Advertisement

Journal of Chemical Ecology

, Volume 31, Issue 7, pp 1445–1473 | Cite as

Plant Cyanogenesis of Phaseolus lunatus and its Relevance for Herbivore–Plant Interaction: The Importance of Quantitative Data

  • Daniel J. BallhornEmail author
  • Reinhard Lieberei
  • Jörg U. Ganzhorn
Article

Abstract

Quantitative experimental results on the antiherbivorous effect of cyanogenesis are rare. In our analyses, we distinguished between the total amount of cyanide-containing compounds stored in a given tissue [cyanogenic potential (HCNp)] and the capacity for release of HCN per unit time (HCNc) from these cyanogenic precursors as a reaction to herbivory. We analyzed the impact of these cyanogenic features on herbivorous insects using different accessions of lima beans (Phaseolus lunatus L.) with different cyanogenic characteristics in their leaves and fourth instars of the generalist herbivore Schistocerca gregaria Forskål (Orthoptera, Acrididae). Young leaves exhibit a higher HCNp and HCNc than mature leaves. This ontogenetic variability of cyanogenesis was valid for all accessions studied. In no-choice bioassays, feeding of S. gregaria was reduced on high cyanogenic lima beans compared with low cyanogenic beans. A HCNp of about 15 μmol cyanide/g leaf (fresh weight) with a corresponding HCNc of about 1 μmol HCN released from leaf material within the first 10 min after complete tissue disintegration appears to be a threshold at which the first repellent effects on S. gregaria were observed. The repellent effect of cyanogenesis increased above these thresholds of HCNp and HCNc. No repellent action of cyanogenesis was observed on plants with lower HCNp and HCNc. These low cyanogenic accessions of P. lunatus were consumed extensively—with dramatic consequences for the herbivore. After consumption, locusts showed severe symptoms of intoxication. Choice assays confirmed the feeding preference of locusts for low over high cyanogenic leaf material of P. lunatus. The bioassays revealed total losses of HCN between 90 and 99% related to the estimated amount of ingested cyanide-containing compounds by the locusts. This general finding was independent of the cyanogenic status (high or low) of the leaf material.

Key Words

Cyanogenesis chemical defense Phaseolus lunatus Schistocerca gregaria herbivory cyanogenic potential cyanogenic capacity plant–herbivore interactions 

Notes

Acknowledgments

We thank Prof. Dr. David S. Seigler for fruitful discussions. We also thank the “Institut für Pflanzengenetik und Kulturpflanzenforschung” in Gatersleben for providing the seed material of our experimental plants.

References

  1. Abbott, R. J. 1977A quantitative association between soil moisture content and the frequency of the cyanogenic form of Lotus corniculatus L. at Birsay, OrkneyHeredity38397400Google Scholar
  2. Baudoin, J. P., Barthelemy, Y. J., Ndungo, V. 1991Variability of cyanide contents in the primary and secondary genepools of the lima bean, Phaseolus lunatus L. FAO/IBPGRPlant Genet. Resour. Newsl.8559Google Scholar
  3. Bernays, E. A. 1991Relationship between deterrence and toxicity of plant secondary compounds for the grasshopper Schistocerca americanaJ. Chem. Ecol.1725192526Google Scholar
  4. Bernays, E. A., Chapman, E. M., Leather, E. M., McCaffery, A. R. 1977The relationship of Zonocerus variegatus (L.) (Acridoidea: Prygomorphidae) with cassava (Manihot esculenta)Bull. Entomol. Res.67391404Google Scholar
  5. Blaise, S., Cartier, D., Reynaud, D. 1991Evolution and differentiation of Lotus corniculatus/Lotus alpinus populations from French south-western Alps. I. Morphologic and cyanogenic variationsEvol. Trends Plants5137148Google Scholar
  6. Bokanga, M., Ekanayake, I. J., and Dixon, A. G. O. 1994. Genotype–environment interactions for cyanogenic potential in cassava, pp. 131–140, in M. Bokanga, A. J. A. Essers, N. Poulter, H. Rosling and O. Tewe (eds.). International Workshop on Cassava Safety. Acta Hortic. 375.Google Scholar
  7. Brattsten, L. B., Samuelian, J. H., Long, K. Y., Kincaid, S. A., Evans, C. K. 1983Cyanide as feeding stimulant for the southern armyworm, Spodoptera eridaniaEcol. Entomol.8125132Google Scholar
  8. Calatayud, P. A., Rü, B. 1996Study of the nutritional relationships between the cassava mealybug and its host plantBull. Soc. Zool. Fr. Evol. Zool.121391398in FrenchGoogle Scholar
  9. Calatayud, P. A., Tertuliano, M., Rü, B. 1994Seasonal variation in secondary compounds in the phloem sap of cassava in relation to plant genotype and infestation by Phenacoccue manihoti (Homoptera: Pseudococcidae)Bull. Entomol. Res.84453459Google Scholar
  10. Caradus, J. R., Forde, M. B. 1996Characterisation of white clover populations collected from the Caucuses and high altitude regions of eastern TurkeyGenet. Resour. Crop Ecol.43143155Google Scholar
  11. Caradus, J. R., Mackay, A. C., Charlton, J. F. L., Chapman, D. F. 1990Genocology of white clover (Trifolium repens L.) from wet and dry hill country pasturesN.Z. J. Agric. Res.33377384Google Scholar
  12. Coley, P. D. 1980Effects of leaf age and plant life history patterns on herbivoryNature284545546Google Scholar
  13. Coley, P. D. 1988Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defenseOecologia74531536Google Scholar
  14. Coley, P. D., Bryant, J. P., Chapin, F. S.,III 1985Resource availability and plant anti-herbivore defenseScience230895899Google Scholar
  15. Conn, E. E. 1980Cyanogenic glycosidesBell, E. A.Charlwood, B. V. eds. Encyclopedia of Plant Physiology. New Series 8SpringerBerlin Heidelberg New York461491Google Scholar
  16. Cooper-Driver, G. A., Swain, T. 1976Cyanogenic polymorphism in bracken in relation to herbivore predationNature260604.PubMedGoogle Scholar
  17. Cooper-Driver, G. A., Finch, S., Swain, T., Bernays, E. 1977Seasonal variation in secondary plant compounds in relation to the palatability of Pteridium aquilinumBiochem. Syst. Ecol.5177183Google Scholar
  18. Crush, J. R., Caradus, J. R. 1995Cyanogenesis potential and iodine concentration in white clover (Trifolium repens L.) cultivarsN.Z. J. Agric. Res.38309316Google Scholar
  19. Debouck, D. 1991Systematics and morphologySchoonhoven, A.Voysest, O. eds. Common Beans: Research for Crop ImprovementCommonwealth Agricultural Bureaux InternationalWallingford, UK55118Google Scholar
  20. Ellis, W. M., Keymer, R. J., Jones, D. A. 1977aThe effect of temperature on the polymorphism of cyanogenesis in Lotus corniculatus LHeredity38339347Google Scholar
  21. Engler, H. S., Spencer, K. C., Gilbert, L. E. 2000Insect metabolism: Preventing cyanide release from leavesNature406144145PubMedGoogle Scholar
  22. Feeny, P. 1976Plant apparency and chemical defenseRecent Adv. Phytochem.10140Google Scholar
  23. Fischer, D., Kogan, M., Paxton, J. 1990Effect of glyceollin, a soybean phytoalexin on feeding by three phytophagous beetles (Coleoptera: Coccinellidae and Chrysomelidae): Dose versus responseEnviron. Entomol.1912781282Google Scholar
  24. Frehner, M., Conn, E. E. 1987The linamarin β-glucosidase in Costa Rica wild bean (Phaseolus lunatus L.) is apoplasticPlant Physiol.8412961300Google Scholar
  25. Gleadow, R. M., Woodrow, I. E. 2000aTemporal and spatial variation in cyanogenic glycosides in Eucalyptus cladocalyxTree Physiol.20591598Google Scholar
  26. Gleadow, R. M., Woodrow, I. E. 2000bPolymorphism in cyanogenic glycoside content and cyanogenic β-glucosidase activity in natural populations of Eucalyptus cladocalyxAust. J. Plant Physiol.27693699Google Scholar
  27. Gleadow, R. M., Woodrow, I. E. 2002Constraints on effectiveness of cyanogenic glycosides in herbivore defenseJ. Chem. Ecol.2813011313PubMedGoogle Scholar
  28. Hayden, K. J., Parker, I. M. 2002Plasticity in cyanogenesis of Trifolium repens L.: inducibility, fitness costs and variable expressionEvol. Ecol. Res.4155168Google Scholar
  29. Heil, M. 2004Direct defense or ecological costs: Responses of herbivorous beetles to volatiles released by wild lima bean (Phaseolus lunatus)J. Chem. Ecol.3012891295PubMedGoogle Scholar
  30. Hösel, W., Conn, E. E. 1982The aglycone specificity of plant β-glucosidasesTrends Biochem. Sci.7219221Google Scholar
  31. Hruska, A. J. 1988Cyanogenic glucosides as defence compoundsJ. Chem. Ecol.1422132217Google Scholar
  32. Hughes, M. A. 1991The cyanogenic polymorphism in Trifolium repens L. (white clover)Heredity66105115Google Scholar
  33. Jones, D. A. 1962Selective eating of the acyanogenic form of the plant Lotus corniculatus by various animalsNature19311091110Google Scholar
  34. Jones, D. A. 1966On the polymorphism of cyanogenesis in Lotus corniculatus. I. Selection by animalsCan. J. Genet. Cytol.8556567Google Scholar
  35. Jones, D. A. 1972Cyanogenic glycosides and their functionHarborne, J. B. eds. Phytochemical EcologyAcademic PressLondon103124Google Scholar
  36. Jones, D. A. 1988Cyanogenesis in animal–plant interactionsEvered, D.Harnett, S. eds. Cyanide Compounds in BiologyJohn Wiley & SonsChichester, UK151170Google Scholar
  37. Jones, D. A. 1998Why are so many food plants cyanogenic?Phytochemistry47155162PubMedGoogle Scholar
  38. Kakes, P. 1989An analysis of the costs and benefits of the cyanogenic system in Trifolium repensTheor. Appl. Genet.77111118Google Scholar
  39. Lieberei, R. 1988Relationship of cyanogenic capacity (HCN-c) of the rubber tree Hevea brasiliensis to susceptibility to Microcyclus ulei, the agent causing South American leaf blightJ. Phytopathol.1225467Google Scholar
  40. Lieberei, R., Schrader, A., Biehl, B., Chee, K. H. 1983Effect of cyanide on Microcyclus ulei culturesJ. Rubber Res. Inst. Malays.31227235Google Scholar
  41. Lieberei, R., Nahrstedt, A., Selmar, D., Gasparotto, L. 1986The occurrence of Lotaustralin in the genus Hevea and changes of HCN-potential in developing organs of Hevea brasiliensisPhytochemistry2515731578Google Scholar
  42. Lieberei, R., Biehl, B., Giesemann, A., Junqueira, N. T. V. 1989Cyanogenesis inhibits active defence reactions in plantsPlant Physiol.903336Google Scholar
  43. Lieberei, R., Fock, H. P., Biehl, B. 1996Cyanogenesis inhibits active defence in plants: Inhibition by gaseous HCN of photosynthetic CO2 fixation and respiration in intact leavesAngew. Bot.70230238Google Scholar
  44. Liu, S., Norris, D., Hartwig, E., Xu, M. 1992Inducible phytoalexins in juvenile soybean genotypes predict soybean looper resistance in the fully developed plantsPlant Physiol.10014791485Google Scholar
  45. Loyd, R. and Gray, E. 1970. Amount and distribution of hydrocyanic acid potential during the life cycle of plants of three Sorghum cultivars. Agron. J. 394–397.Google Scholar
  46. Mainguet, A. M., Louveaux, A., Sayed, G., Rollin, P. 2000Ability of a generalist insect, Schistocerca gregaria, to overcome thioglucoside defense in desert plants: tolerance oradaption?Entomol. Exp. Appl.94309317Google Scholar
  47. McMahon, J. M., White, W. L. B., Sayre, R. T. 1995Cyanogenesis in cassava (Manihot esculenta Crantz)J. Exp. Bot.46731741Google Scholar
  48. Møller, B. L., Seigler, D. S. 1999Biosynthesis of cyanogenic glucosides, cyanolipids and related compoundsSingh, B. K. eds. Plant Amino AcidsM. DekkerNew York563609Google Scholar
  49. Mowat, D. J., Clawson, S. 1996Oviposition and hatching of the clover weevil Sitona lepidus Gyll (Coleoptera, Curculionidae)Grass Forage Sci.51418423Google Scholar
  50. Nahrstedt, A. 1985Cyanogenesis and the role of cyanogenic compounds in insectsPlant Syst. Evol.1503547Google Scholar
  51. Nahrstedt, A. 1988Cyanogenic compounds as protecting agents for organismsEvered, D.Harnett, S. eds. Cyanide Compounds in BiologyJohn Wiley & SonsChichester, UK131150Google Scholar
  52. Patton, C. A., Ranney, T. G., Burton, J. D., Wallenbach, J. F. 1997Natural pest resistance of Prunus taxa to feeding by adult Japanese beetles—role of endogenous allelochemicals in host plant resistanceJ. Am. Soc. Hortic. Sci.122668672Google Scholar
  53. Poulton, J. E. 1983Cyanogenic compounds in plants and their toxic effectsKeeler, R. F.Tu, T. A. eds. Handbook of Natural Toxins 1Marcel Dekker Inc.New YorkGoogle Scholar
  54. Poulton, J. E. 1988Localisation and catabolism of cyanogenic glycosidesEvered, D.Harnett, S. eds. Cyanide Compounds in Biology. Proceedings of the CIBA Foundation Symposium 140John Wiley & SonsChichester, UK6791Google Scholar
  55. Poulton, J. E. 1990Cyanogenesis in plantsPlant Physiol.94401405Google Scholar
  56. Poulton, J. E., Li, C. P. 1994Tissue level compartmentation of (R)-amygdalin and amygdalin hydrolase prevents large-scale cyanogenesis in undamaged Prunus seedsPlant Physiol.1042935PubMedGoogle Scholar
  57. Provenza, F. D., Pfister, J. A., Cheney, C. D. 1992Mechanisms of learning in diet selection with reference to phytotoxicosis in herbivoresJ. Range Manag.453645Google Scholar
  58. Schappert, P. J., Shore, J. S. 1999aCyanogenesis in Turnera ulmifolia L. (Turneraceae). I. Phenotypic distribution and genetic variation for cyanogenesis on JamaicaHeredity74392404Google Scholar
  59. Schappert, P. J., Shore, J. S. 1999bEffects on cyanogenesis polymorphism in Turnera ulmifolia on Euptoieta hegesia and potential Anolis predatorsJ. Chem. Ecol.2514551479Google Scholar
  60. Schappert, P. J., Shore, J. S. 1999cCyanogenesis, herbivory and plant defense in Turnera ulmifolia on JamaicaEcoscience6511520Google Scholar
  61. Schappert, P. J., Shore, J. S. 2000Cyanogenesis in Turnera ulmifolia L. (Turneraceae). I. Developmental expression, heritability and cost of cyanogenesisEvol. Ecol. Res.2337352Google Scholar
  62. Seigler, D. S. 1998Cyanogenic glycosides and cyanolipidsSeigler, D. S. eds. Plant Secondary MetabolismKluwer Academic PressBoston273296Google Scholar
  63. Selmar, D. 1986. Cyanogenese in Hevea brasiliensis, zwei Wege zur Metabolisierung cyanogener Glycoside. Ph.D. Dissertation. TU Braunschweig, 12–13, 14–15, 63–64, 131–136 (in German).Google Scholar
  64. Shore, J. S., Obrist, C. M. 1992Variation in cyanogenesis within and among populations and species of Turnera series Canaligerae (Turneraceae)Biochem. Syst. Ecol.20915Google Scholar
  65. Solomonson, L. P. 1981Vennesland, B.Conn, E. E.Knowles, C. J.Westby, J.Wissing, F. eds. Cyanide in BiologyAcademic PressLondon1128Google Scholar
  66. Statistica 6.0. 2001. System Reference by StatSoft, Inc.Google Scholar
  67. Swain, E., Li, C. P., Poulton, J. E. 1992Tissue and subcellular localization of enzymes catabolizing (R)-amygdalin in mature Prunus serotina seedsPlant Physiol.100291300Google Scholar
  68. Tattersal, D. B., Bak, S., Jones, P. R., Olsen, C. E., Nielsen, J. K., Hansen, M. L., HØj, P. B., MØller, B. L. 2001Resistance to an herbivore through engineered glucoside synthesisScience29318261828PubMedGoogle Scholar
  69. Till, I. 1987Variability of expression of cyanogenesis in white clover (Trifolium repens L.)Heredity59265271Google Scholar
  70. Thayer, S. S., Conn, E. E. 1981Subcellular localization of dhurrin β-glucosidase and hydroxynitrilase in the mesophyll cells of Sorghum leaf bladesPlant Physiol.67617.Google Scholar
  71. Underwood, N. 1999The influence of plant and herbivore characteristics on the interaction between induced resistance and herbivore population dynamicsAm. Nat.153282294Google Scholar
  72. Underwood, N., Morris, W., Gross, K., Lockwood, J. R. I. 2000Induced resistance to Mexican bean beetles in soybeans: Variation among genotypes and lack of correlation with constitutive resistanceOecologia1228389Google Scholar
  73. Vetter, J. 2000Plant cyanogenic glycosidesToxicon381136PubMedGoogle Scholar
  74. Zagrobelny, M., Bak, S., Rasmussen, A. V., JØrgensen, B., Naumann, C. M., MØller, B. L. 2004Cyanogenic glucosides and plant–insect interactionsPhytochemistry65293306PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Daniel J. Ballhorn
    • 1
    Email author
  • Reinhard Lieberei
    • 1
  • Jörg U. Ganzhorn
    • 2
  1. 1.Biocenter Klein Flottbek and Botanical GardenUniversity of HamburgHamburgGermany
  2. 2.Biocenter Grindel and Zoological Museum, Department of Ecology and ConservationUniversity of HamburgHamburgGermany

Personalised recommendations