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Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores

  • Plant-microbe-animal interactions - Original research
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Abstract

Plants are frequently attacked by both pathogens and insects, and an attack from one can induce plant responses that affect resistance to the other. However, we currently lack a predictive framework for understanding how pathogens, their vectors, and other herbivores interact. To address this gap, we have investigated the effects of a viral infection in the host plant on both its aphid vector and non-vector herbivores. We tested whether the infection by three different strains of Potato virus Y (PVYNTN, PVYNO and PVYO) on tomato plants affected: (1) the induced plant defense pathways; (2) the abundance and fecundity of the aphid vector (Macrosiphum euphorbiae); and (3) the performance of two non-vector species: a caterpillar (Trichoplusia ni) and a beetle (Leptinotarsa decemlineata). While infection by all three strains of PVY induced the salicylate pathway, PVYNTN induced a stronger and longer response. Fecundity and density of aphids increased on all PVY-infected plants, suggesting that the aphid response is not negatively associated with salicylate induction. In contrast, the performance of non-vector herbivores positively correlated with the strength of salicylate induction. PVYNTN infection decreased plant resistance to both non-vector herbivores, increasing their growth rates. We also demonstrated that the impact of host plant viral infection on the caterpillar results from host plant responses and not the effects of aphid vector feeding. We propose that pathogens chemically mediate insect–plant interactions by activating the salicylate pathway and decreasing plant resistance to chewing insects, which has implications for both disease transmission and insect community structure.

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Acknowledgments

We are greatly indebted to Dawn Smith and Stewart Gray’s laboratory for kindly helping us with viral infection and proving the virus strains used in the experiments. We thank Rayko Halitschke for his valuable assistance in the phytohormone analyses, Ordom Huot for his help with laboratory work, and Cesar Rodriguez-Saona and Isgouhi Kaloshian for providing the aphids. This study strongly benefited from comments and suggestions by Anurag Agrawal, Alison Power, Gui Becker, Suzi Claflin, Scott McArt, Ian Kaplan, the editor John Lill, and two anonymous reviewers. This project received financial support from Sigma Xi (Cornell Chapter), the Department of Ecology and Evolutionary Biology, and the Department of Entomology at Cornell. M. F. K. B. is recipient of the Olin fellowship and the CAPES/Fulbright fellowship (BEX 2234-08-4). The experiments comply with the current laws of the USA, in which the experiments were performed.

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  1. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14853, USA

    Mônica F. Kersch-Becker & Jennifer S. Thaler

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

    Mônica F. Kersch-Becker & Jennifer S. Thaler

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  1. Mônica F. Kersch-Becker
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Correspondence to Mônica F. Kersch-Becker.

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Communicated by John Lill.

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Kersch-Becker, M.F., Thaler, J.S. Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores. Oecologia 174, 883–892 (2014). https://doi.org/10.1007/s00442-013-2812-7

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