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

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 vibr...

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Main Authors: Mélanie J. A. Body, William C. Neer, Caitlin Vore, Chung-Ho Lin, Danh C. Vu, Jack C. Schultz, Reginald B. Cocroft, Heidi M. Appel
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.00810/full
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spelling doaj-7ecb13cddbaf4d62a8dd8e9a4a9cff942020-11-24T21:24:24ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-06-011010.3389/fpls.2019.00810454219Caterpillar Chewing Vibrations Cause Changes in Plant Hormones and Volatile Emissions in Arabidopsis thalianaMélanie J. A. Body0Mélanie J. A. Body1William C. Neer2Caitlin Vore3Caitlin Vore4Chung-Ho Lin5Danh C. Vu6Jack C. Schultz7Jack C. Schultz8Reginald B. Cocroft9Heidi M. Appel10Heidi M. Appel11Division of Plant Sciences, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, United StatesDepartment of Environmental Sciences, The University of Toledo, Toledo, OH, United StatesDivision of Plant Sciences, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, United StatesDivision of Plant Sciences, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, United StatesCornell Cooperative Extension Erie County, East Aurora, NY, United StatesSchool of Natural Resources, University of Missouri, Columbia, MO, United StatesSchool of Natural Resources, University of Missouri, Columbia, MO, United StatesDivision of Plant Sciences, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, United StatesDepartment of Environmental Sciences, The University of Toledo, Toledo, OH, United StatesDivision of Biological Sciences, University of Missouri, Columbia, MO, United StatesDivision of Plant Sciences, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, United StatesDepartment of Environmental Sciences, The University of Toledo, Toledo, OH, United StatesPlant 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.https://www.frontiersin.org/article/10.3389/fpls.2019.00810/fullplant defenseherbivoryfeeding vibrationsvolatile organic compoundsphytohormones
collection DOAJ
language English
format Article
sources DOAJ
author Mélanie J. A. Body
Mélanie J. A. Body
William C. Neer
Caitlin Vore
Caitlin Vore
Chung-Ho Lin
Danh C. Vu
Jack C. Schultz
Jack C. Schultz
Reginald B. Cocroft
Heidi M. Appel
Heidi M. Appel
spellingShingle Mélanie J. A. Body
Mélanie J. A. Body
William C. Neer
Caitlin Vore
Caitlin Vore
Chung-Ho Lin
Danh C. Vu
Jack C. Schultz
Jack C. Schultz
Reginald B. Cocroft
Heidi M. Appel
Heidi M. Appel
Caterpillar Chewing Vibrations Cause Changes in Plant Hormones and Volatile Emissions in Arabidopsis thaliana
Frontiers in Plant Science
plant defense
herbivory
feeding vibrations
volatile organic compounds
phytohormones
author_facet Mélanie J. A. Body
Mélanie J. A. Body
William C. Neer
Caitlin Vore
Caitlin Vore
Chung-Ho Lin
Danh C. Vu
Jack C. Schultz
Jack C. Schultz
Reginald B. Cocroft
Heidi M. Appel
Heidi M. Appel
author_sort Mélanie J. A. Body
title Caterpillar Chewing Vibrations Cause Changes in Plant Hormones and Volatile Emissions in Arabidopsis thaliana
title_short Caterpillar Chewing Vibrations Cause Changes in Plant Hormones and Volatile Emissions in Arabidopsis thaliana
title_full Caterpillar Chewing Vibrations Cause Changes in Plant Hormones and Volatile Emissions in Arabidopsis thaliana
title_fullStr Caterpillar Chewing Vibrations Cause Changes in Plant Hormones and Volatile Emissions in Arabidopsis thaliana
title_full_unstemmed Caterpillar Chewing Vibrations Cause Changes in Plant Hormones and Volatile Emissions in Arabidopsis thaliana
title_sort caterpillar chewing vibrations cause changes in plant hormones and volatile emissions in arabidopsis thaliana
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2019-06-01
description 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.
topic plant defense
herbivory
feeding vibrations
volatile organic compounds
phytohormones
url https://www.frontiersin.org/article/10.3389/fpls.2019.00810/full
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