The Oxylipin Signaling Pathway Is Required for Increased Aphid Attraction and Retention on Virus-Infected Plants S. Bera 1 & R. Blundell 2 & D. Liang 2 & D. W. Crowder 3 & C. L. Casteel 1 Received: 12 November 2019 /Revised: 19 January 2020 /Accepted: 27 January 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020 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. Keywords Luteovirus . Enamovirus . Lipoxygenase . Hyperoxide lyase . Hormone . Cross-talk . Phytobiome Introduction In a rapidly changing environment viruses are considered su- perior pathogens due to their high rates of mutation and ca- pacity to evolve quickly (Fraile and García-Arenal 2018). This superiority is evident in the fact that most emerging infectious diseases are caused by viruses (Anderson et al. 2004). Over time and due to their ability to quickly evolve, viruses have developed myriad ways to change host physiology and ensure their own survival. This is evident when comparing changes in plant transcripts and metabolites in response to an evolved virus and an unevolved virus, where there are differential ef- fects on stress-related transcripts, plant metabolism, growth, and development (Agudelo-Romero et al. 2008; Hillung et al. 2016; Cervera et al. 2018). Virus-induced changes in host physiology can also affect interactions with other organisms (Mauck et al. 2018). For example, more than 55% of all known plant viruses are dependent on aphid vectors for trans- mission (Hogenhout et al. 2008) and plant viruses are known to induce specific changes in plants which attract more aphids to infected plants in comparison to healthy plants (Eigenbrode et al. 2018). Some of the strategies exploited by viruses to increase vector attraction are to increase the plant’ s nutrient content (Casteel et al. 2014; Blanc and Michalakis 2016), to suppress the defense signaling pathway that target the vectors (Casteel et al. 2015; Wu et al. 2017), or to induce a blend of volatiles to attract more vectors (Claudel et al. 2018; Mwando et al. 2018; Safari et al. 2019). These changes in host physiol- ogy can make the infected plant more attractive to vectors and in some cases increase insect performance and the number of vectors in the environment. Increased rates of vector contact and increased vector populations should lead to more transmis- sion of the virus and increased survival (Sisterson 2008). Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10886-020-01157-7) contains supplementary material, which is available to authorized users. * C. L. Casteel ccasteel@cornell.edu 1 School of Integrative Plant Science, Plant-Microbe Biology and Plant Pathology Section, Cornell University, Ithaca, NY 14853, USA 2 Department of Plant Pathology, University of California Davis, Davis, CA 95616, USA 3 Department of Entomology, Washington State University, Pullman, WA 99164, USA Journal of Chemical Ecology https://doi.org/10.1007/s10886-020-01157-7