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Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites

  • Plant-microbe-animal interactions - Original research
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Abstract

Induced defenses mediate interactions between parasites sharing the same host plant, but the outcomes of these interactions are challenging to predict because of spatiotemporal variation in plant responses and differences in defense pathways elicited by herbivores or pathogens. Dissecting these mediating factors necessitates an approach that encompasses a diversity of parasitic feeding styles and tracks interactions over space and time. We tested indirect plant-mediated relationships across three tomato (Solanum lycopersicum) consumers: (1) the fungal pathogen—powdery mildew, Oidium neolycopersici; (2) a sap-feeding insect—silverleaf whitefly, Bemisia tabaci; and (3) a chewing insect—the leaf miner, Tuta absoluta. Further, we evaluated insect/pathogen responses on local vs. systemic leaves and over short (1 day) vs. long (4 days) time scales. Overall, we documented: (1) a bi-directional negative effect between O. neolycopersici and B. tabaci; (2) an asymmetrical negative effect of B. tabaci on T. absoluta; and (3) an asymmetrical positive effect of T. absoluta on O. neolycopersici. Spatiotemporal patterns varied depending on the species pair (e.g., whitefly effects on leaf miner performance were highly localized to the induced leaf, whereas effects on pathogen growth were both local and systemic). These results highlight the context-dependent effects of induced defenses on a diverse community of tomato parasites. Notably, the outcomes correspond to those predicted by phytohormonal theory based on feeding guild differences with key implications for the recent European invasion by T. absoluta.

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Acknowledgments

The authors declare that they have no conflict of interest and that all experiments were conducted in compliance with US law. We thank the editor (Roland Brandl), two anonymous reviewers for helpful comments on an earlier version of this manuscript, and Hélène Kazuro for assistance throughout the experiments. This work was supported by funds from the Environment and Agronomy department of INRA and from the French ministry of agriculture (CASDAR 10063) to ND.

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  1. Raphaëlle Mouttet

    Present address: Laboratoire de la Santé des Végétaux, unité entomologie et plantes invasives, ANSES, Campus international de Baillarguet, 34988, Montferrier-sur Lez, France

Authors and Affiliations

  1. French National Institute for Agricultural Research (INRA), ISA, 400 Route des Chappes, 06903, Sophia-Antipolis, France

    Raphaëlle Mouttet, Philippe Bearez, Edwige Amiens-Desneux & Nicolas Desneux

  2. Department of Entomology, Purdue University, 901 W. State St., West Lafayette, IN, USA

    Ian Kaplan

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  1. Raphaëlle Mouttet
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Correspondence to Nicolas Desneux.

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Communicated by Roland Brandl.

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Mouttet, R., Kaplan, I., Bearez, P. et al. Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites. Oecologia 173, 1379–1386 (2013). https://doi.org/10.1007/s00442-013-2716-6

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