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Extrafloral nectar secretion from wounds of Solanum dulcamara

Nature Plants volume 2, Article number: 16056 (2016) Cite this article

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Abstract

Plants usually close wounds rapidly to prevent infections and the loss of valuable resources such as assimilates1. However, herbivore-inflicted wounds on the bittersweet nightshade Solanum dulcamara appear not to close completely and produce sugary wound secretions visible as droplets. Many plants across the plant kingdom secrete sugary nectar from extrafloral nectaries2 to attract natural enemies of herbivores for indirect defence3,4. As ants forage on wound edges of S. dulcamara in the field, we hypothesized that wound secretions are a form of extrafloral nectar (EFN). We show that, unlike EFN from known nectaries, wound secretions are neither associated with any specific structure nor restricted to certain locations. However, similar to EFN, they are jasmonate-inducible and the plant controls their chemical composition. Wound secretions are attractive for ants, and application of wound secretion mimics increases ant attraction and reduces herbivory on S. dulcamara plants in a natural population. In greenhouse experiments, we reveal that ants can defend S. dulcamara from two of its native herbivores, slugs and flea beetle larvae. Since nectar is defined by its ecological function as a sugary secretion involved in interactions with animals5, such ‘plant bleeding’ could be a primitive mode of nectar secretion exemplifying an evolutionary origin of structured extrafloral nectaries.

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Figure 1: Wound secretions of S. dulcamara.
Figure 2: S. dulcamara wound secretions differ from phloem sap, are regulated by jasmonic acid, and attract ants.
Figure 3: Higher ant attendance reduces leaf damage on S. dulcamara in nature.
Figure 4: Ants reduce performance and herbivory of two native herbivores on S. dulcamara.

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Acknowledgements

We thank our students J. Schößler and M. Wank for help during experiments, A. Erban for assistance on the analysis of the GC–MS chromatograms, R. Radek for supporting SEM measurements and T. Sonsalla for help with figure art work. We thank the Freie Universität Berlin for funding as well as the German Research Foundation (DFG) for financial support to establish a German–Dutch cooperation (DFG: STE_2014_1_1). O.W.C. was funded by a grant of the bilateral agreement for higher education (Erasmus) between the Freie Universität Berlin and Radboud University, and a stipend of the CRC973 funded by the DFG. A.S. acknowledges funding by the CRC973 (project B2) and N.M.v.D. gratefully acknowledges the support of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig funded by the German Research Foundation (FZT 118).

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Authors and Affiliations

  1. Molecular Ecology, Dahlem Centre of Plant Sciences, Institute of Biology/Freie Universität Berlin, Haderslebener Strasse 9, 12163 Berlin, Germany

    Tobias Lortzing, Onno W. Calf, Marlene Böhlke, Daniel Geuß, Susanne Kosanke & Anke Steppuhn

  2. Molecular Interaction Ecology, Institute of Water and Wetland Research, Radboud University, PO Box 9010, 6500 GL Nijmegen, The Netherlands

    Onno W. Calf & Nicole M. van Dam

  3. Applied Metabolome Analysis, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam, Germany

    Jens Schwachtje & Joachim Kopka

  4. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany

    Nicole M. van Dam

  5. Institute of Ecology, Friedrich Schiller University Jena, Dornburger-Strasse. 159, 07743 Jena, Germany

    Nicole M. van Dam

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  1. Tobias Lortzing
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Contributions

T.L. and A.S. designed this study. The experimental work was planned by T.L., A.S., O.W.C., N.M.v.D., and for metabolite analysis also by J.K. Experiments and analyses were conducted by T.L., O.W.C., M.B., D.G., S.K. and additionally by J.S. and J.K. for the metabolite analysis. T.L. and A.S. wrote the first draft of the manuscript that was edited and revised by all authors.

Corresponding author

Correspondence to Anke Steppuhn.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Materials and Methods, Supplementary Tables 1–4 and Supplementary Figs 1–5. (PDF 625 kb)

Supplementary Dataset (XLSX 82 kb)

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Lortzing, T., Calf, O., Böhlke, M. et al. Extrafloral nectar secretion from wounds of Solanum dulcamara. Nature Plants 2, 16056 (2016). https://doi.org/10.1038/nplants.2016.56

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