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Journal of Chemical Ecology

, Volume 45, Issue 5–6, pp 515–524 | Cite as

Pathogen-Mediated Tritrophic Interactions: Baculovirus-Challenged Caterpillars Induce Higher Plant Defenses than Healthy Caterpillars

  • Qinjian PanEmail author
  • Ikkei Shikano
  • Kelli Hoover
  • Tong-Xian LiuEmail author
  • Gary W. Felton
Article

Abstract

Although the tritrophic interactions of plants, insect herbivores and their natural enemies have been intensely studied for several decades, the roles of entomopathogens in their indirect modulation of plant-insect relationships is still unclear. Here, we employed a sublethal dose of a baculovirus with a relatively broad host range (AcMNPV) to explore if feeding by baculovirus-challenged Helicoverpa zea caterpillars induces direct defenses in the tomato plant. We examined induction of plant defenses following feeding by H. zea, including tomato plants fed on by healthy caterpillars, AcMNPV-challenged caterpillars, or undamaged controls, and subsequently compared the transcript levels of defense related proteins (i.e., trypsin proteinase inhibitors, peroxidase and polyphenol oxidase) and other defense genes (i.e., proteinase inhibitor II and cysteine proteinase inhibitor) from these plants, in addition to comparing caterpillar relative growth rates. As a result, AcMNPV-challenged caterpillars induced the highest plant anti-herbivore defenses. We examined several elicitors and effectors in the secretions of these caterpillars (i.e., glucose oxidase, phospholipase C, and ATPase hydrolysis), which surprisingly did not differ between treatments. Hence, we suggest that the greater induction of plant defenses by the virus-challenged caterpillars may be due to differences in the amount of these secretions deposited during feeding or to some other unknown factor(s).

Keywords

Plant defense Induce defense Immune responses Saliva Oral secretions Ventral eversible gland Herbivore perception 

Notes

Acknowledgments

This research was financially supported by the U.S. National Science Foundation (IOS-1645548) awarded to GWF, IS, and KH. QJP acknowledges financial support from China Scholarship Council (Grant 201506300111). IS acknowledges financial support from Natural Sciences and Engineering Research Council of Canada Postdoctoral Fellowship (NSERC PDF-488105-2016). The financial support from Northwest A&F University’ Special Talent Fund to TXL is greatly appreciated. We appreciate all technical assistance and suggestions from M. Peiffer and F. McCullough. We thank Dr. D. Luthe (Department of Plant Science, Pennsylvania State University) for sharing her laboratory equipment.

Supplementary material

10886_2019_1077_Fig9_ESM.png (13 kb)
Fig. S1

Dose response of virus (AcMNPV)-challenged fifth instar Trichoplusia ni and fourth instar Helicoverpa zea caterpillars. (PNG 12 kb)

10886_2019_1077_MOESM1_ESM.eps (730 kb)
High resolution image (EPS 729 kb)
10886_2019_1077_MOESM2_ESM.docx (13 kb)
Table S1 Tomato primers used for RT-PCR in this study. (DOCX 13 kb)

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Crop Stress Biology for Arid Areas, and Key Laboratory of Integrated Pest Management on the Loess Plateau of Ministry of AgricultureNorthwest A&F UniversityYanglingChina
  2. 2.Department of Entomology and Center for Chemical EcologyPennsylvania State UniversityUniversity ParkUSA

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