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
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2009
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/56c6d6bfe31741249327ae218aed9995
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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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An ecological analysis of the herbivory-elicited JA burst and its metabolism: plant memory processes and predictions of the moving target model.

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