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Variation in Below-to Aboveground Systemic Induction of Glucosinolates Mediates Plant Fitness Consequences under Herbivore Attack

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Abstract

Plants defend themselves against herbivore attack by constitutively producing toxic secondary metabolites, as well as by inducing them in response to herbivore feeding. Induction of secondary metabolites can cross plant tissue boundaries, such as from root to shoot. However, whether the potential for plants to systemically induce secondary metabolites from roots to shoots shows genetic variability, and thus, potentially, is under selection conferring fitness benefits to the plants is an open question. To address this question, we induced 26 maternal plant families of the wild species Cardamine hirsuta belowground (BG) using the wound-mimicking phytohormone jasmonic acid (JA). We measured resistance against a generalist (Spodoptera littoralis) and a specialist (Pieris brassicae) herbivore species, as well as the production of glucosinolates (GSLs) in plants. We showed that BG induction increased AG resistance against the generalist but not against the specialist, and found substantial plant family-level variation for resistance and GSL induction. We further found that the systemic induction of several GSLs tempered the negative effects of herbivory on total seed set production. Using a widespread natural system, we thus confirm that BG to AG induction has a strong genetic component, and can be under positive selection by increasing plant fitness. We suggest that natural variation in systemic induction is in part dictated by allocation trade-offs between constitutive and inducible GSL production, as well as natural variation in AG and BG herbivore attack in nature.

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Acknowledgements

We thank Mégane Rohrer and Ludovico Formenti for assisting with experimental work and trait measurements. This work was supported by Swiss National Science Foundation grants 179481 and 159869 to SR.

Author information

MB and SR conceived and designed the experiments. MB conducted experiments and chemical analyses. MB and SR analysed the data and wrote the manuscript. The authors declare no conflicts of interest.

Correspondence to Moe Bakhtiari.

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Bakhtiari, M., Rasmann, S. Variation in Below-to Aboveground Systemic Induction of Glucosinolates Mediates Plant Fitness Consequences under Herbivore Attack. J Chem Ecol (2020). https://doi.org/10.1007/s10886-020-01159-5

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Keywords

  • Brassicaceae
  • Fitness impact of herbivory
  • Generalist herbivore
  • Glucosinolates
  • Induced systemic resistance
  • Plant-herbivore interaction