Journal of Chemical Ecology

, Volume 28, Issue 12, pp 2449–2463 | Cite as

Comparative Physiological Responses in Chinese Cabbage Induced by Herbivory and Fungal Infection

  • Michael Rostás
  • Richard Bennett
  • Monika Hilker


Fungal infection of Chinese cabbage leaves by Alternaria brassicae has earlier been shown to have detrimental effects on larval development of the chrysomelid beetle Phaedon cochleariae. Furthermore, adults of this leaf beetle avoid fungus-infected Chinese cabbage leaves for oviposition and feeding. However, herbivory had no impact on fungal growth. In this study, we investigated physiological responses of the host plant to herbivore attack and fungal infection in order to elucidate the mechanisms of the described ecological interactions between the fungus and the herbivore. Changes in primary factors (water, C/N ratio, protein, sucrose) and defense-related plant compounds (glucosinolates, anthocyanins, peroxidase) were measured. Herbivory and fungal infection reduced the sucrose concentration of leaves and increased amounts of indole glucosinolates as well as total anthocyanins. In addition, water content was slightly lower in insect-damaged but not in infected leaves. Higher levels of peroxidase activity resulted exclusively from fungal infection. The C/N ratio and total protein content remained unaffected by either treatment. The implications of the induced plant changes on the herbivore are discussed.

Tripartite interactions phytopathogenic fungus infection herbivory induced resistance cross-effects nutrients glucosinolates anthocyanins peroxidase Chinese cabbage Phaedon cochleariae Alternaria brassicae 


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  1. Ayres, P. G. 1992. Pests and Pathogens—Plant Responses to Foliar Attack. Bios Scientific Publishers, Oxford.Google Scholar
  2. Bains, P. S. and Tewari, J. P. 1987. Purification, chemical characterization and host-specifity of the toxin produced by Alternaria brassicae. Physiol. Mol. Plant Pathol. 30:259–271.CrossRefGoogle Scholar
  3. Baur, R., StÄdler, E., Monde, K., and Tagasuki, M. 1998. Phytoalexins from Brassica (Cruciferae) as oviposition stimulants for the cabbage root fly, Delia radicum. Chemoecology 8:163–168.CrossRefGoogle Scholar
  4. Baldwin, I. T. and Preston, C. A. 1999. The eco-physiological complexity of plant responses to insect herbivores. Planta 208:137–145.CrossRefGoogle Scholar
  5. Bates, N. J. and Rothstein, S. J. 1998. C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J. 16:561–569.CrossRefGoogle Scholar
  6. Bi, J. L., Murphy, J. B., and Felton, G. W. 1997. Antinutritive and oxidative components as mechanisms of induced resistance in cotton to Helicoverpa zea. J. Chem. Ecol. 23:97–117.CrossRefGoogle Scholar
  7. Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.CrossRefGoogle Scholar
  8. Clancy, K.M. 1992. The role of sugars in western spruce budworm nutritional ecology. Ecol. Entomol. 17:189–197.CrossRefGoogle Scholar
  9. Constabel, C. P. 1999. A survey of herbivore-inducible defensive proteins and phytochemicals, pp. 137–166, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.). Induced Plant Defenses against Pathogens and Herbivores: Biochemistry, Ecology, and Agriculture. APS Press, St. Paul.Google Scholar
  10. Dadd, R. H. 1985. Nutrition: organisms, pp. 313–390, in G. A. Kerkut and L. I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 4, Regulation: Digestion, Nutrition, Excretion. Pergamon, Oxford.Google Scholar
  11. Doughty, K. J., Porter, A. J. R., Morton, A. M., Kiddle, G., Bock, C. H., and Wallsgrove, R. 1991. Variation in the glucosinolate content of oilseed rape (Brassica napus L.) leaves. II. Response to infection by Alternaria brassicae (Berk.) Sacc. Ann. Appl. Biol. 118:469–477.CrossRefGoogle Scholar
  12. Dowd, P. F. and Lagrimini, L.M. 1997. Examination of different tobacco (Nicotiana spp.) types underand overproducing tobacco anionic peroxidase for their leaf resistance against Helicoverpa zea. J. Chem. Ecol. 23:2357–2370.CrossRefGoogle Scholar
  13. Duniway, J. M. and Durbin, R. D. 1971. Some effects of Uromyces phaseoli on the transpiration rate and stomatal response of bean leaves. Phytopathology 61:409–411.CrossRefGoogle Scholar
  14. Fahey, J. W., Zalcman, A. T., and Talalay, P. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51CrossRefGoogle Scholar
  15. Franceschi, V. R. and Grimes, H. D. 1991. Induction of soybean vegetative storage proteins and anthocyanins by low-level atmospheric methyl jasmonate. Proc. Nal. Acad. Sci. USA 88:6745–6749.CrossRefGoogle Scholar
  16. GÖtz, M. 1996. Zur vegetativen und generativen Entwicklung der obligat biotrophen Parasiten in den Pathosystemen Triticum aestivum/Blumeria graminis und Phaseolus vulgaris/Uromyces appendiculatus. Ph.D. thesis. Technische Universität Braunschweig, Germany.Google Scholar
  17. Gupta, S. K., Gupta, P. P., Yadava, T. P., and Kaushik, C. D. 1990. Metabolic changes in mustard due to alternaria leaf blight. Indian Phytopathol. 43:64–69.Google Scholar
  18. GrÖntoft, M. and O'Connor, D. 1990. Greenhouse method for testing of resistance of young Brassica plants to Alternaria brassicae. Plant Breed. 105:160–164.CrossRefGoogle Scholar
  19. Hammerschmidt, R. 1999. Induced disease resistance: howdo induced plants stop pathogens? Physiol. Mol. Plant Pathol. 55:77–85.CrossRefGoogle Scholar
  20. Harborne, J. B. and Williams, C. A. 1995. Anthocyanins and other flavonoids. Nat. Prod. Rep. 12:639–657.CrossRefGoogle Scholar
  21. Harborne, J. B. and Williams, C. A. 2000. Advances in flavonoid research since 1992. Phytochemistry 55:481–504.CrossRefGoogle Scholar
  22. Hatcher, P. E. 1995. Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biol. Rev. 70:639–694.CrossRefGoogle Scholar
  23. Hatcher, P. E. and Ayres, P. G. 1997. Indirect interactions between insect herbivores and pathogenic fungi on leaves, pp. 133–149, in A. C. Gange and V. K. Brown (eds.). Multitrophic Interactions in Terrestrial Systems. Blackwell Science, Oxford.Google Scholar
  24. Hatcher, P. E., Paul, N. D., Ayres, P. G., and Whittaker, J. B. 1994. The effect of a foliar disease (rust) on the development of Gastrophysa viridula (Coleoptera:Chrysomelidae). Ecol. Entomol. 19:349–360.CrossRefGoogle Scholar
  25. Hatcher, P. E., Ayres, P. G., and Paul, N. D. 1995. The effect of natural and simulated insect herbivory, and leaf age, on the process of infection of Rumex crispus L. and R. obtusifolius L. by Uromyces rumicis (Schum.) Wint. New Phytol. 130:239–249.CrossRefGoogle Scholar
  26. Hedin, P. A., Jenkins, J. N., Collum, D. H., White, W. H., Parrott, W. L., and Macgown, M. W. 1983. Cyanidin-3-β-glucoside, a newly recognized basis for resistance in cotton to the tobacco budworm Heliothis virescens (Fab.) (Lepidoptera: Noctuidae). Experientia 39:799–801.CrossRefGoogle Scholar
  27. Hopkins, R. J., Griffiths, D. W., Birch, A. N. E., and MCkinley, R. G. 1998. Influence of increasing herbivore pressure on modification of glucosinolate content of swedes (Brassica napus spp.rapifera). J. Chem. Ecol. 24:2003–2019.CrossRefGoogle Scholar
  28. Jones, C. G., Hare, J. D., and Compton, S. J. 1989. Measuring plant protein with the Bradford assay. J. Chem. Ecol. 15:979–992.CrossRefGoogle Scholar
  29. Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, Illinois.CrossRefGoogle Scholar
  30. Karban, R. and Kuc, J. 1999. Induced resistance against pathogens and herbivores: an overview, pp. 1–15, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.). Induced Plant Defenses against Pathogens and Herbivores. APS Press, St. Paul, Minnesota.Google Scholar
  31. Kiddle, G. A., Bennett, R. N., Botting, N. P., Davidson, N. E., Robertson, A. A. B., and Wallsgrove, R. M. 2001. High performance liquid-chromatography separation of natural and synthetic desulfoglucosinolates and their chemical validation by spectroscopic, NMR, and CI-MS methods. Phytochem. Methods 12:226–242.CrossRefGoogle Scholar
  32. Kingsley, P., Scriber, J. M., Grau, C. R., and Delwiche, P. A. 1983. Feeding and growth performance of Spodoptera eridania (Noctuidae: Lepidoptera) on “vernal” alfalfa as influenced by Verticillium wilt. Prot. Ecol. 5:127–134.Google Scholar
  33. Koritsas, V. M., Lewis, J. A., and Fenwick, G. R. 1991. Glucosinolate response of oilseed rape, mustard and kale to mechanical wounding and infestation by cabbage stem flea beetle (Psylliodes chrysocephala). Ann. Appl. Biol. 118:209–221.CrossRefGoogle Scholar
  34. KÖhle, H. 1989. FrUntersuchungen zur Physiologie des Alternaria-Befalls von Raps. Z. Pflanzenkrankh. Pflanzensch. 96:225–238.Google Scholar
  35. Lim, C. O., Lee, S. I., Chung, W. S., Park, S. H., Hwang, I., and Cho, M. J. 1996. Characterization of a cDNA encoding cystein proteinase inhibitor from Chinese cabbage (Brassica campestris L. ssp. pekinensis) flower buds. Plant Mol. Biol. 30:373–379.CrossRefGoogle Scholar
  36. Lo, S. C. and Nicholson, R. L. 1998. Reduction of light-induced anthocyanin accumulation in inoculated sorghum mesocotyls. Plant Physiol. 116:979–989.CrossRefGoogle Scholar
  37. Louda, S. and Mole, S. 1991. Glucosinolates: chemistry and ecology, pp. 123–164, in G. A. Rosenthal and M. R. Beerenbaum (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, San Diego, California.CrossRefGoogle Scholar
  38. Ludwig-Müller, J., Schubert, B., Pieper, K., Ihmig, S., and Hilgenberg, W. 1997. Glucosinolate content in susceptible and resistant Chinese cabbage varieties during development of clubroot disease. Phytochemistry 44:407–414.CrossRefGoogle Scholar
  39. Manicelli, A. L. 1984. Photoregulation of anthocyanin synthesis. Plant Physiol. 75:447–453.CrossRefGoogle Scholar
  40. Matsuda, K. 1988. Feeding stimulants of leaf beetles, pp. 41–56, in P. Jolivet, E. Petitpierre, T. H. Hsiao (eds.). Biology of Chrysomelidae. Kluwer Academic Publishers, Dordrecht, The Netherlands.CrossRefGoogle Scholar
  41. MÜller, C. 1999. Chemische Ökologie des Phytophagenkomplexes an Tanacetum vulgare L. (Asteraceae). PhD thesis. Freie Universität, Berlin.Google Scholar
  42. Nielsen, J. K. 1978. Host plant discrimination within Cruciferae: feeding responses of four leaf beetles (Coleoptera: Chrysomelidae) to glucosinolates, cucurbitacins and cardenolides. Entomol. Exp. Appl. 24:41–54. CABBAGE RESPONSES TO HERBIVORY AND INFECTION 2463CrossRefGoogle Scholar
  43. Østergaard, L., Teilum, K., Mirza, O., Mattsson, O., Petersen, M., Welinder, K. G., Mundy, J., Gajhede, M., and Henriksen, A. 2000. Arabidopsis ATP A2 peroxidase. Expression and high resolution structure of a plant peroxidase with implications for lignification. Plant Mol. Biol. 44:231–243.CrossRefGoogle Scholar
  44. Paul, N. D., Hatcher, P. E., and Taylor, J. E. 2000. Coping with multiple enemies: an integration of molecular and ecological perspectives. Trends Plant Sci. 5:220–225.CrossRefGoogle Scholar
  45. RostÁs, M. and Hilker, M. 2002a. Asymmetric plant-mediated cross-effects between a herbivorous insect and a phytopathogenic fungus. Agric. For. Entomol. In press.CrossRefGoogle Scholar
  46. RostÁs, M. and Hilker, M. 2002b. Feeding damage by larvae of the mustard leaf beetle deters conspecific females from oviposition and feeding. Entomol. Exp. Appl. In press.CrossRefGoogle Scholar
  47. Schoonhoven, L. M., Jermy, T., and Van Loon, J. J. A. 1998. Insect-Plant Biology. Chapman & Hall, London, United Kingdom.CrossRefGoogle Scholar
  48. Siemens, D. H. and Mitchell olds, T. 1996. Glucosinolates and herbivory by specialists (Coleoptera: Chrysomelidae, Lepidoptera: Plutellidae): Consequences of concentration and induced resistance. Environ. Entom. 25:1344–1353.CrossRefGoogle Scholar
  49. Slansky, F. and Scriber, J. M. 1985. Food consumption and utilization, pp. 88–163, in G. A. Kerkut and L. I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology,Vol. 4, Regulation: Digestion, Nutrition, Excretion. Pergamon, Oxford.Google Scholar
  50. Stout, M. J. and Bostock, R.M. 1999. Specificity of induced responses to arthropods and pathogens, pp. 183–209, in A. A. Agrawal, S. Tuzun, E. Bent (eds.). Induced Plant Defenses Against Pathogens and Herbivores. APS Press, St. Paul, Minnesota.Google Scholar
  51. Stout, M. J., Workman, K. V., Bostock, R. M., and Duffey, S. S. 1998. Stimulation and attenuation of induced resistance by elicitors and inhibitors of chemical induction in tomato (Lycopersicon esculentum) foliage. Entomol. Exp. Appl. 86:267–279.CrossRefGoogle Scholar
  52. Stout, M. J, Fidantsef, A. L., Duffey, S. S., and Bostock, R. M. 1999. Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum. Physiol. Mol. Plant Pathol. 54:115–130.CrossRefGoogle Scholar
  53. Valentine, H. T., Wallner, E., and Wargo, P. M. 1983. Nutritional changes in host foliage during and after defoliation, and their relation to the weight of gypsy moth pupae. Oecologia 57:298–302.CrossRefGoogle Scholar
  54. Wallsgrove, R. M., Doughty, K., and Bennett, R. N. 1999. Glucosinolates, pp. 523–562, in B. K. Singh (ed.). Plant Amino Acids: Biochemistry and Biotechnology. Marcel Dekker, New York.Google Scholar

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • Michael Rostás
    • 1
  • Richard Bennett
    • 2
  • Monika Hilker
    • 1
  1. 1.Institut für Biologie, Angewandte Zoologie/Ökologie der TiereFreie Universität BerlinBerlinGermany
  2. 2.Institute of Food ResearchColney, NorwichUnited Kingdom

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