Inhibition of elongation growth by two sesquiterpene lactones isolated from Helianthus annuus L.

Possible molecular mechanism

Abstract

Two sesquiterpene lactones belonging to the germacranolides were isolated from the leaves and stems of Helianthus annuus L. Their formation in the plant is light-dependent. Both sesquiterpene lactones (SL) strongly inhibit indole-3-acetic acid (IAA)-induced elongation growth of Avena sativa L. coleoptile segments and Helianthus annuus L. hypocotyl segments. Both SL do not, however, inhibit acid-induced growth nor growth triggered by fusicoccin at all. In the presence of dithiothreitol (DTT), the inhibitory effect of SL in the Avena-segment-test can be completely neutralized. This can be attributed to the binding of DTT to both SL. Using thin-layer-chromatography it could be shown that the inhibitors build adducts with SH-rich compounds, e.g., cysteine, glutathione, mercapto-ethanol, and DTT, whose Rf-value significantly differs from those of the primary substances. If the coleoptile segments are first treated with an inhibitor and the inhibitor is subsequently washed out, close to normal elongation growth can be induced by adding an IAA-solution. If the segments are simultaneously treated with inhibitor and IAA, no notable growth can be initiated for an extended amount of time, after the removal of both substances and the anewed addition of IAA. Fusicoccin, however, can immediately neutralize the induced growth inhibition. The same irreversible inhibition is observed when 2,4-dichlorophenoxyacetic acid (2,4-D) is used: If coleoptile segments are treated with an inhibitor plus 2,4-D or an inhibitor plus 3,5-dichlorophenoxyacetic acid (3,5-D), respectively, IAA-induced growth after removal of the substances can only be observed by those coleoptiles which had previously been treated with the non-auxin, 3,5-D plus an inhibitor. Based on these results, a possible mechanism describing how the inhibitor functions is discussed. The binding of an auxin to an auxin receptor sets a SH-group free (possibly due to a change in the conformation of the receptor); a site is given to which the inhibitor can bind irreversibly (via a S-bond). The IAA-receptor-inhibitor-complex is then no longer able to initiate elongation growth. If auxin is not present, no lasting bond between the inhibitor and the receptor can occur, since the essential SH-group remains masked. The inhibitor can be washed out again. Consequently, the SL's have to be able to intervene at the beginning of the IAA-induced reaction sequence, while the following steps remain uninfluenced, i.e. namely, the active excretion of protons into the cell wall compartments, which is directly induced by fusicoccin and causes elongation growth.

This is a preview of subscription content, log in to check access.

Abbreviations

2,4-D:

2,4-dichlorophenoxy-acetic acid

3,5-D:

3,5-dichlorophenoxy-acetic acid

DTT:

dithiothreitol

FC:

Fusicoccin

GA3 :

gibberellic acid

IAA:

indole-3-acetic acid

MES:

2-(N-morpholino)-ethane sulfonic acid

SL:

sesquiterpene lactone(s)

References

  1. Baruah, N.C., Sharma, R.P., Madhusudanam, K.P., Thyagarajan, G., Herz, W., Murari, R. (1979) Sesquiterpene lactones of Tithonia diversifolia. Stereochemistry of tagitinins and related compounds. J. Org. Chem. 44, 1831–1835

    Google Scholar 

  2. Bates, G.W., Cleland, R.E. (1979) Protein synthesis and auxininduced growth: inhibitor studies. Planta 145, 437–442

    Google Scholar 

  3. Cleland, R.E. (1971) Cell wall extension. Annu. Rev. Plant Physiol. 22, 197–222

    Google Scholar 

  4. Cleland, R., Rayle, D. (1978) Auxin, H+-excretion and cell elongation. Bot. Mag., Special issue 1, 125–139

    Google Scholar 

  5. Dohrmann, U., Hertel, R., Kowalik, H. (1978) Properties of auxin binding in different subcellular fractions from maize coleoptiles. Planta 140, 97–106

    Google Scholar 

  6. Hager, A. (1962) Untersuchungen über einen durch H+-Ionen induzierbaren Zellstreckungsmechanismus. Habil. Schrift, Naturwiss. Fakultät, Universität München

  7. Hager, A. (1980) Avena coleoptile segments: hyperelongation growth after anaerobic treatment. Z. Naturforsch. 35c, 794–804

    Google Scholar 

  8. Hager, A., Frenzel, R., Laible, D. (1980) ATP-dependent proton transport into vesicles of microsomal membranes of Zea mays coleoptiles. Z. Naturforsch. 35c, 783–793

    Google Scholar 

  9. Hager, A., Helmle, M. (1981) Properties of an ATP-fueled Cl--dependent proton pump localized in membranes of microsomal vesicles from maize coleoptiles. Z. Naturforsch. 36c, 997–1008

    Google Scholar 

  10. Hager, A., Hermsdorf, P. (1981) H+/Ca2+ antiporter in membranes of microsomal vesicles from maize coleoptiles, a secondary energized Ca2+ pump. Z. Naturforsch. 36c, 1009–1012

    Google Scholar 

  11. Hager, A., Menzel, H., Krauss, A. (1971) Versuche und Hypothese zur Primärwirkung des Auxins beim Streckungswachstum. Planta 100, 47–75

    Google Scholar 

  12. Hegnauer, R. (1964) Chemotaxonomie der Pflanzen, vol. 3, pp. 447–544. Birkhäuser, Basel

    Google Scholar 

  13. Heroult V. (1971) Chemotaxonomy of the family Compositae. In: Pharmacognosy and phytochemistry, pp. 93–110, Wagner, H., Hörhammer, L., eds, Springer, Berlin Heidelberg New York

    Google Scholar 

  14. Heroult, V., Sorm, F. (1969) Chemotaxonomy of the sesquiterpenoids of the Compositae. In: Perspectives in phytochemistry, pp. 139–165, Harborne, J.B., Swain, T., eds. Academic Press, London New York

    Google Scholar 

  15. Hertel, R. (1979) Auxin receptors in plant membranes: subcellular fractionation and specific binding assays. In: Plant organelles. Methodological surveys in biochemistry, vol. 9, pp. 173–183, Reid, E., ed. Ellis Horwood, Chichester

    Google Scholar 

  16. Herz, W., Sharma, R.P. (1975) A trans-1,2-cis-4,5-germacranolide and other new germacranolides from Tithonia species. J. Org. Chem. 40, 3118–3123

    Google Scholar 

  17. Herz, W., Kumar, N. (1981) Heliangolides from Helianthus maximiliani. Phytochemistry 20, 93–98

    Google Scholar 

  18. Kalsi, P.S., Vij, V.K., Singh, O.S., Wadia, M.S. (1977) Terpenoid lactones as plant growth regulators. Phytochemistry 16, 784–786

    Google Scholar 

  19. Kalsi, P.S., Gupta, D., Dhillon, R.S., Arora, G.S., Talwar, K.K., Wadia, M.S. (1981) Plant growth activity of guaianolides with C-4 oxygen-containing groups. Phytochemistry 20, 1539–1542

    Google Scholar 

  20. Kefeli, V.J., Kadyrov, C.S. (1971) Natural growth inhibitors, their chemical and physiological properties. Annu. Rev. Plant Physiol. 22, 185–196

    Google Scholar 

  21. Kefeli, V.J. (1977) Natural plant growth inhibitors and phytohormones. Dr. W. Junk. The Hague

    Google Scholar 

  22. Krauss, A. (1971) Untersuchungen zum Streckungswachstum der Pflanzen. Diss., Ludwig-Maximilians-Universität, München

    Google Scholar 

  23. Kupchan, S.M., Fessler, D.C., Eakin, M.A., Giacobbe, T.J. (1970) Reactions of alpha methylene lactone tumor inhibitors with model biological nucleophiles. Science 168, 376–378

    Google Scholar 

  24. Lado, P., Caldogno, F.R., Pennachioni, A., Marrè, E. (1973) Mechanism of growth promoting action of fusicoccin. Planta 110, 311–320

    Google Scholar 

  25. Lee, K.-H., Ibuka, T., Wu, R.-Y., Geissmann, T.A. (1977a) Structure-antimicrobial activity relationships among the sesquiterpene lactones and related compounds. Phytochemistry 16, 1177–1181

    Google Scholar 

  26. Lee, K.-H., Hall, J.H., Mar, E.C., Starnes, C., El Gebaly, S.A., Waddell, T.G., Hadgraft, R.J., Ruffner, c.G., Weidner, J. (1977b) Sesquiterpene antitumor agents: inhibitors of cellular metabolism. Science 196, 533–536

    Google Scholar 

  27. Marrè, E. (1977) Effect of fusicoccin and hormones on plant cell membrane activities: Observations and hypothesis. In: Regulation of cell membrane activities in plants, pp. 185–201, Marrè, E., Ciferri, O., eds. Elsevier-North-Holland, Amsterdam

    Google Scholar 

  28. Marrè, E. (1979) Fusicoccin: a tool in plant physiology. Annu. Rev. Plant Physiol. 30, 273–288

    Google Scholar 

  29. Ogura, M., Cordell, G.A., Farnsworth, N.R. (1978) Anticancer sesquiterpene lactones of Michella compressa. Phytochemistry 17, 957–961

    Google Scholar 

  30. Ohno, N., Mabry, T.J. (1980) Sesquiterpene lactones and diterpene carboxylic acids in Helianthus niveus. Phytochemistry 19, 609–614

    Google Scholar 

  31. Powell, R.G., Smith, C.R. (1980) Antitumor agents from higher plants. Recent Adv. Phytochem. 14, 23–51

    Google Scholar 

  32. Ray, P.M. (1977) Auxin-binding sites of maize coleoptiles are localized on membranes of endoplasmatic reticulum. Plant Physiol. 59, 594–599

    Google Scholar 

  33. Rayle, D.L., Cleland, R. (1972) The in-vitro acid-growth response: relation to in-vivo growth response and auxin action. Planta 104, 282–296

    Google Scholar 

  34. Rayle, D.L., Cleland, R.E. (1977) Control of plant cell enlargement by hydrogen ions. Curr. Top. Dev. Biol. 34, 187–214

    Google Scholar 

  35. Rodriguez, E., Towers, G.H.N., Mitchell, J.C. (1976) Biological activities of sesquiterpene lactones. Phytochemistry 15, 1573–1580

    Google Scholar 

  36. Rubery, P.H. (1981) Auxin receptors. Annu. Rev. Plant Physiol. 32, 569–596

    Google Scholar 

  37. Sequeira, L., Hemingway, R.J., Kupchan, S.M.(1968) Vernolepin: A new reversible plant growth inhibitor. Science 161, 789–790

    Google Scholar 

  38. Shibaoka, H. (1961) Studies on the mechanism of growth inhibiting effect of light. Plant Cell Physiol. 2, 175–197

    Google Scholar 

  39. Spring, O., Albert, K., Gradmann, W. (1981) Annuithrin, a new biologically active germacranolide from Helianthus annuus Phytochemistry 20, 1883–1885

    Google Scholar 

  40. Spring, O., Albert, K., Hager, A. (1982) New biologically active heliangolides from Helianthus annuus. Phytochemistry 21, (in press)

  41. Spring, O., Kupka, J., Maier, B., Hager, A. (1982) Biological activities of sesquiterpene lactones from Helianthus annuus: Antimicrobial and cytotoxic properties; influence on DNA, RNA and protein synthesis. Z. Naturforsch. 37c (in press)

  42. Venis, M.A. (1977) Receptors for plant hormones. Adv. Bot. Res. 5, 53–88

    Google Scholar 

  43. Willuhn, G. (1981) Neue Ergebnisse der Arnikaforschung. Pharmazie in unserer Zeit 10, 1–7

    Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Spring, O., Hager, A. Inhibition of elongation growth by two sesquiterpene lactones isolated from Helianthus annuus L.. Planta 156, 433–440 (1982). https://doi.org/10.1007/BF00393314

Download citation

Key words

  • Auxin receptor
  • Elongation growth
  • Helianthus
  • Sesquiterpene lactone