Phytohormones in Fall Armyworm Saliva Modulate Defense Responses in Plants

Abstract

Insect herbivory induces plant defense responses that are often modulated by components in insect saliva, oral secretions or regurgitant, frass, or oviposition fluids. These secretions contain proteins and small molecules that act as elicitors or effectors of plant defenses. Several non-protein elicitors have been identified from insect oral secretions, whereas studies of insect saliva have focused mainly on protein identification. Yet, insect saliva may also contain non-protein molecules that could activate defense responses in plants. The goal of this study was to identify non-protein plant defense elicitors present in insect saliva. We used the fall armyworm (FAW), Spodoptera frugiperda and its host plants tomato, maize, and rice as a model system. We tested the effect of protein-digested saliva or non-protein components on herbivore-induced defense responses in maize, rice and tomato. We identified phytohormones in FAW saliva using high performance liquid chromatography coupled with mass spectrometry. The results of this study show that non-protein components in FAW saliva modulated defense responses in different plant species. The saliva of this insect contains benzoic acid, and the phytohormones jasmonic acid, salicylic acid, and abscisic acid at concentrations of <5 ng per μl of saliva. Plant treatment with similar phytohormone quantities detected in FAW saliva upregulated the expression of a maize proteinase inhibitor gene in maize, and down-regulated late herbivore-induced defenses in tomato plants. We conclude that FAW saliva is a complex fluid that, in addition to known enzymatic plant defense elicitors, contains phytohormones and other small molecules.

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Acknowledgements

We thank Dr. Robert Meagher from the USDA-ARS in Gainesville, FL for providing eggs of FAW caterpillars from genotyped corn and rice strains. We also thank Dr. Dawn Luthe for graciously lending the qPCR machine, plant tissue grinder, and other lab equipment to us. We also thank Mr. Scott DiLoreto for glasshouse management. Special thanks to Dr. W. P. Williams for supplying the B73 maize seeds, and to the United States Department of Agriculture –Agricultural Research Service Dale Bumpers National Rice Research Center in Arkansas for supplying seeds of the rice cultivar Nipponbare. We greatly appreciate support provided by United States Department of Agriculture (AFRI 2017-67013-26596); National Science Foundation (IOS-1645548); Hatch Project Grant PEN04576; Pennsylvania State University (2013-CAS Graduate Student Award), and the Entomological Society of America (2014-Monsanto Research Grant).

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Correspondence to Flor Edith Acevedo or Gary W. Felton.

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Fig. S1
figure8

Peroxidase (POX) activity in tomato plants treated with either a mixture of phytohormones or water plus methanol at different time points. Bar values are untransformed means ± SEM; different letters indicate significant differences obtained with ANOVA following Tukey tests at α = 0.05 [24 h (F2,21 = 41.8, P < 0.001), 48 h (F2,22 = 73.46, P < 0.001), 72 h (F2,22 = 50.79, P < 0.001), 96 h (F2,27 = 38.16, P < 0.001, log transformed data), n = 10]. Controls are undamaged plants (PNG 106 kb)

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Acevedo, F.E., Smith, P., Peiffer, M. et al. Phytohormones in Fall Armyworm Saliva Modulate Defense Responses in Plants. J Chem Ecol 45, 598–609 (2019). https://doi.org/10.1007/s10886-019-01079-z

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Keywords

  • Oral secretions
  • Insect saliva
  • Phytohormones
  • Plant defenses
  • Induced defenses
  • Salicylic acid
  • Jasmonic acid
  • Benzoic acid
  • Abscisic acid