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Metabolomic profiling reveals shifts in defenses of an invasive plant

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Abstract

Post-introduction evolution of plant defense traits is fundamental to several important theories for plant invasiveness. Research on chemical defense traits of invasive plants has focused mostly on targeted chemical analysis, however, such analyses restrict novel insights to known compounds. Here, we provide an untargeted metabolomic analysis of native and invasive Purple Loosestrife populations and we experimentally test if admixture between introduced populations provides a basis for rapid defense chemistry evolution. Invasive populations showed improved growth and generalist herbivore resistance, but lower resistance to a specialist weevil, consistent with the Shifting Defense Hypothesis of plant invasions. Metabolomic profiling revealed large shifts in chemistry between native and invasive populations, including differences in alkaloids and flavonoids. Experimental admixture increased chemical diversity and plant growth in the native populations, indicating its potential to fuel rapid evolution, but admixture did not affect generalist and specialist herbivory. Our untargeted metabolomics analysis provides novel insights in the evolutionary changes in the chemistry of invasive plants, and reveals the chemical associations of a shift from defenses against specialist to generalist herbivores in invasive populations.

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Data availability

Data from LC–MS chemical profiling, plant phenotyping and herbivory assays are deposited in the open data repository ZENODO under https://doi.org/10.5281/zenodo.7198269.

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Acknowledgements

We thank Meta Schönau for facilitating the plant crossing at the Tübingen greenhouses, Sarah Gebauer for help with the experiment, Justin Fulkerson, Kirk Moloney, Claus Holzapfel, Lorenz Henneberg, Jasmin Joshi, and Jörg Müller for collecting seeds, and Bert Schipper for help with the chemical analyses. JS was supported by a grant from the China Scholarship Council (CSC file no. 201206140020). MM was supported by a DFG-SPP 1529 grant from the Deutsche Forschungsgemeinschaft.

Funding

JS was supported by a grant from the China Scholarship Council (CSC file no. 201206140020). MM was supported by a DFG-SPP 1529 grant from the Deutsche Forschungsgemeinschaft.

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Authors and Affiliations

  1. Institute of Ecology and Evolution, Plant Ecology Group, University of Tübingen, 72076, Tübingen, Germany

    Jun Shi, Katja Tielbörger & Mirka Macel

  2. Ningbo Academy of Agricultural Sciences, Ningbo, Zhejiang Province, People’s Republic of China

    Jun Shi

  3. Center for Plant Molecular Biology, Analytics Unit, University of Tübingen, 72076, Tübingen, Germany

    Mark Stahl

  4. Bioscience, Wageningen University and Research Centre, Wageningen, The Netherlands

    Ric C. H. de Vos

  5. Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB, Wageningen, The Netherlands

    Koen J. F. Verhoeven

  6. Aeres University of Applied Sciences, Arboretum West 98, 1325 WB, Almere, The Netherlands

    Mirka Macel

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  1. Jun Shi
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  2. Mark Stahl
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  3. Ric C. H. de Vos
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Contributions

JS, KT, MM and KJFV designed the experiments; JS performed the experiments; MS and RCHdV performed the chemical analyses; JS and MM analyzed the data; JS, KJFV and MM wrote the manuscript with input from all.

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Correspondence to Koen J. F. Verhoeven.

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Shi, J., Stahl, M., de Vos, R.C.H. et al. Metabolomic profiling reveals shifts in defenses of an invasive plant. Biol Invasions 25, 3293–3306 (2023). https://doi.org/10.1007/s10530-023-03109-0

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