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Potato tuber herbivory increases resistance to aboveground lepidopteran herbivores

  • Plant-microbe-animal interactions - original research
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Abstract

Plants mediate interactions between aboveground and belowground herbivores. Although effects of root herbivory on foliar herbivores have been documented in several plant species, interactions between tuber-feeding herbivores and foliar herbivores are rarely investigated. We report that localized tuber damage by Tecia solanivora (Guatemalan tuber moth) larvae reduced aboveground Spodoptera exigua (beet armyworm) and Spodoptera frugiperda (fall armyworm) performance on Solanum tuberosum (potato). Conversely, S. exigua leaf damage had no noticeable effect on belowground T. solanivora performance. Tuber infestation by T. solanivora induced systemic plant defenses and elevated resistance to aboveground herbivores. Lipoxygenase 3 (Lox3), which contributes to the synthesis of plant defense signaling molecules, had higher transcript abundance in T. solanivora-infested leaves and tubers than in equivalent control samples. Foliar expression of the hydroxycinnamoyl-CoA quinate hydroxycinnamoyl transferase (HQT) and 3-hydroxy-3-methylglutaryl CoA reductase I (HMGR1) genes, which are involved in chlorogenic acid and steroidal glycoalkaloid biosynthesis, respectively, also increased in response to tuber herbivory. Leaf metabolite profiling demonstrated the accumulation of unknown metabolites as well as the known potato defense compounds chlorogenic acid, α-solanine, and α-chaconine. When added to insect diet at concentrations similar to those found in potato leaves, chlorogenic acid, α-solanine, and α-chaconine all reduced S. exigua larval growth. Thus, despite the fact that tubers are a metabolic sink tissue, T. solanivora feeding elicits a systemic signal that induces aboveground resistance against S. exigua and S. frugiperda by increasing foliar abundance of defensive metabolites.

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Acknowledgments

This research was funded by United States Department of Agriculture—National Institute of Food and Agriculture award number 2014-67013-21659 to GJ and KP. We thank Meena Haribal and Melkamu G. Woldemariam for assistance with the metabolomics assays, and the Triad Foundation for making possible the purchase of a Thermo Q-Exactive mass spectrometer.

Author contribution statement

PK, EGG, EVO, KP, and GJ conceived and designed the experiments. PK, EVO, and EGG conducted the experiments. PK analyzed the data. PK, GJ, KP, EGG, and EVO wrote the manuscript.

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Authors and Affiliations

  1. Boyce Thompson Institute for Plant Research, 533 Tower Road, Ithaca, NY, 14853, USA

    Pavan Kumar, Erandi Vargas Ortiz & Georg Jander

  2. Department of Entomology, Cornell University, Ithaca, NY, 14853, USA

    Etzel Garrido & Katja Poveda

Authors
  1. Pavan Kumar
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  2. Erandi Vargas Ortiz
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  3. Etzel Garrido
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  4. Katja Poveda
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  5. Georg Jander
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Corresponding author

Correspondence to Georg Jander.

Additional information

Communicated by Colin Mark Orians.

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Kumar, P., Ortiz, E.V., Garrido, E. et al. Potato tuber herbivory increases resistance to aboveground lepidopteran herbivores. Oecologia 182, 177–187 (2016). https://doi.org/10.1007/s00442-016-3633-2

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