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The Oxylipin Signaling Pathway Is Required for Increased Aphid Attraction and Retention on Virus-Infected Plants

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Abstract

Many studies have shown that virus infection alters phytohormone signaling and insect vector contact with hosts. Increased vector contact and movement among plants should increase virus survival and host range. In this study we examine the role of virus-induced changes in phytohormone signaling in plant-aphid interactions, using Pea enation mosaic virus (PEMV), pea aphids (Acyrthosiphon pisum), and pea (Pisum sativum) as a model. We observed that feeding by aphids carrying PEMV increases salicylic acid and jasmonic acid accumulation in pea plants compared to feeding by virus-free aphids. To determine if induction of the oxylipin jasmonic acid is critical for aphid settling, attraction, and retention on PEMV-infected plants, we conducted insect bioassays using virus-induced gene silencing (VIGS), an oxylipin signaling inducer, methyl jasmonate (MeJA), and a chemical inhibitor of oxylipin signaling, phenidone. Surprisingly, there was no impact of phenidone treatment on jasmonic acid or salicylic acid levels in virus-infected plants, though aphid attraction and retention were altered. These results suggest that the observed impacts of phenidone on aphid attraction to and retention on PEMV-infected plants are independent of the jasmonic acid and salicylic acid pathway but may be mediated by another component of the oxylipin signaling pathway. These results shed light on the complexity of viral manipulation of phytohormone signaling and vector-plant interactions.

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Acknowledgements

We thank Dr. Ida Elisabeth Johansen and Dr. Alan Miller for providing constructs, and Leilani Jones and the many undergraduates that helped maintain plants and insects. This work was supported by USDA-NIFA award 2017-67013-26537.

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Authors and Affiliations

  1. School of Integrative Plant Science, Plant-Microbe Biology and Plant Pathology Section, Cornell University, Ithaca, NY, 14853, USA

    S. Bera & C. L. Casteel

  2. Department of Plant Pathology, University of California Davis, Davis, CA, 95616, USA

    R. Blundell & D. Liang

  3. Department of Entomology, Washington State University, Pullman, WA, 99164, USA

    D. W. Crowder

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  1. S. Bera
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  2. R. Blundell
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  3. D. Liang
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  5. C. L. Casteel
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Correspondence to C. L. Casteel.

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ESM 1

Supplemental Fig. 1 There was a decrease in relative transcript abundance of Coi1 in silenced plants using VIGS. **denotes P < 0.01, significant difference by t-test. Supplemental Fig. 2 Ten virus-free aphids were kept on phenidone-treated or untreated healthy plants, with access to an untreated healthy plant in the same pot for 24 h. Phenidone treatment on healthy plants had no effect on aphid migration off the healthy plant. Mean ± SE of N = 8. Supplemental Fig. 3 Jasmonic acid levels in Pisum sativum plants after induction with methyl jasmonate (MeJA) or MeJA and phenidone. Phenidone reduced MeJA induction of jasmonic acid. **denotes P < 0.01, significant difference by LSD test. Mean ± SE of N = 19. (PDF 195 kb) (PDF 195 kb)

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Bera, S., Blundell, R., Liang, D. et al. The Oxylipin Signaling Pathway Is Required for Increased Aphid Attraction and Retention on Virus-Infected Plants. J Chem Ecol 46, 771–781 (2020). https://doi.org/10.1007/s10886-020-01157-7

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