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Priming Seeds with Indole and (Z)-3-Hexenyl Acetate Enhances Resistance Against Herbivores and Stimulates Growth

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Abstract

A striking feature of plant ecology is the ability of plants to detect and respond to environmental cues such as herbivore-induced plant volatiles (HIPVs) by priming or directly activating defenses against future herbivores. However, whether seeds also respond to compounds that are common constituents of HIPV blends and initiate future plant resistance is unknown. Considering that seeds depend on other environmental cues to determine basic survival traits such as germination timing, we predicted that seeds exposed to synthetic constituents of HIPV blends would generate well-defended plants. We investigated the effect of seed exposure to common volatiles on growth, reproduction, and resistance characteristics in the model plants Arabidopsis thaliana and Medicago truncatula using herbivores from two feeding guilds. After seed scarification and vernalization, we treated seeds with one of seven different plant-derived volatile compounds for 24 h. Seeds were then germinated and the resulting plants were assayed for growth, herbivore resistance, and expression of inducible defense genes. Of all the synthetic volatiles tested, indole specifically reduced both beet armyworm growth on A. thaliana and pea aphid fecundity on M. truncatula. The induction of defense genes was not affected by seed exposure to indole in either plant species, indicating that activation of direct resistance rather than inducible resistance is the mechanism by which seed priming operates. Moreover, neither plant species showed any negative effect of seed exposure to any synthetic volatile on vegetative and reproductive growth. Rather, M. truncatula plants derived from seeds exposed to (Z)-3-hexanol and (Z)-3-hexenyl acetate grew larger compared to controls. Our results indicate that seeds are sensitive to specific volatiles in ways that enhance resistance profiles with no apparent costs in terms of growth. Seed priming by HIPVs may represent a novel ecological mechanism of plant-to-plant interactions, with broad potential applications in agriculture and seed conservation.

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Acknowledgements

This work was supported financially in part by a National Science Foundation grants IOS-2101059 and IOS-1656625 to C.J.F. We thank Dr. Julia Frugoli for generously providing M. truncatula, A-17 seeds and Dr. Susana Karen Gomez for supplying the pea aphids. We thank Allie Peot, Rachel Haslem and Grace Freundlich for lab assistance. Raysun Frost and Maria Shields provided critical feedback on the manuscript. Comments from two anonymous reviewers improved the manuscript.

Funding

This work was supported financially in part by a National Science Foundation grants IOS-2101059 and IOS-1656625 to C.J.F.

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Authors and Affiliations

  1. Department of Biology, University of Louisville, 40292, Louisville, KY, USA

    Abhinav K. Maurya, Leila Pazouki & Christopher J. Frost

  2. BIO5 Institute, University of Arizona, 85721, Tucson, AZ, USA

    Christopher J. Frost

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  1. Abhinav K. Maurya
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  2. Leila Pazouki
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  3. Christopher J. Frost
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Correspondence to Christopher J. Frost.

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Maurya, A.K., Pazouki, L. & Frost, C.J. Priming Seeds with Indole and (Z)-3-Hexenyl Acetate Enhances Resistance Against Herbivores and Stimulates Growth. J Chem Ecol 48, 441–454 (2022). https://doi.org/10.1007/s10886-022-01359-1

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  • DOI: https://doi.org/10.1007/s10886-022-01359-1

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