Root JA Induction Modifies Glucosinolate Profiles and Increases Subsequent Aboveground Resistance to Herbivore Attack in Cardamine hirsuta

Alteration and induction of plant secondary metabolites after herbivore attack have been shown in almost all the studied plant species. Induction can be at the local site of damage, or systemic, such as from roots to shoots. In addition to immediate induction, previous herbivore bouts have been show...

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Main Authors: Moe Bakhtiari, Gaétan Glauser, Sergio Rasmann
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2018.01230/full
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author Moe Bakhtiari
Gaétan Glauser
Sergio Rasmann
author_facet Moe Bakhtiari
Gaétan Glauser
Sergio Rasmann
author_sort Moe Bakhtiari
collection DOAJ
description Alteration and induction of plant secondary metabolites after herbivore attack have been shown in almost all the studied plant species. Induction can be at the local site of damage, or systemic, such as from roots to shoots. In addition to immediate induction, previous herbivore bouts have been shown to “prime” the plants for a stronger and faster response only after a subsequent attack happens. Whereas several studies revealed a link between root herbivory and increased resistance against aboveground (AG) herbivory, the evidence of root defense priming against subsequent AG herbivory is currently lacking. To address this gap, we induced Cardamine hirsuta roots by applying jasmonic acid (JA), and, after a time lag, we subjected both control and JA-treated plants to AG herbivory by the generalist herbivore Spodoptera littoralis. We addressed the effect of root JA addition on AG herbivore resistance by measuring larval weight gain and tested the effect of root induction on abundance and composition of glucosinolates (GSLs) in shoots, prior, and after subsequent herbivory. We observed a strong positive effect of root induction on the resistance against AG herbivory. The overall abundance and identity of GSLs was globally affected by JA induction and by herbivore feeding, independently, and we found a significant correlation between larval growth and the shoot GSL profiles only after AG herbivory, 11 days after induction in roots. Contrary to expectations of priming, we observed that JA induction in roots altered the GSLs profile in the leaves that was maintained through time. This initial modification was sufficient to maintain a lower caterpillar weight gain, even 11 days post-root induction. Altogether, we show that prior root defense induction increases AG insect resistance by modifying and maintaining variation in GSL profiles during insect feeding.
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spelling doaj.art-81ea98151597424a8b1c41584ab5816e2022-12-21T23:50:01ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-08-01910.3389/fpls.2018.01230356846Root JA Induction Modifies Glucosinolate Profiles and Increases Subsequent Aboveground Resistance to Herbivore Attack in Cardamine hirsutaMoe Bakhtiari0Gaétan Glauser1Sergio Rasmann2Laboratory of Functional Ecology, Institute of Biology, University of Neuchâtel, Neuchâtel, SwitzerlandNeuchâtel Platform of Analytical Chemistry, Neuchâtel, SwitzerlandLaboratory of Functional Ecology, Institute of Biology, University of Neuchâtel, Neuchâtel, SwitzerlandAlteration and induction of plant secondary metabolites after herbivore attack have been shown in almost all the studied plant species. Induction can be at the local site of damage, or systemic, such as from roots to shoots. In addition to immediate induction, previous herbivore bouts have been shown to “prime” the plants for a stronger and faster response only after a subsequent attack happens. Whereas several studies revealed a link between root herbivory and increased resistance against aboveground (AG) herbivory, the evidence of root defense priming against subsequent AG herbivory is currently lacking. To address this gap, we induced Cardamine hirsuta roots by applying jasmonic acid (JA), and, after a time lag, we subjected both control and JA-treated plants to AG herbivory by the generalist herbivore Spodoptera littoralis. We addressed the effect of root JA addition on AG herbivore resistance by measuring larval weight gain and tested the effect of root induction on abundance and composition of glucosinolates (GSLs) in shoots, prior, and after subsequent herbivory. We observed a strong positive effect of root induction on the resistance against AG herbivory. The overall abundance and identity of GSLs was globally affected by JA induction and by herbivore feeding, independently, and we found a significant correlation between larval growth and the shoot GSL profiles only after AG herbivory, 11 days after induction in roots. Contrary to expectations of priming, we observed that JA induction in roots altered the GSLs profile in the leaves that was maintained through time. This initial modification was sufficient to maintain a lower caterpillar weight gain, even 11 days post-root induction. Altogether, we show that prior root defense induction increases AG insect resistance by modifying and maintaining variation in GSL profiles during insect feeding.https://www.frontiersin.org/article/10.3389/fpls.2018.01230/fullbelowground-aboveground primingglucosinolatesinsect resistanceplant-mediated above-belowground interactionplant chemical defensesphytohormones
spellingShingle Moe Bakhtiari
Gaétan Glauser
Sergio Rasmann
Root JA Induction Modifies Glucosinolate Profiles and Increases Subsequent Aboveground Resistance to Herbivore Attack in Cardamine hirsuta
Frontiers in Plant Science
belowground-aboveground priming
glucosinolates
insect resistance
plant-mediated above-belowground interaction
plant chemical defenses
phytohormones
title Root JA Induction Modifies Glucosinolate Profiles and Increases Subsequent Aboveground Resistance to Herbivore Attack in Cardamine hirsuta
title_full Root JA Induction Modifies Glucosinolate Profiles and Increases Subsequent Aboveground Resistance to Herbivore Attack in Cardamine hirsuta
title_fullStr Root JA Induction Modifies Glucosinolate Profiles and Increases Subsequent Aboveground Resistance to Herbivore Attack in Cardamine hirsuta
title_full_unstemmed Root JA Induction Modifies Glucosinolate Profiles and Increases Subsequent Aboveground Resistance to Herbivore Attack in Cardamine hirsuta
title_short Root JA Induction Modifies Glucosinolate Profiles and Increases Subsequent Aboveground Resistance to Herbivore Attack in Cardamine hirsuta
title_sort root ja induction modifies glucosinolate profiles and increases subsequent aboveground resistance to herbivore attack in cardamine hirsuta
topic belowground-aboveground priming
glucosinolates
insect resistance
plant-mediated above-belowground interaction
plant chemical defenses
phytohormones
url https://www.frontiersin.org/article/10.3389/fpls.2018.01230/full
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AT gaetanglauser rootjainductionmodifiesglucosinolateprofilesandincreasessubsequentabovegroundresistancetoherbivoreattackincardaminehirsuta
AT sergiorasmann rootjainductionmodifiesglucosinolateprofilesandincreasessubsequentabovegroundresistancetoherbivoreattackincardaminehirsuta