Caterpillar Chewing Vibrations Cause Changes in Plant Hormones and Volatile Emissions in Arabidopsis thaliana

Front Plant Sci. 2019 Jun 26:10:810. doi: 10.3389/fpls.2019.00810. eCollection 2019.

Abstract

Plant perception of insect feeding involves integration of the multiple signals involved: wounding, oral secretions, and substrate borne feeding vibrations. Although plant responses to wounding and oral secretions have been studied, little is known about how signals from the rapidly transmitted vibrations caused by chewing insect feeding are integrated to produce effects on plant defenses. In this study, we examined whether 24 h of insect feeding vibrations caused changes in levels of phytohormones and volatile organic compounds (VOCs) produced by leaves of Arabidopsis thaliana when they were subjected to just feeding vibrations or feeding vibrations and wounding + methyl jasmonate (MeJA), compared to their respective controls of silent sham or wounding + MeJA. We showed that feeding vibrations alone caused a decrease in the concentrations of most phytohormones, compared to those found in control plants receiving no vibrations. When feeding vibrations were combined with wounding and application of MeJA, the results were more complex. For hormones whose levels were induced by wounding and MeJA (jasmonic acid, indole-3-butyric acid), the addition of feeding vibrations caused an even larger response. If the level of hormone was unchanged by wounding and MeJA compared with controls, then the addition of feeding vibrations had little effect. The levels of some VOCs were influenced by the treatments. Feeding vibrations alone caused an increase in β-ionone and decrease in methyl salicylate, and wounding + MeJA alone caused a decrease in benzaldehyde and methyl salicylate. When feeding vibrations were combined with wounding + MeJA, the effects on β-ionone and methyl salicylate were similar to those seen with feeding vibrations alone, and levels of benzaldehyde remained low as seen with wounding + MeJA alone. The widespread downregulation of plant hormones observed in this study is also seen in plant responses to cold, suggesting that membrane fluidity changes and/or downstream signaling may be common to both phenomena.

Keywords: feeding vibrations; herbivory; phytohormones; plant defense; volatile organic compounds.