology 79:213–219
    [Google Scholar]
  28. Keller N. P., Turner G., Bennett J. W. 2005; Fungal secondary metabolism – from biochemistry to genomics. Nat Rev Microbiol 3:937–947
    [Google Scholar]
  29. Kuyama S., Tamura T. 1957; Cercosporin. A pigment of Cercospora kikuchii Matsumoto et Tomoyasu. II. Physical and chemical properties of cercosporin and its derivatives. J Am Chem Soc 79:5725–5729
    [Google Scholar]
  30. Leisman G. B., Daub M. E. 1992; Singlet oxygen yields, optical properties, and phototoxicity of reduced derivatives of the photosensitizer cercosporin. Photochem Photobiol 55:373–379
    [Google Scholar]
  31. Okubo A., Yamazaki S., Fuwa K. 1975; Biosynthesis of cercosporin. Agric Biol Chem 39:1173–1175
    [Google Scholar]
  32. Panagiotis M., Kritonas K., Irini N. O., Kiriaki C., Nicolaos P., Athanasios T. 2007; Expression of the yeast cpd1 gene in tobacco confers resistance to the fungal toxin cercosporin. Biomol Eng 24:245–251
    [Google Scholar]
  33. Pitkin J. W., Panaccione D. G., Walton J. D. 1996; A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum . Microbiology 142:1557–1565
    [Google Scholar]
  34. Rule G. S., Pratt E. A., Chin C. C., Wold F., Ho C. 1985; Overproduction and nucleotide sequence of the respiratory d-lactate dehydrogenase of Escherichia coli . J Bacteriol 161:1059–1068
    [Google Scholar]
  35. Schafer W. 1994; Molecular mechanisms of fungal pathogenicity to plants. Annu Rev Phytopathol 32:461–477
    [Google Scholar]
  36. Shim W.-B., Dunkle L. D. 2003; CZK3 , a MAP kinase kinase kinase homolog in Cercospora zeae-maydis , regulates cercosporin biosynthesis, fungal development, and pathogenesis. Mol Plant Microbe Interact 16:760–768
    [Google Scholar]
  37. Sollod C. C., Jenns A. J., Daub M. E. 1992; Cell surface redox potential as a mechanism of defense against photosensitizers in fungi. Appl Environ Microbiol 58:444–449
    [Google Scholar]
  38. Sweigard J. A., Chumley F. C., Carroll A. M., Farrall L., Valent B. 1997; A series of vectors for fungal transformation. Fungal Genet Newsl 44:52–53
    [Google Scholar]
  39. Taylor T. V., Mitchell T. K., Daub M. E. 2006; An oxidoreductase is involved in cercosporin degradation by the bacterium Xanthomonas campestris pv. zinniae . Appl Environ Microbiol 72:6070–6078
    [Google Scholar]
  40. Upchurch R. G., Walker D. C., Rollins J. A., Ehrenshaft M., Daub M. E. 1991; Mutants of Cercospora kikuchii altered in cercosporin synthesis and pathogenicity. Appl Environ Microbiol 57:2940–2945
    [Google Scholar]
  41. van den Heuvel R. H. H., Fraaije M. W., Mattevi A., van Berkel W. J. H. 2000; Asp-170 is crucial for the redox properties of vanillyl-alcohol oxidase. J Biol Chem 275:14799–14808
    [Google Scholar]
  42. Walton J. D. 1996; Host-selective toxins: agents of compatibility. Plant Cell 8:1723–1733
    [Google Scholar]
  43. Yamazaki S., Ogawa T. 1972; The chemistry and stereochemistry of cercosporin. Agric Biol Chem 36:1707–1718
    [Google Scholar]
  44. Yamazaki S., Okube A., Akiyama Y., Fuwa K. 1975; Cercosporin, a novel photodynamic pigment isolated from Cercospora kikuchii . Agric Biol Chem 39:287–288
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/007294-0
Loading
/content/journal/micro/10.1099/mic.0.2007/007294-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error