Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Detection and cellular localization of elemental sulphur in disease-resistant genotypes of Theobroma cacao

Nature volume 379, pages 159–162 (1996)Cite this article

Abstract

DISEASE-RESISTANT genotypes are the basis for controlling many major microbial pathogens of economic plants. Resistance is often linked with organic, antimicrobial phytoalexins, produced de novo in cells surrounding apoptotic or 'hypersensitive' cells that die rapidly after contact with incompatible pathogens1–3. Here we report the production by resistant genotypes of Theobroma cacaoof four phytoalexins in response to a xylem-invading fungal pathogen; these comprised two phenolics, a triterpenoid and, highly unusually in a higher eukaryote, elemental sulphur as cyclooctasulphur S8. Energy-dispersive X-ray microanalysis revealed a high accumulation of sulphur only in cells and structures in potential contact with the vascular pathogen; that is, xylem parenchyma, xylem vessel cell walls and gels occluding vessels. Our data provide a rare example of cellular localization of an antimicrobial substance and evidence for the first time for accumulation of elemental sulphur in a plant linked with a resistance response; this discovery comes centuries after man first used elemental sulphur as a potent fungicide4,5.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Mansfield, J. M. in Natural Antimicrobial Systems (eds Gould, G.W. et al.) 191–205 (Bath Univ. Press, 1986).

    Google Scholar 

  2. Bailey, J. A. & Mansfield, J. W. Phytoalexins (Blackie, Glasgow, 1982).

    Google Scholar 

  3. Darvill, A. G. & Albersheim, P. A. Rev. Pl. Physiol. 35, 243–275 (1984).

    Article  CAS  Google Scholar 

  4. Tweedy, B. G. Residue Rev. 78, 43–68 (1981).

    CAS  Google Scholar 

  5. Legris-Delaporte, S., Ferron, F., Landry, J. & Coster, C. Pl. Physiol. 85, 1026–1030 (1987).

    Article  CAS  Google Scholar 

  6. Holderness, M. Biochemist 2, 11–13 (1993).

    Google Scholar 

  7. Resende, M. L. V., Flood, J. & Cooper, R. M. Pl. Path. 44, 374–383 (1995).

    Article  Google Scholar 

  8. Yaguchi, Y., Sakurai, N., Nagai, M. & Inoue, T. Chem. Pharm. Bull. 36, 1419–1424 (1988).

    Article  CAS  Google Scholar 

  9. Davies, J. R. & Thuraisingham, S. T. J. Chromatogr. 35, 513–518 (1968).

    Article  CAS  Google Scholar 

  10. Devys, M. et al. Tetrahedron Lett. 29, 6447–6448 (1988).

    Article  CAS  Google Scholar 

  11. Young, L. & Maw, G. A. The Metabolism of Sulphur Compounds (Methuen, London, 1958).

    Google Scholar 

  12. Joyard, J., Fores, E., Blée, E. & Douce, R. Pl. Physiol. 88, 961–964 (1988).

    Article  CAS  Google Scholar 

  13. Izak, R. R., Stierle, D. B. & Sims, J. J. Phytochemisfry 21, 229 (1982).

    Article  Google Scholar 

  14. Steudel, R., Holdt, G., Visscher, P. T. & Van Gemerden, H. Arch. Microbiol. 153, 432–437 (1990).

    Article  CAS  Google Scholar 

  15. Kylin, H., Atuma, S., Hovander, L. & Jensen, S. Experientia 50, 80–85 (1994).

    Article  CAS  Google Scholar 

  16. Mansfield, J. W., Hargreaves, J. A. & Boyle, F. C. Nature 252, 316–317 (1974).

    Article  ADS  CAS  Google Scholar 

  17. Mayana, S. & Tani, T. Physiol. Pl. Path. 21, 141–149 (1982).

    Article  Google Scholar 

  18. Mace, M. E., Bell, A. A. & Beckman, C. H. Can. J. Bot. 54, 2095–2099 (1976).

    Article  CAS  Google Scholar 

  19. Moesta, P., Seydel, U., Lindner, B. & Grisebach, H. Z. Naturf. 37c, 748–751 (1982).

    Article  CAS  Google Scholar 

  20. Hahn, M. G., Bonhoff, A. & Grisebach, H. Pl. Physiol. 77, 591–601 (1985).

    Article  CAS  Google Scholar 

  21. Cooper, R. M. in Plant Disease Control: Resistance and Susceptibility (eds Staples, R. C. & Toenniesen, G. H.) 105–142 (Wiley, New York, 1981).

    Google Scholar 

  22. Durrands, P. K. & Cooper, R. M. Physiol. molec. Pl. Path. 32, 343–362 (1988).

    Article  CAS  Google Scholar 

  23. Ward, E. W. B., Stoessl, A. & Stothers, J. B. Phytochemistry 16, 2024–2025 (1977).

    Article  CAS  Google Scholar 

  24. Jolivet, P., Bergeron, E., Zimierski, A. & Meunier, J.-C. Phytochemistry 38, 9–14 (1995).

    Article  CAS  Google Scholar 

  25. Beffa, T. Can. J. Microbiol. 39, 736–741 (1993).

    Article  CAS  Google Scholar 

  26. Diallo, B., et al. J. nat. Prod. 52, 879–881 (1989).

    Article  CAS  Google Scholar 

  27. Gottstein, D. & Cross, D. Trees Struct. Funct. 6, 55–68 (1992).

    Article  Google Scholar 

  28. Jensen, J. S. & Lokke, H. J. Pl. Dis. Prot. 97, 328–338 (1990).

    CAS  Google Scholar 

  29. Kokubun, T., Harborne, J. B. & Eagles, J. Phytochemistry 35, 331–333 (1994).

    Article  CAS  Google Scholar 

  30. Ride, J. P. in Biochemical Plant Pathology (ed. Callow, J.) 215–236 (Wiley, Chichester, 1983).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biology and Biochemistry, University of Bath, Bath, Avon, BA2 7AY, UK

    Richard M. Cooper, Mario L. V. Resende & Julie Flood

  2. School of Pharmacy and pharmacology, University of Bath, Bath, Avon, BA2 7AY, UK

    Michael G. Rowan

  3. School of Materials Science, University of Bath, Bath, Avon, BA2 7AY, UK

    Ursula Potter

  4. IACR, Long Ashton Research Station, Department of Agricultural Sciences, University of Bristol, Long Ashton, Avon, BS18 9AF, UK

    Michael H. Beale

Authors
  1. Richard M. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mario L. V. Resende
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julie Flood
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael G. Rowan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael H. Beale
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ursula Potter
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cooper, R., Resende, M., Flood, J. et al. Detection and cellular localization of elemental sulphur in disease-resistant genotypes of Theobroma cacao. Nature 379, 159–162 (1996). https://doi.org/10.1038/379159a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/379159a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing