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A Native Parasitic Plant Systemically Induces Resistance in Jack Pine to a Fungal Symbiont of Invasive Mountain Pine Beetle

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Abstract

Conifer trees resist pest and pathogen attacks by complex defense responses involving different classes of defense compounds. However, it is unknown whether prior infection by biotrophic pathogens can lead to subsequent resistance to necrotrophic pathogens in conifers. We used the infection of jack pine, Pinus banksiana, by a common biotrophic pathogen dwarf mistletoe, Arceuthobium americanum, to investigate induced resistance to a necrotrophic fungus, Grosmannia clavigera, associated with the mountain pine beetle, Dendroctonus ponderosae. Dwarf mistletoe infection had a non-linear, systemic effect on monoterpene production, with increasing concentrations at moderate infection levels and decreasing concentrations at high infection levels. Inoculation with G. clavigera resulted in 33 times higher monoterpene concentrations and half the level of phenolics in the necrotic lesions compared to uninoculated control trees. Monoterpene production following dwarf mistletoe infection seemed to result in systemic induced resistance, as trees with moderate disease severity were most resistant to G. clavigera, as evident from shorter lesion lengths. Furthermore, trees with moderate disease severity had the highest systemic but lowest local induction of α-pinene after G. clavigera inoculation, suggesting a possible tradeoff between systemically- and locally-induced defenses. The opposing effects to inoculation by G. clavigera on monoterpene and phenolic levels may indicate the potential for biosynthetic tradeoffs by the tree between these two major defense classes. Our results demonstrate that interactions between a biotrophic parasitic plant and a necrotrophic fungus may impact mountain pine beetle establishment in novel jack pine forests through systemic effects mediated by the coordination of jack pine defense chemicals.

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Acknowledgements

Funding for this research was provided by the Alberta Innovates–New Faculty Award, Canada Research Chairs program, and NSERC-Discovery to N. E., as well as Alberta Innovates Technology Futures, the Vanier Canada Graduate Scholarship, and the Izzak Walton Killam Memorial Scholarship to J. G. K. We would like to thank L. Barnhardt from Alberta Environment and Parks for help with site selection and S. Taft, A. Sturm, I. Lusebrink and J. Therrien (University of Alberta) for field assistance. Furthermore, we acknowledge the contribution of S. Landhäusser and P. Chow (University of Alberta) in conducting carbohydrate analysis. We are also thankful to two anonymous reviewers for their constructive suggestions that greatly improved the manuscript.

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  1. Patrick Sherwood

    Present address: The James Hutton Institute, Craigiebuckler Aberdeen, Scotland, AB15 8QH, UK

Authors and Affiliations

  1. Department of Renewable Resources, University of Alberta, Edmonton, AB, T6G 2E3, Canada

    Jennifer G. Klutsch, Ahmed Najar & Nadir Erbilgin

  2. Department of Plant Pathology, The Ohio State University, Columbus, OH, 43210, USA

    Patrick Sherwood & Pierluigi Bonello

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  1. Jennifer G. Klutsch
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Correspondence to Jennifer G. Klutsch.

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Klutsch, J.G., Najar, A., Sherwood, P. et al. A Native Parasitic Plant Systemically Induces Resistance in Jack Pine to a Fungal Symbiont of Invasive Mountain Pine Beetle. J Chem Ecol 43, 506–518 (2017). https://doi.org/10.1007/s10886-017-0845-9

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