Plant Cell Reports

, Volume 28, Issue 12, pp 1895–1903

Streptomyces scabiei and its toxin thaxtomin A induce scopoletin biosynthesis in tobacco and Arabidopsis thaliana

  • Sylvain Lerat
  • Amadou H. Babana
  • Mohamed El Oirdi
  • Abdelbassed El Hadrami
  • Fouad Daayf
  • Nathalie Beaudoin
  • Kamal Bouarab
  • Carole Beaulieu
Original Paper


Streptomyces scabiei is the predominant causal agent of common scab of potato in North America. The virulence of common scab-causing streptomycetes relies on their capacity to synthesize thaxtomins. In this study, the effects of S. scabiei infection and of thaxtomin A, the main toxin produced by S. scabiei, were tested for the elicitation of plant defense molecules in the model plants tobacco (Nicotiana tabacum) and Arabidopsis thaliana. Tobacco leaves infected with spores of S. scabiei strain EF-35 or infiltrated with purified thaxtomin A produced a blue fluorescent compound that was not detected in leaves infiltrated with spores of a S. scabiei mutant deficient in thaxtomin A biosynthesis. Thin layer chromatography and high performance liquid chromatography identified this fluorescent compound as scopoletin, a plant defense phytoalexin. Arabidopsis seedlings grown in liquid medium also excreted scopoletin as a reaction to S. scabiei and thaxtomin A. The effects of the presence of scopoletin on S. scabiei were also investigated. The phytoalexin scopoletin caused a slight reduction of bacterial growth and a severe decrease of thaxtomin A production. Scopoletin was shown to inhibit thaxtomin A production by repression of a gene involved in the toxin biosynthesis.


Common scab Model plants Scopoletin Streptomyces scabiei Thaxtomin A 


  1. Beauséjour J, Goyer C, Vachon J, Beaulieu C (1999) Production of thaxtomin A by Streptomyces scabies strains in plant extract containing-media. Can J Microbiol 45:764–768CrossRefGoogle Scholar
  2. Bischoff V, Cookson SJ, Wu S, Scheible W-R (2009) Thaxtomin A affects CESA-complex density, expression of cell wall genes, cell wall composition, and causes ectopic lignification in Arabidopsis thaliana seedlings. J Exp Bot 60:955–965CrossRefPubMedGoogle Scholar
  3. Carpinella MC, Ferrayoli CG, Palacios SM (2005) Antifungal synergistic effect of scopoletin, a hydroxycoumarin isolated from Melia azedarach L. fruits. J Agr Food Chem 53:2922–2927CrossRefGoogle Scholar
  4. Chong J, Baltz R, Schmitt C, Beffa R, Fritig B, Saindrenan P (2002) Downregulation of a pathogen-responsive tobacco UDP-Glc:phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance. Plant Cell 14:1093–1107CrossRefPubMedGoogle Scholar
  5. Coffeen WC, Wolpert TJ (2004) Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 16:857–873CrossRefPubMedGoogle Scholar
  6. Conn VM, Walker AR, Franco CMM (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21:208–218CrossRefPubMedGoogle Scholar
  7. Curtis MJ, Wolpert TJ (2004) The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity. Plant J 38:244–259CrossRefPubMedGoogle Scholar
  8. Daayf F, Schmitt A, Bélanger RR (1997) Evidence of phytoalexins in cucumber leaves infected with powdery mildew following treatment with leaf extracts of Reynoutria sacchalinensis. Plant Physiol 113:719–727PubMedGoogle Scholar
  9. Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847CrossRefPubMedGoogle Scholar
  10. Doumbou CL, Salove MKH, Crawford DL, Beaulieu C (2001) Actinomycetes, promising tool to control plant diseases and to promote plant growth. Phytoprotection 82:85–102Google Scholar
  11. Duval I, Brochu V, Simard S, Beaulieu C, Beaudoin N (2005) Thaxtomin A induces programmed cell death in Arabidopsis thaliana suspension-cultured cells. Planta 222:820–831CrossRefPubMedGoogle Scholar
  12. Errakhi R, Dauphin A, Meimoun P, Lehner A, Reboutier D, Vatsa P, Briand J, Madiona K, Rona JP, Barakate M, Wendehenne D, Beaulieu C, Bouteau F (2008) An early Ca2+ influx is a prerequisite to thaxtomin A-induced cell death in Arabidopsis thaliana cells. J Exp Bot 59:4259–4270CrossRefPubMedGoogle Scholar
  13. Faucher E, Savard T, Beaulieu C (1992) Characterization of actinomycetes isolated from common scab lesions on potato tubers. Can J Plant Pathol 14:197–202Google Scholar
  14. Fry BA, Loria R (2002) Thaxtomin A: evidence for a plant cell wall target. Physiol Mol Plant Pathol 60:1–8CrossRefGoogle Scholar
  15. Gachon C, Baltz R, Saindrenan P (2004) Over-expression of a scopoletin glucosyltransferase in Nicotiana tabacum leads to precocious lesion formation during the hypersensitive response to tobacco mosaic virus but does not affect virus resistance. Plant Mol Biol 54:137–146CrossRefPubMedGoogle Scholar
  16. Goyer C, Beaulieu C (1997) Host range of streptomycete strains causing common scab. Plant Dis 81:901–904CrossRefGoogle Scholar
  17. Goyer C, Vachon J, Beaulieu C (1998) Pathogenicity of Streptomyces scabies mutants altered in thaxtomin A production. Phytopathology 88:442–445CrossRefPubMedGoogle Scholar
  18. Goyer C, Charest P-M, Toussaint V, Beaulieu C (2000) Ultrastructural effects of thaxtomin A produced by Streptomyces scabies on mature potato tuber tissues. Can J Bot 78:374–380CrossRefGoogle Scholar
  19. Healy FG, Wach M, Krasnoff SB, Gibson DM, Loria R (2000) The txtAB genes of the plant pathogen Streptomyces acidiscabies encode a peptide synthetase required for phytotoxin thaxtomin A production and pathogenicity. Mol Microbiol 38:794–804CrossRefPubMedGoogle Scholar
  20. Hill J, Lazarovits G (2005) A mail survey of growers to estimate potato common scab prevalence and economic loss in Canada. Can J Plant Pathol 27:46–52Google Scholar
  21. Joshi MV, Bignell DRD, Johnson EG, Sparks JP, Gibson DM, Loria R (2007) The AraC/XylS regulator TxtR modulates thaxtomin biosynthesis and virulence in Streptomyces scabies. Mol Microbiol 66:633–642CrossRefPubMedGoogle Scholar
  22. Kai K, Shimizu B-I, Mizutani M, Watanabe K, Sakata K (2006) Accumulation of coumarins in Arabidopsis thaliana. Phytochemistry 67:379–386CrossRefPubMedGoogle Scholar
  23. Kers JA, Wach MJ, Krasnoff SB, Widom J, Cameron KD, Bukhalid RA, Gibson DM, Crane BR, Loria R (2004) Nitration of a peptide phytotoxin by bacterial nitric oxide synthase. Nature 429:79–82CrossRefPubMedGoogle Scholar
  24. King RR, Lawrence CH, Clark MC, Calhoun LA (1989) Isolation and characterization of phytotoxins associated with Streptomyces scabies. J Chem Soc Chem Commun 13:849–850CrossRefGoogle Scholar
  25. King RR, Lawrence CH, Calhoun LA (1992) Chemistry of phytotoxins associated with Streptomyces scabies, the causal organism of potato common scab. J Agr Food Chem 40:834–837CrossRefGoogle Scholar
  26. Lawrence CH, Clark MC, King RR (1990) Induction of common scab symptoms in aseptically cultured potato tubers by the vivotoxin, thaxtomin. Phytopathology 80:606–608CrossRefGoogle Scholar
  27. Leiner RH, Fry BA, Carling DE, Loria R (1996) Probable involvement of thaxtomin A in pathogenicity of Streptomyces scabies on seedlings. Phytopathology 86:709–713CrossRefGoogle Scholar
  28. Lerat S, Simao-Beaunoir A-M, Beaulieu C (2009a) Genetic and physiological determinants of Streptomyces scabies pathogenicity. Mol Plant Pathol 10:579–585CrossRefPubMedGoogle Scholar
  29. Lerat S, Simao-Beaunoir A-M, Wu R, Beaudoin N, Beaulieu C (2009b) Involvement of the plant polymer suberin and the disaccharide cellobiose in triggering thaxtomin A biosynthesis, a phytotoxin produced by the pathogenic agent Streptomyces scabies. Phytopathology (in press)Google Scholar
  30. Manulis S, Shafrir H, Epstein E, Lichter A, Barash I (1994) Biosynthesis of indole-3-acetic-acid via the indole-3-acetamide pathway in Streptomyces spp. Microbiology 140:1045–1050CrossRefPubMedGoogle Scholar
  31. Matros A, Mock HP (2004) Ectopic expression of a UDP-glucose:phenylpropanoid glucosyltransferase leads to increased resistance of transgenic tobacco plants against infection with Potato Virus Y. Plant Cell Physiol 45:1185–1193CrossRefPubMedGoogle Scholar
  32. Nolte P, Secor GA, Gudmestad NC, Henningson PJ (1993) Detection and identification of fluorescent compounds in potato tuber tissue with corky patch syndrome. Am Potato J 70:649–666CrossRefGoogle Scholar
  33. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007CrossRefGoogle Scholar
  34. Scheible W-R, Fry B, Kochevenko A, Schindelasch D, Zimmerli L, Somerville S, Loria R, Somerville CR (2003) An Arabidopsis mutant resistant to thaxtomin A, a cellulose synthesis inhibitor from Streptomyces species. Plant Cell 15:1781–1794CrossRefPubMedGoogle Scholar
  35. Tada Y, Kusaka K, Betsuyaku S, Shinogi T, Sakamoto M, Ohura Y, Hata S, Mori T, Tosa Y, Mayama S (2005) Victorin triggers programmed cell death and the defense response via interaction with a cell surface mediator. Plant Cell Physiol 46:1787–1789CrossRefPubMedGoogle Scholar
  36. Tegg RS, Melian L, Wilson CR, Shabala S (2005) Plant cell growth and ion flux responses to the streptomycete phytotoxin thaxtomin A: calcium and hydrogen flux patterns revealed by the non-invasive MIFE technique. Plant Cell Physiol 46:638–648CrossRefPubMedGoogle Scholar
  37. Tegg RS, Gill WM, Thompson HK, Davies NW, Ross JJ, Wilson CR (2008) Auxin-induced resistance to common scab disease of potato linked to inhibition of thaxtomin A toxicity. Plant Dis 92:1321–1328CrossRefGoogle Scholar
  38. Valle T, Lopez JL, Hernandez JM, Corchete P (1997) Antifungal activity of scopoletin and its differential accumulation in Ulmus pumila and Ulmus campestris cell suspension cultures infected with Ophiostoma ulmi spores. Plant Sci 125:97–101CrossRefGoogle Scholar
  39. Wolpert TJ, Macko V, Acklin W, Jaun B, Seibl J, Meili J, Arigoni D (1985) Structure of victorin C, the major host-selective toxin from Cochliobolus victoriae. Experientia 41:1524–1529CrossRefGoogle Scholar
  40. Yao N, Tada Y, Sakamoto M, Nakayashiki H, Park P, Tosa Y, Mayama S (2002) Mitochondrial oxidative burst involved in apoptotoic response in oats. Plant J 30:567–579CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Sylvain Lerat
    • 1
  • Amadou H. Babana
    • 2
  • Mohamed El Oirdi
    • 1
  • Abdelbassed El Hadrami
    • 3
  • Fouad Daayf
    • 3
  • Nathalie Beaudoin
    • 1
  • Kamal Bouarab
    • 1
  • Carole Beaulieu
    • 1
  1. 1.Centre SÈVE, Département de BiologieUniversité de SherbrookeSherbrookeCanada
  2. 2.Département de BiologieUniversité de BamakoBamakoMali
  3. 3.Department of Plant Science, 222 Agriculture BuildingUniversity of ManitobaWinnipegCanada

Personalised recommendations