An ecological analysis of the herbivory-elicited JA burst and its metabolism: plant memory processes and predictions of the moving target model.

<h4>Background</h4>Rapid herbivore-induced jasmonic acid (JA) accumulation is known to mediate many induced defense responses in vascular plants, but little is known about how JA bursts are metabolized and modified in response to repeated elicitations, are propagated throughout elicited...

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Autores principales: William Stork, Celia Diezel, Rayko Halitschke, Ivan Gális, Ian T Baldwin
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Publicado: Public Library of Science (PLoS) 2009
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spelling oai:doaj.org-article:56c6d6bfe31741249327ae218aed99952021-11-25T06:16:47ZAn ecological analysis of the herbivory-elicited JA burst and its metabolism: plant memory processes and predictions of the moving target model.1932-620310.1371/journal.pone.0004697https://doaj.org/article/56c6d6bfe31741249327ae218aed99952009-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/19277115/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Rapid herbivore-induced jasmonic acid (JA) accumulation is known to mediate many induced defense responses in vascular plants, but little is known about how JA bursts are metabolized and modified in response to repeated elicitations, are propagated throughout elicited leaves, or how they directly influence herbivores.<h4>Methodology/principal findings</h4>We found the JA burst in a native population of Nicotiana attenuata to be highly robust despite environmental variation and we examined the JA bursts produced by repeated elicitations with Manduca sexta oral secretions (OS) at whole- and within-leaf spatial scales. Surprisingly, a 2(nd) OS-elicitation suppressed an expected JA burst at both spatial scales, but subsequent elicitations caused more rapid JA accumulation in elicited tissue. The baseline of induced JA/JA-Ile increased with number of elicitations in discrete intervals. Large veins constrained the spatial spread of JA bursts, leading to heterogeneity within elicited leaves. 1(st)-instar M. sexta larvae were repelled by elicitations and changed feeding sites. JA conjugated with isoleucine (JA-Ile) translates elicitations into defense production (e.g., TPIs), but conjugation efficiency varied among sectors and depended on NaWRKY3/6 transcription factors. Elicited TPI activity correlated strongly with the heterogeneity of JA/JA-Ile accumulations after a single elicitation, but not repeated elicitations.<h4>Conclusions/significance</h4>Ecologically informed scaling of leaf elicitation reveals the contribution of repeated herbivory events to the formation of plant memory of herbivory and the causes and importance of heterogeneity in induced defense responses. Leaf vasculature, in addition to transmitting long-distance damage cues, creates heterogeneity in JA bursts within attacked leaves that may be difficult for an attacking herbivore to predict. Such unpredictability is a central tenet of the Moving Target Model of defense, which posits that variability in itself is defensive.William StorkCelia DiezelRayko HalitschkeIvan GálisIan T BaldwinPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 4, Iss 3, p e4697 (2009)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
William Stork
Celia Diezel
Rayko Halitschke
Ivan Gális
Ian T Baldwin
An ecological analysis of the herbivory-elicited JA burst and its metabolism: plant memory processes and predictions of the moving target model.
description <h4>Background</h4>Rapid herbivore-induced jasmonic acid (JA) accumulation is known to mediate many induced defense responses in vascular plants, but little is known about how JA bursts are metabolized and modified in response to repeated elicitations, are propagated throughout elicited leaves, or how they directly influence herbivores.<h4>Methodology/principal findings</h4>We found the JA burst in a native population of Nicotiana attenuata to be highly robust despite environmental variation and we examined the JA bursts produced by repeated elicitations with Manduca sexta oral secretions (OS) at whole- and within-leaf spatial scales. Surprisingly, a 2(nd) OS-elicitation suppressed an expected JA burst at both spatial scales, but subsequent elicitations caused more rapid JA accumulation in elicited tissue. The baseline of induced JA/JA-Ile increased with number of elicitations in discrete intervals. Large veins constrained the spatial spread of JA bursts, leading to heterogeneity within elicited leaves. 1(st)-instar M. sexta larvae were repelled by elicitations and changed feeding sites. JA conjugated with isoleucine (JA-Ile) translates elicitations into defense production (e.g., TPIs), but conjugation efficiency varied among sectors and depended on NaWRKY3/6 transcription factors. Elicited TPI activity correlated strongly with the heterogeneity of JA/JA-Ile accumulations after a single elicitation, but not repeated elicitations.<h4>Conclusions/significance</h4>Ecologically informed scaling of leaf elicitation reveals the contribution of repeated herbivory events to the formation of plant memory of herbivory and the causes and importance of heterogeneity in induced defense responses. Leaf vasculature, in addition to transmitting long-distance damage cues, creates heterogeneity in JA bursts within attacked leaves that may be difficult for an attacking herbivore to predict. Such unpredictability is a central tenet of the Moving Target Model of defense, which posits that variability in itself is defensive.
format article
author William Stork
Celia Diezel
Rayko Halitschke
Ivan Gális
Ian T Baldwin
author_facet William Stork
Celia Diezel
Rayko Halitschke
Ivan Gális
Ian T Baldwin
author_sort William Stork
title An ecological analysis of the herbivory-elicited JA burst and its metabolism: plant memory processes and predictions of the moving target model.
title_short An ecological analysis of the herbivory-elicited JA burst and its metabolism: plant memory processes and predictions of the moving target model.
title_full An ecological analysis of the herbivory-elicited JA burst and its metabolism: plant memory processes and predictions of the moving target model.
title_fullStr An ecological analysis of the herbivory-elicited JA burst and its metabolism: plant memory processes and predictions of the moving target model.
title_full_unstemmed An ecological analysis of the herbivory-elicited JA burst and its metabolism: plant memory processes and predictions of the moving target model.
title_sort ecological analysis of the herbivory-elicited ja burst and its metabolism: plant memory processes and predictions of the moving target model.
publisher Public Library of Science (PLoS)
publishDate 2009
url https://doaj.org/article/56c6d6bfe31741249327ae218aed9995
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