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Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant

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Abstract

Legume-associated nitrogen-fixing bacteria play a key role for plant performance and productivity in natural and agricultural ecosystems. Although this plant-microbe mutualism has been known for decades, studies on effects of rhizobia colonisation on legume-herbivore interactions are scarce. We hypothesized that additional nitrogen provided by rhizobia may increase plant resistance by nitrogen-based defense mechanisms. We studied this below-aboveground interaction using a system consisting of lima bean (Phaseolus lunatus L.), rhizobia, and the Mexican bean beetle (Epilachna varivestis Muls.) as an insect herbivore. We showed that the rhizobial symbiosis not only promotes plant growth but also improves plant defense and resistance against herbivores. Results of our study lead to the suggestion that nitrogen provided by rhizobia is allocated to the production of nitrogen-containing cyanogenic defense compounds, and thereby crucially determines the outcome of plant-herbivore interactions. Our study supports the view that the fitness benefit of root symbioses includes defence mechanisms and thus extends beyond the promotion of plant growth. Since the associations between legumes and nitrogen-fixing rhizobia are ubiquitous in terrestrial ecosystems, improved knowledge on rhizobia-mediated effects on plant traits―and the resulting effects on higher trophic levels―is important for better understanding of the role of these microbes for ecosystem functioning.

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Abbreviations

HCNp:

cyanogenic potential; amount of cyanogenic precursors in a given plant tissue

L:D:

light:dark period

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Acknowledgements

We acknowledge funding through the University of Duisburg-Essen and the German Science Foundation (Deutsche Forschungsgemeinschaft; DFG, grant Ba 3966/1-1). We further would like to thank Manfred Jensen for fruitful discussions and Sascha Eilmus for cultivation of bacteria. We especially thank Prof. Peter Bayer for his continuous support.

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Authors and Affiliations

  1. Department of General Botany/Plant Ecology, University of Duisburg-Essen, Universitätsstr. 5, 45117, Essen, Germany

    Sylvia Thamer

  2. Department Community Ecology, Helmholtz-Centre for Environmental Research - UFZ, Theodor-Lieser-Str. 4, 06120, Halle, Germany

    Martin Schädler

  3. Ghent University, Terrestrial Ecology Unit, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Dries Bonte

  4. Department of Plant Biology, University of Minnesota, 250 Biological Sciences Center, 1445 Gortner Ave, St. Paul, MN, 55108, USA

    Daniel J. Ballhorn

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  1. Sylvia Thamer
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  2. Martin Schädler
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  4. Daniel J. Ballhorn
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Correspondence to Daniel J. Ballhorn.

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Responsible Editor: Juha Mikola.

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Thamer, S., Schädler, M., Bonte, D. et al. Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant. Plant Soil 341, 209–219 (2011). https://doi.org/10.1007/s11104-010-0635-4

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