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Systemic, Genotype-Specific Induction of Two Herbivore-Deterrent Iridoid Glycosides in Plantago lanceolata L. in Response to Fungal Infection by Diaporthe adunca (Rob.) Niessel

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Abstract

Iridoid glycosides are a group of terpenoid secondary plant compounds known to deter generalist insect herbivores. In ribwort plantain (Plantago lanceolata), the iridoid glycosides aucubin and catalpol can be induced following damage by insect herbivores. In this study, we investigated whether the same compounds can be induced following infection by the fungal pathogen Diaporthe adunca, the causal agent of a stalk disease in P. lanceolata. Significant induction of aucubin and catalpol was observed in two of the three plant genotypes used in this study following inoculation with the pathogen. In one of the genotypes, induction occurred within 6 hr after inoculation, and no decay was observed within 8 days. The highest level of induction was observed in reproductive tissues (spikes and stalks) where infection took place. In these tissues, iridoid glycoside levels in infected plants were, on average, 97% and 37% higher than the constitutive levels in the corresponding control plants, respectively. Significant induction was also observed in leaves (24%) and roots (17%). In addition to significant genotypic variation in the level of induction, we found genetic variation for the tissue-specific pattern of induction, further broadening the scope for evolutionary fine-tuning of induced responses. Recent studies have revealed a negative association between iridoid glycoside levels in P. lanceolata genotypes and the amount of growth and reproduction of D. adunca that these genotypes support. However, for the three genotypes used in the present study, differences in resistance were not related to their constitutive or induced levels of iridoid glycosides, suggesting that additional resistance mechanisms are important in this host-pathogen system. We conclude that iridoid glycosides in P. lanceolata can be induced both by arthropods and pathogenic micro-organisms. Pathogen infection could, therefore, potentially enhance resistance to generalist insect herbivores in this species.

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REFERENCES

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Bailey, J. A. and Mansfield, J. W. (eds.). 1982. Phytoalexins. Blackie, Glasgow.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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. 2446 MARAK, BIERE, AND VAN DAMME

    Chapter  Google Scholar 

  • Bowers, M. D. and Puttick, G. M. 1988. Response of generalist and specialist insect to qualitative allelochemical variation. J. Chem. Ecol. 14:319–334.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bowers, M. D. and Stamp, N. E. 1992. Chemical variation within and between individuals of Plantago lanceolata (Plantaginaceae). J. Chem. Ecol. 18:985–995.

    Article  CAS  Google Scholar 

  • Bowers, M. D. and Stamp, N. E. 1993. Effects of plant age, genotype, and herbivory on Plantago performance and chemistry. Ecology 74:1778–1791.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Darrow, K. and Bowers, M. D. 1997. Phenological and population variation in iridoid glycosides of Plantago lanceolata (Plantaginaceae). Biochem. Syst. Ecol. 25:1–11.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Fajer, E. D., Bowers, M. D., and Bazzaz, F. A. 1992. The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago: a test of the carbon/nutrient balance hypothesis. Am. Nat. 104:707–723.

    Article  Google Scholar 

  • Felton, G. W. and Korth, K. L. 2000. Trade-offs between pathogen and herbivore resistance. Curr. Opin. Plant Biol. 3:309–314.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Hammerschmidt, R. and Kuc, J. 1995. Induced Resistance to Disease in Plants. Kluwer Academic Publishers, Dordrecht, The Netherlands.

  • Hammerschmidt, R. and Schultz, J. C. 1996. Multiple Defenses and Signals in Plant Defense against Pathogens and Herbivores. Rec. Adv. Phytochem. 30:122–154.

    Google Scholar 

  • Harborne, J. B. 1993. Introduction to Ecological Biochemistry. 4th edn. Academic Press, London, United Kingdom.

    Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Hatcher, P. E. 1995. Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biol. Rev. 70:639–694.

    Article  Google Scholar 

  • Hougen-Eitzman, D. and Rausher, M. D. 1994. Interactions between herbivorous insects and plantinsect coevolution. Am. Nat. 143:677–697.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Jensen, S. R. 1991. Plant iridoids, their biosynthesis and distribution in angiosperms, pp. 133–158, in J. B. Harborne and F. A. Tomas-Barberan (eds.). Ecological Chemistry and Biochemistry of Plant Terpenoids. Clarendon Press, Oxford.

    Google Scholar 

  • Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, Illinois.

    Book  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Krischik, V. A., Goth, P., and Barbosa, P. 1991. Generalized plant defense: effects on multiple species. Oecologia 85:562–571.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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).

  • Mcgarvey, D. J. and Croteau, R. 1995. Terpenoid metabolism. Plant Cell 7:1015–1026.

    Article  CAS  Google Scholar 

  • Nitao, J. K. and Zangerl, A. R. 1987. Floral development and chemical defense allocation in wild parsnip (Pastinaca sativa). Ecology 68:521–529.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Roddick, J. G. 1974. The steroidal glycoalkaloid tomatine. Phytochemistry 13:9–25.

    Article  CAS  Google Scholar 

  • Rombouts, J. E. and Links, J. 1956. The chemical nature of the antibacterial substance present in Aucuba japonica Thunbg. Experientia 12:78–80.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Stamp, N. E. and Bowers, M. D. 1994. Effects of cages, plant age and mechanical clipping on plantain chemistry. Oecologia 99:66–71.

    Article  Google Scholar 

  • Stamp, N. E. and Bowers, M. D. 1996. Consequences for plantain chemistry and growth when herbivores are attacked by predators. Ecology 77:535–549.

    Article  Google Scholar 

  • Stamp, N.E. and Bowers, M.D. 2000. Do enemies of herbivores influence plant growth and chemistry? Evidence from a seminatural experiment. J. Chem. Ecol. 26:2367–2386.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Google Scholar 

  • Tuomi, J., NiemelÄ, P., Rousi, M., SirÄn, S., and Vuorisalo, T. 1988. Induced accumulation of foliage phenols in mountain birch: branch response to defoliation. Am. Nat. 132:602–608.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Wink, M. 1984. Chemical defense of Leguminosae: are quinolizidine alkaloids part of the antimicrobial system of lupines ? Z. Naturforsch. C 39:548–552.

    Google Scholar 

  • Zangerl, A. R. and Berenbaum, M. R. 1990. Furanocoumarin induction in wild parsnip: genetics and populational variation. Ecology 71:1933–1940.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

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Marak, H.B., Biere, A. & Van Damme, J.M.M. Systemic, Genotype-Specific Induction of Two Herbivore-Deterrent Iridoid Glycosides in Plantago lanceolata L. in Response to Fungal Infection by Diaporthe adunca (Rob.) Niessel. J Chem Ecol 28, 2429–2448 (2002). https://doi.org/10.1023/A:1021475800765

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