Systemic, genotype-specific induction of two herbivore-deterrent iridoid glycosides in Plantago lanceolata L. in response to fungal infection by Diaporthe adunca (ROB.) niessel

Journal of Chemical Ecology

Volumn 28, Issue 12, 2002, Pages 2429-2448

  Marak, Hamida B ^a   Biere, Arjen ^a   Van Damme, Jos M M ^a  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

Author keywords

Constitutive chemical defense; Diaporthe adunca; Genetic variation; Induced chemical defense; Plant herbivore interactions; Plant pathogen interactions; Plantago lanceolata

Indexed keywords

AUCUBIN; CATALPOL; GLYCOSIDE; IRIDOID;

ANTIFEEDANT; ANTIHERBIVORE DEFENSE; FUNGAL DISEASE; HOST-PATHOGEN INTERACTION; INSECT; PLANT-HERBIVORE INTERACTION; SECONDARY METABOLITE;

ADAPTATION; ANIMAL; ARTICLE; ASCOMYCETES; BIOSYNTHESIS; CONTROLLED STUDY; DIAPORTHE ADUNCA; FEEDING BEHAVIOR; FUNGUS; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENOTYPE; HOST RESISTANCE; INSECT; MYCOSIS; NONHUMAN; PATHOGENICITY; PLANT; PLANT DEFENSE; PLANT GROWTH; PLANT HERBIVORE INTERACTION; PLANT LEAF; PLANT PATHOGEN INTERACTION; PLANT REPRODUCTION; PLANT ROOT; PLANT STEM; PLANTAGO; PLANTAGO LANCEOLATA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ASCOMYCOTA; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENOTYPE; GLYCOSIDES; INSECTS; PLANTS, EDIBLE;

ANIMALIA; ARTHROPODA; ASCOMYCOTA; DIAPORTHE; DIAPORTHE ADUNCA; FUNGI; HEXAPODA; INSECTA; LANCEOLATA; MUSA X PARADISIACA; PLANTAGO LANCEOLATA;

EID: 0036963295     PISSN: 00980331     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1021475800765     Document Type: Article

References (66)

1. ADLER, L. S., SCHMITT, J., and BOWERS, M. D. 1995. Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75-85,
2. AGRAWAL, A. A. 2000. Induced plant defense: evolution of induction and adaptive phenotypic plasticity, pp. 251-268, in A. A. Agrawal, S. Tuzun and E. Bent (eds.). Induced Plant Defenses Against Herbivores. Biochemistry, Ecology, and Agriculture. APS Press, St. Paul, Minnesota.
3. BAILEY, J, A. and MANSFIELD, J. W. (eds.). 1982. Phytoalexins. Blackie, Glasgow.
4. BALDWIN, I. T. and KARB, M. J. 1995. Plasticity in the allocation of nicotine to reproductive parts in Nicotiana attenuata. J. Chem. Ecol. 21:897-909.
5. BARBOSA, P. 1991. Plant pathogens and nonvector herbivores, pp. 341-382, in P. Barbosa, V. A. Krischik and C. G. Jones (eds.). Microbial Mediation of Plant-Herbivore Interactions. John Wiley, New York.
6. BOWERS, M. D. 1991. Iridoid glycosides, pp. 297-325, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites, 2nd. ed. Academic Press, San Diego, California.
7. BOWERS, M. D. and PUTTICK, G. M. 1988. Response of generalist and specialist insect to qualitative allelochemical variation. J. Chem. Ecol. 14:319-334.
8. BOWERS, M. D. and PUTTICK, G. M. 1989. Iridoid glycosides and insect feeding preferences: gypsy moths (Lymantria dispar, Lymantriidae) and buckeyes (Junonia coenia, Nymphalidae). Ecol. Entomol. 14:247-256.
9. BOWERS M. D. and STAMP, N. E. 1992. Chemical variation within and between individuals of Plantago lanceolata (Plantaginaceae). J. Chem. Ecol. 18:985-995.
10. BOWERS, M. D. and STAMP, N. E. 1993. Effects of plant age, genotype, and herbivory on Plantago performance and chemistry. Ecology 74:1778-1791.
11. BOWERS, M. D. and STAMP, N. E. 1997. Effects of host plant genotype and predators on iridoid glycoside content of pupae of a specialist insect herbivore, Junonia coenia (Nymphalidae). Biochem. Syst. Ecol. 25:571-580.
12. BOWERS, M. D., COLLINGE, S. K., GAMBLE, S. E., and SCHMITT, J. 1992. Effects of genotype, habitat, and seasonal variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores. Oecologia 91:201-207.
13. CAMARA, M. D. 1997. Predator responses to sequestered plant toxins in the buckeye caterpillars: are tritrophic interactions locally variable? J. Chem. Ecol. 23:2093-2106.
14. DAMTOFT, S., JENSEN, S. R., and NIELSEN, B. J. 1983. The biosynthesis of iridoid glucosides from 8-epi-deoxyloganic acid. Biochem. Soc. Trans. 11: 593-594.
15. DARROW, K. and BOWERS, M. D. 1997. Phenological and population variation in iridoid glycosides of Plantago lanceolata (Plantaginaceae). Biochem. Syst. Ecol. 25:1-11.
16. DARROW, K. and BOWERS, M. D. 1999. Effects of herbivore damage and nutrient level on induction of iridoid glycosides in Plantago lanceolata. J. Chem. Ecol. 25:1427-1440.
17. DAVINI, E., IAVARONE, C., TROGOLO, C., AURELI, P., and PASOLINI, B. 1986. The quantitative isolation and antimicrobial activity of the aglycone of aucubin. Phytochemistry 25:2420-2422.
18. DE NOOIJ, M. P. and VAN DER AA, H. A. 1987. Phomopsis subordinaria and associated stalk disease in natural populations of Plantago lanceolata. Can. J. Bot. 65:2318-2325.
19. DUFF, R. B., BACON, J. S. D., MUNDIE, C. M., FARMER, V. C., RUSSELL, J. D., and FORRESTER, A. R. 1965. Catalpol and methylcatalpol: Naturally ocurring glycosides in Plantago and Buddleia species. Biochem. J. 96:1-5.
20. DYER, L. A. and BOWERS, M. D. 1996. The importance of sequestered iridoid glycosides as a defense against an ant predator. J. Chem. Ecol. 22:1527-1539.
21. 2 environments on production of carbon-based allelochemicals in Plantago: a test of the carbon/nutrient balance hypothesis. Am. Nat. 104:707-723.
22. FELTON, G. W. and KORTH, K. L. 2000. Trade-offs between pathogen and herbivore resistance. Curr. Opin. Plant Biol. 3:309-314.
23. GANGE, A. C. and WEST, H. M. 1994. Interactions between arbuscular mycorrhizal fungi and foliarfeeding insects on Plantago lanceolata L. New Phytol. 128:79-87.
24. GARDNER, D. R. and STERMITZ, F. R. 1988. Host plant utilization and iridoid glycoside sequestration by Euphdryas anicia (Lepidoptera: Nymphalidae). J. Chem. Ecol. 14:2147-2168.
25. HAECK, J. 1992. Phytosociology of Plantago habitats in the Netherlands and the relation with habitat characteristics, pp. 20-29, in P. J. C. Kuiper and M. Bos (eds.). Plantago. A Multidisciplinary Study. Springer-Verlag, Berlin.
26. HAMMERSCHMIDT, R. and KUC, J. 1995. Induced Resistance to Disease in Plants. Kluwer Academic Publishers, Dordrecht, The Netherlands.
27. HAMMERSCHMIDT, R. and SCHULTZ, J. C. 1996. Multiple Defenses and Signals in Plant Defense against Pathogens and Herbivores. Rec. Adv. Phytochem. 30:122-154.
28. HARBORNE, J. B. 1993. Introduction to Ecological Biochemistry. 4th edn. Academic Press, London, United Kingdom.
29. HARTMANN, T. 1991. Alkaloids, pp. 79-121, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites, 2nd. ed. Academic Press, San Diego, California.
30. HATCHER, P. E. 1995. Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biol. Rev. 70:639-694.
31. HOUGEN-EITZMAN, D. and RAUSHER, M. D. 1994. Interactions between herbivorous insects and plantinsect coevolution. Am. Nat. 143:677-697.
32. ISHIGURO, K., YAMAKI, M., and TAKAGI, S. 1982. Studies on the iridoid related compounds. I. On antimicrobial activity of aucubigenin and certain iridoid aglycones. Yakugaku Zasshi 102:755-759.
33. JARZOMSKI, C. M., STAMP, N. E., and BOWERS, M. D. 2000. Effects of plant phenology, nutrients and herbivory on growth and defensive chemistry of plantain, Plantago lanceolata. Oikos 88:371-379.
34. JENSEN, S. R. 1991. Plant iridoids, their biosynthesis and distribution in angiosperms, pp. 133-158, in J. B. Harbome and F. A. Tomas-Barberan (eds.). Ecological Chemistry and Biochemistry of Plant Terpenoids. Clarendon Press, Oxford.
35. KARBAN, R. and BALDWIN, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, Illinois.
36. KLEPZIG, K. D., SMALLEY, E. B., and RAFFA, K. F. 1996. Combined chemical defenses against an insect-fungal complex. J. Chem. Ecol. 22:1367-1385.
37. KLOCKARS, G. K., BOWERS, M. D., and COONEY, B. 1993. Leaf variation in iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and oviposition of the buckeye butterfly, Junonia coenia (Nymphalidae). Chemoecology 4:72-78.
38. KOGAN, M. and FISCHER, D. C. 1991. Inducible defences in soybean against herbivorous insects, pp. 347-378, in D. W. Tallamy and M. J. Raupp (eds.). Phytochemical Induction by Herbivores. John Wiley, New York.
39. KRISCHIK, V. A. 1991. Specific or generalized plant defense: reciprocal interactions between herbivores and pathogens, pp. 309-340, in P. Barbosa, V. A. Krischik and C. G. Jones (eds.). Microbial Mediation of Plant-Herbivore Interactions. John Wiley, New York.
40. KRISCHIK, V. A., GOTH, P., and BARBOSA, P. 1991. Generalized plant defense: effects on multiple species. Oecologia 85:562-571.
41. LINDERS, E. G. A. 1996. A possible role of sexuality in the population structure of Diaporthe adunca, a pathogen of Plantago lanceolata. Plant Pathol. 45:697-709.
42. LINDERS, E. G. A., VAN DAMME, J. M. M., and ZADOKS, J. C. 1996. Transmission and overseasoning of Diaporthe adunca on Plantago lanceolata. Plant Pathol. 45:59-69.
43. MARAK, H. B. 2000. Costs and benefits of iridoid glycosides as defense against pathogenic fungi of Plantago lanceolata. PhD thesis. Univerity of Utrecht, The Netherlands.
44. MARAK, H. B., BIERE, A., and VAN DAMME, J. M. M. 2000. Direct and correlated responses to selection on iridoid glycosides in Plantago lanceolata L. J. Evol. Biol. 13:985-996.
45. MARAK, H. B., BIERE, A., and VAN DAMME, J. M. M. 2002. Two herbivor-deterrent iridoid glycosides reduce the in-vitro growth of a specialist but not of a generalist pathogenic fungus of Plantago lanceolata. J. Chemoecology (in press).
46. MCGARVEY, D. J. and CROTEAU, R. 1995. Terpenoid metabolism. Plant Cell 7:1015-1026.
47. NITAO, J. K. and ZANGERL, A. R. 1987. Floral development and chemical defense allocation in wild parsnip (Pastinaca sativa). Ecology 68:521-529.
48. PAUL, N. D., HATCHER, P. E., and TAYLOR, J. E. 1999. Coping with multiple enemies: an integration of molecular and ecological perspectives. Trends Plant Sci. 5:220-225.
49. PEREYRA, P. C. and BOWERS, M. D. 1988. Iridoid glycosides as oviposition stimulants for the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 14:917-928.
50. RHOADES, D. F. 1979. Evolution of plant chemical defense against herbivores, pp. 3-54, in G. A. Rosenthal and D. H. Janzen (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York.
51. RODDICK, J. G. 1974. The steroidal glycoalkaloid tomatine. Phytochemistry 13:9-25.
52. ROMBOUTS, J. E. and LINKS, J. 1956. The chemical nature of the antibacterial substance present in Aucuba japonica Thunbg. Experientia 12:78-80.
53. SAGAR, G. R. and HARPER, J. L. 1964. Biological flora of the British Isles. Plantago major L., P. media L. and P. lanceolata L. J. Ecol. 52:189-221.
54. SINDEN, S. L., GROTH, R. W., and O'BRIEN, M. J. 1973. Effect of tomato alkaloids on the growth of Alternaria solani and their possible role as resistance factors in potatoes. Phytopathology 63:303-307.
55. SINDEN, S. L., SCHALK, J. M., and STONER, A. K. 1978. Effects of daylength and maturity of tomato plants on tomatine content and resistance to the Colorado potato beetle. J. Am. Soc. Hortic. Sci. 103:596-600.
56. STAMP, N. E. and BOWERS, M. D. 1994. Effects ofcages, plant age and mechanical clipping on plantain chemistry. Oecologia 99:66-71.
57. STAMP, N. E. and BOWERS, M. D. 1996. Consequences for plantain chemistry and growth when herbivores are attacked by predators. Ecology 77:535-549.
58. STAMP, N. E. and BOWERS, M. D. 2000. Do enemies ofherbivores influence plant growth and chemistry? Evidence from a seminatural experiment. J. Chem. Ecol. 26:2367-2386.
59. STERMITZ, F. R. 1988. Iridoid glycosides and aglycones as chiral synthons, bioactive compounds and Lepidopteran defenses, pp. 397-402, in H. G. Cutter (ed.) Biologically Active Natural Products. ACS Symposium 380. American Chemical Society, Washington, D.C.
60. STOUT, M. J. and BOSTOCK, R. M. 2000. Specificity of induced responses to arthropods and pathogens, pp. 183-209, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.). Induced Plant Defenses Against Herbivores. Biochemistry, Ecology, and Agriculture. APS Press, St. Paul, Minnesota,
61. TUOMI, J., NIEMELÄ, P., ROUSI, M., SIRÉN, S., and VUORISALO, T. 1988. Induced accumulation of foliage phenols in mountain birch: branch response to defoliation. Am. Nat. 132:602-608.
62. VAN DER SLUIS, W. G., VAN DER NAT, J. M., and LABADIE, R. P. 1983. Thin-layer chromatographic bioassay of iridoid and secoiridoid glucosides with a fungitoxic aglucone moiety using β-glucosidase and the fungus Penicillium expansum as a test organism. J. Chromatogr. 259:522-526.
63. VAN DER TOORN, J., TEN HOVE, H. J., and VAN ELDIJK, F. 1984. Transplant experiments with Plantago lanceolata. Progress Report 82, Institute for Ecological Research, Heteren, NL, pp. 39-44.
64. WINK, M. 1984. Chemical defense of Leguminosae: are quinolizidine alkaloids part of the antimicrobial system of lupines ? Z. Naturforsch. C 39:548-552.
65. ZANGERL, A. R. and BERENBAUM, M. R. 1990. Furanocoumarin induction in wild parsnip: genetics and populational variation. Ecology 71:1933-1940.
66. ZANGERL, A. R. and RUTLEDGE, C. E. 1996. The probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. Am. Nat. 147:599-608.