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Resistance in the Plant, Barbarea vulgaris, and Counter-Adaptations in Flea Beetles Mediated by Saponins

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Abstract

Three saponins and two sapogenins had differential effects on food consumption in five near-isogenic flea beetle lines, which differ in their ability to utilize a novel host plant, Barbarea vulgaris (Brassicaceae). The ability to live on this plant is controlled by major, dominant R-genes in the flea beetle, Phyllotreta nemorum (Coleoptera: Chrysomelidae: Alticinae). A susceptible genotype (rr) is unable to live on the plant, whereas resistant genotypes (RR and Rr) can utilize the novel host plant. Among compounds isolated from B. vulgaris, hederagenin cellobioside (hederagenin-3-O-(4-O-β-D-glucopyranosyl)-β-D-glucopyranoside) inhibited feeding, whereas the effect of oleanolic acid cellobioside was much weaker. The aglycones (sapogenins) were inactive. Although hederagenin cellobioside was active against all flea beetle lines, its effect on food consumption was much stronger on the susceptible genotype (rr) compared to the resistant genotype (Rr). Susceptible and resistant flea beetle genotypes were equally sensitive to a non-host saponin, α-hederin (hederagenin-3-O-(2-O-α-L-rhamnopyranosyl)-α-L-arabinopyranoside). These results suggest that R-alleles in flea beetles might be specific adaptations to defensive saponins in B. vulgaris. A possible mechanism of action of the R-alleles might be to encode for an enzyme (e.g. a glucosidase), which is able to cleave glycosidic bonds in hederagenin cellobioside, but not in α-hederin. The potential role of saponins as defensive compounds in B. vulgaris and as targets for counter-adaptations in flea beetles and other insects is discussed.

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Acknowledgements

We thank David B. Collinge, Manabu Kamimura, Tamara van Mölken, Mari-Anne Newman, Carl Erik Olsen, and Vera Kuzina Poulsen for helpful comments on the manuscript. The work was supported by grants from The Danish Natural Science Research Council (21-02-0534) and The Danish Agency for Science, Technology and Innovation (274-06-0370).

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Authors and Affiliations

  1. Department of Basic Sciences and Environment, Faculty of Life Sciences, University of Copenhagen, Thorvaldsensvej 40, DK 1871, Frederiksberg C, Denmark

    Jens K. Nielsen

  2. Faculty of Pharmaceutical Science, Fukuoka University, 8-19-1, Nanakuma, Jonan-ku, Fukuoka, Japan

    Tsuneatsu Nagao & Hikaru Okabe

  3. National Institute of Agrobiological Sciences, Ohwashi 1-2, Tsukuba, Ibaraki, 305-8634, Japan

    Tetsuro Shinoda

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  1. Jens K. Nielsen
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  2. Tsuneatsu Nagao
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  3. Hikaru Okabe
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  4. Tetsuro Shinoda
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Correspondence to Jens K. Nielsen.

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Tsuneatsu Nagao deceased: Sept 24, 2002.

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Nielsen, J.K., Nagao, T., Okabe, H. et al. Resistance in the Plant, Barbarea vulgaris, and Counter-Adaptations in Flea Beetles Mediated by Saponins. J Chem Ecol 36, 277–285 (2010). https://doi.org/10.1007/s10886-010-9758-6

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