Skip to main content
SpringerLink
Log in

Several biotic and abiotic elicitors act synergistically in the induction of phytoalexin accumulation in soybean

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Summary

Plants often respond to microbial infection by producing antimicrobial compounds called phytoalexins. Plants also produce phytoalexins in response to in vitro treatment with molecules called elicitors. Specific elicitors, including a hexa-β-glucosyl glucitol derived from fungal cell walls, the pectin-degrading enzyme endopolygalacturonic acid lyase, and oligogalacturonides obtained by either partial acid hydrolysis or enzymatic degradation of plant cell walls or citrus polygalacturonic acid, induce soybean (Glycine max. L.) cytoledons to accumulate phytoalexins. The experiments reported here demonstrate that the elicitor-active hexa-β-glucosyl glucitol acts synergistically with several biotic and abiotic elicitors in the induction of phytoalexins in soybean cotyledons. At concentrations below 50 ng/ml, the hexa-β-glucosyl glucitol does not induce significant phytoalexin accumulation. When assayed in combination with either endopolygalacturonic acid lyase or with a decagalacturonide released from citrus polygalacturonic acid by this lyase, however, the observed elicitor activity of the hexa-β-glucosyl glucitol is as much as 35-fold higher than the sum of the responses of these elicitors assayed separately. A similar synergism was also demonstrated for the combination of the hexa-β-glucosyl glucitol with dilute solutions of sodium acetate, sodium formate, or sodium propionate buffers. These buffers are thought to damage or kill plant cells, which may cause the release of oligogalacturonides from the plant cell wall. The results suggest that oligogalacturonides act as signals of tissue damage and, as such, can enhance the response of plant tissues to other elicitor-active molecules during the initiation of phytoalexin accumulation.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Albersheim P, Valent B: Host-pathogen interactions in plants. Plants, when exposed to oligosaccharides of fungal origin, defend themselves by accumulating antibiotics. J Cell Biol 78: 627–643, 1978.

    Google Scholar 

  2. Bailey JA: Mechanisms of phytoalexin accumulation. In: Bailey JA, Mansfield JW (eds) Phytoalexins John Wiley and Sons, New York, 1982, pp 289–318.

    Google Scholar 

  3. Bell AA: Biochemical mechanisms of disease resistance. Ann Rev Plant Physiol 32:21–81, 1981.

    Google Scholar 

  4. Bishop PD, Pearce G, Bryant JE, Ryan CA: Isolation and characterization of the proteinase inhibitor-inducing factor from tomato leaves. Identity and activity of poly- and oligogalacturonide fragments. J Biol Chem 259:13172–13177, 1984.

    Google Scholar 

  5. Blumenkrantz N, Asboe-Hansen G: New method for quantitative determination of uronic acids. Anal Biochem 54:484–489, 1973.

    Google Scholar 

  6. Bruce RJ, West CA: Elicitation of casbene synthetase activity in castor bean. The role of pectic fragments of the plant cell wall in elicitation by a fungal endopolygalacturonase. Plant Physiol 69:1181–1188, 1982.

    Google Scholar 

  7. Chappell J, Hahlbrock K: Transcription of plant defence genes in response to UV light or fungal elicitor. Nature 311:76–78, 1984.

    Google Scholar 

  8. Clarke EGC, Humphreys DJ: Toxic factors in pea haulm silage effluent: the factor affecting germination and growth in plants. J Sci Fd Agric 21:225–227, 1970.

    Google Scholar 

  9. Cramer CL, Ryder TB, Bell JN, Lamb CJ: Rapid switching of plant gene expression induced by fungal elicitor. Science 227:1240–1243, 1985.

    Google Scholar 

  10. Cruikshank IAM: A review of the role of phytoalexins in disease resistance mechanisms. Pontif Acad Sci Scr Varia 41:509–569, 1977.

    Google Scholar 

  11. Darvill AG, Albersheim P: Phytoalexins and their elicitors — a defense against microbial infection in plants. Ann Rev Plant Pathol 35:243–275, 1984.

    Google Scholar 

  12. Davis KR, Lyon GD, Darvill AG, Albersheim P: Hostpathogen interactions XXV. Endopolygalacturonic acid lyase from Erwinia carotovora elicits phytoalexin accumulation by releasing plant cell wall fragments. Plant Physiol 74:52–60, 1984.

    Google Scholar 

  13. Davis KR, Darvill AG, Albersheim P, Dell A: Host-pathogen interactions XXIX. Oligogalacturonides released from sodium polypectate by endopolygalacturonic acid lyase are elicitors of phytoalexins in soybean. Plant Physiol, in press.

  14. Davis KR, Darvill AG, Albersheim P, Dell A: Host-pathogen interactions XXX. Characterization of elicitors of phytoalexin accumulation in soybean released from soybean cell walls by endopolygalacturonic acid lyase. Z Naturforsch, in press.

  15. Dische Z: Color reaction of carbohydrates. In: Whistler RL, Wolfrom ML (eds) Methods in Carbohydrate Chemistry, Vol I. Academic Press, New York, 1962, pp 478–481.

    Google Scholar 

  16. Dixon RA, Dey PM, Lamb CJ: Phytoalexins: enzymology and molecular biology. In: Meister A (ed) Advances in Enzymology, Vol 55, John Wiley and Sons, New York, 1983, pp 1–136.

    Google Scholar 

  17. Ebel J: Induction of phytoalexin synthesis in plants following microbial infection or treatment with elicitors. ACS Symp S 257:257–271, 1984.

    Google Scholar 

  18. Ebel J, Schmidt WE, Loyal R: Phytoalexin synthesis in soybean cells: elicitor induction of phenylalanine ammonia-lyase and chalcone synthase mRNAs and correlation with phytoalexin accumulation. Arch Biochem Biophys 232:240–248, 1984.

    Google Scholar 

  19. Gollin DJ, Darvill AG, Albersheim P: Plant cell wall fragments inhibit flowering and promote vegetative growth in Lemna gibba G3. Biol Cell 51:275–280, 1984.

    Google Scholar 

  20. Hahn MG, Darvill AG, Albersheim P: Host-pathogen interactions XIX. The endogenous elicitor, a fragment of a plant cell wall polysaccharide that elicits phytoalexin accumulation in soybeans. Plant Physiol 68:1161–1169, 1981.

    Google Scholar 

  21. Hahn MG, Bonhoff A, Grisebach H: Quantitative localization of the phytoalexin glyceollin I in relation to fungal hyphae in soybean roots infected with Phytophthora megasperma f.sp. glycinea. Plant Physiol 77:591–601, 1985.

    Google Scholar 

  22. Hargreaves JA: Investigations into the mechanism of mercuric chloride stimulated phytoalexin accumulation in Phaseolus vulgaris and Pisum sativum. Physiol Plant Pathol 15:279–287, 1979.

    Google Scholar 

  23. Hargreaves JA: Accumulation of phytoalexins in cotyledons of French bean (Phaseolus vulgaris L.) following treatment with triton (T-octylphenol polyethoxyethanol) surfactants. New Phytol 87:733–741, 1981.

    Google Scholar 

  24. Jin DF, West CA: Characteristics of galacturonic acid oligomers as elicitors of casbene synthetase activity in castor bean seedlings. Plant Physiol 74:989–992, 1984.

    Google Scholar 

  25. Kuhn DN, Chappell J, Boudet A, Hahlbrock K: Induction of phenylalanine ammonia-lyase and 4-coumarate:CoA ligase mRNAs in cultured plant cells by UV light or fungal elicitor. Proc Natl Acad Sci USA 81:1102–1106, 1984.

    Google Scholar 

  26. Lee S-C, West CA: Polygalacturonase from Rhizopus stolonifer, an elicitor of casbene synthetase activity in castor bean (Ricinus communis L.) seedlings. Plant Physiol 67:633–639, 1981.

    Google Scholar 

  27. Lynch JM: Phytotoxicity of acetic acid produced in the anaerobic decomposition of wheat straw. J Appl Bacteriol 42:81–87, 1977.

    Google Scholar 

  28. Lyon GD, Albersheim P: Host-pathogen interactions XXI. Extraction of a heat-labile elicitor of phytoalexin accumulation from frozen soybean stems. Plant Physiol 70:406–409, 1982.

    Google Scholar 

  29. Mansfield JW: The role of phytoalexins in disease resistance. In: Bailey JA, Mansfield JW (eds) Phytoalexins. John Wiley and Sons, New York, 1982, pp 253–288.

    Google Scholar 

  30. Moesta P, Grisebach H: Investigation of the mechanism of phytoalexin accumulation in soybean induced by glucan or mercuric chloride. Arch Biochem Biophys 211:39–43, 1981.

    Google Scholar 

  31. Nothnagel EA, McNeil M, Albersheim P, Dell A: Hostpathogen interactions XXII. A galacturonic acid oligosaccharide from plant cell walls elicits phytoalexins. Plant Physiol 71:916–926, 1983.

    Google Scholar 

  32. Ossowski P, Pilotti A, Garegg P, Lindberg B: Synthesis of a branched hepta- and octasaccharide with phytoalexin-elicitor activity. Angew Chem Int Ed Engl 22: 793–795, 1983.

    Google Scholar 

  33. Reynolds T: pH restraints on lettuce fruit germination. Ann Bot 39:797–805, 1975.

    Google Scholar 

  34. Robertsen B: Assay for elicitors of lignification in cucumber hypocotyls and purification of elicitors obtained from cucumber cell walls and polygalaturonic acid. Presented at the Sixthe John Innes Symposium: September 17–19, 1984.

  35. Ryder TB, Cramer CL, Bell JN, Robbins MP, Dixon RA, Lamb CJ: Elicitor rapidly induces chalcone synthase mRNA in Phaseolus vulgaris cells at the onset of the phytoalexin defense response. Proc Natl Acad Sci USA 81:5724–5728, 1984.

    Google Scholar 

  36. Sharp JK, Valent B, Albersheim P: Purification and partial characterization of a β-glucan fragment that elicits phytoalexin accumulation in soybean. J Biol Chem 259:11312–11320, 1984.

    Google Scholar 

  37. Sharp JK, McNeil M, Albersheim P: The primary structures of one elicitor-active and seven elicitor-inactive hexa(β-D-glucopyranosyl)-D-glucitols isolated from the mycelial walls of Phytophthora megasperma f.sp. glycinea. J Biol Chem 259:11321–11336, 1984.

    Google Scholar 

  38. Sharp JK, Albersheim P, Ossowski P, Pilotti A, Garegg P, Lindberg B: Comparison of the structures and elicitor activities of a synthetic and a mycelial-wall-derived hexa(β-D-glucopyranosyl)-D-glucitol. J Biol Chem 259:11341–11345, 1984.

    Google Scholar 

  39. Smith DA: Toxicity of phytoalexins. In: Bailey JA, Mansfield JW (eds) Phytoalexins. John Wiley and Sons, New York, 1982, pp 218–252.

    Google Scholar 

  40. Tran Thanh Van K, Toubart P, Cousson A, Darvill AG, Gollin DJ, Chelf P, Albersheim P: Manipulation of the morphogenetic pathways of tobacco explants by oligosaccharins. Nature 314:615–617, 1985.

    Google Scholar 

  41. West CA: Fungal elicitors of the phytoalexin response in higher plants. Naturwissenschaften 68:447–457, 1981.

    Google Scholar 

  42. Yamazaki N, Fry SC, Darvill AG, Albersheim P: Hostpathogen interactions XXIV. Fragments isolated from suspension-cultured sycamore cell walls inhibit the ability of the cells to incorporate [14C]leucine into proteins. Plant Physiol 72:864–869, 1983.

    Google Scholar 

  43. York WS, Darvill AG, Albersheim P: Inhibition of 2,4-dichlorophenoxy-acetic acid-stimulated elongation of pea stem segments by a xyloglucan oligosaccharide. Plant Physiol 75:295–297, 1984.

    Google Scholar 

  44. Yoshikawa M, Keen NT, Wang M-C: A receptor on soybean membranes for a fungal elicitor of phytoalexin accumulation. Plant Physiol 73:497–506, 1983.

    Google Scholar 

Download references

Author information

Author notes

  1. Keith R. Davis, Alan G. Darvill & Peter Albersheim

    Present address: Complex Carbohydrate Research Center, University of Georgia, P.O. Box 5677, 30613, Athens, GA, U.S.A.

Authors and Affiliations

  1. Department of Molecular, Cellular and Developmental Biology, University of Colorado, Campus, Box 215, 80309, Boulder, CO, U.S.A.

    Keith R. Davis, Alan G. Darvill & Peter Albersheim

  2. Department of Chemistry, University of Colorado, Campus, Box 215, 80309, Boulder, CO, U.S.A.

    Keith R. Davis, Alan G. Darvill & Peter Albersheim

Authors
  1. Keith R. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alan G. Darvill
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter Albersheim
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by the United States Department of Energy DE-ACO2-84ER13161. This paper is number XXXI in a series, ‘Host-Pathogen Interactions’. The preceding paper, Host-Pathogen Interactions XXX is ‘Characterization of elicitors of phytoalexin accumulation in soybean released from soybean cells by endopolygalacturonic acid lyase’, by K. R. Davis, A. G. Darvill, P. Albersheim, and A. Dell. Zeitschrift für Naturforsschung, in press.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Davis, K.R., Darvill, A.G. & Albersheim, P. Several biotic and abiotic elicitors act synergistically in the induction of phytoalexin accumulation in soybean. Plant Mol Biol 6, 23–32 (1986). https://doi.org/10.1007/BF00021303

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00021303

Keywords

Search

Navigation