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Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs?

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Abstract

Plants are often attacked by multiple enemies, including pathogens and herbivores. While many plant secondary metabolites show specific effects toward either pathogens or herbivores, some can affect the performance of both these groups of natural enemies and are considered to be “generalized defense compounds”. We tested whether aucubin and catalpol, two iridoid glycosides present in ribwort plantain (Plantago lanceolata), confer in vivo resistance to both the generalist insect herbivore Spodoptera exigua and the biotrophic fungal pathogen Diaporthe adunca using plants from P. lanceolata lines that had been selected for high- and low-leaf iridoid glycoside concentrations for four generations. The lines differed approximately three-fold in the levels of these compounds. Plants from the high-selection line showed enhanced resistance to both S. exigua and D. adunca, as evidenced by a smaller lesion size and a lower fungal growth rate and spore production, and a lower larval growth rate and herbivory under both choice and no-choice conditions. Gravimetric analysis revealed that the iridoid glycosides acted as feeding deterrents to S. exigua, thereby reducing its food intake rate, rather than having post-ingestive toxic effects as predicted from in vitro effects of hydrolysis products. We suggest that the bitter taste of iridoid glycosides deters feeding by S. exigua, whereas the hydrolysis products formed after tissue damage following fungal infection mediate pathogen resistance. We conclude that iridoid glycosides in P. lanceolata can serve as broad-spectrum defenses and that selection for pathogen resistance could potentially result in increased resistance to generalist insect herbivores and vice versa, resulting in diffuse rather than pairwise coevolution.

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Acknowledgements

We thank Karin Mudde and Slavica Ivanovic for their help with the inoculations and herbivore experiments, Sonja Honders for setting up the HPLC analyses, Wiecher Smant for performing the plant nitrogen and phosphorus analyses and Jeff Harvey and two anonymous reviewers for their constructive comments on earlier versions of the manuscript. H.B.M. was supported by a grant from the Egyptian government. Publication 3347, Netherlands Institute of Ecology, NI00-KNAW.

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  1. Department of Plant Population Biology, Netherlands Institute of Ecology (NIOO-KNAW), P.O. Box 40, 6666 ZG, Heteren, The Netherlands

    Arjen Biere, Hamida B. Marak & Jos M. M. van Damme

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  1. Arjen Biere
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  2. Hamida B. Marak
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  3. Jos M. M. van Damme
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Correspondence to Arjen Biere.

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Biere, A., Marak, H.B. & van Damme, J.M.M. Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs?. Oecologia 140, 430–441 (2004). https://doi.org/10.1007/s00442-004-1603-6

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