Cargando…

Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea

Plants respond to herbivore attack by rapidly inducing defenses that are mainly regulated by jasmonic acid (JA). Due to the systemic nature of induced defenses, attack by root herbivores can also result in a shoot response and vice versa, causing interactions between above- and belowground herbivore...

Descripción completa

Detalles Bibliográficos
Autores principales: Tytgat, Tom O.G., Verhoeven, Koen J. F., Jansen, Jeroen J., Raaijmakers, Ciska E., Bakx-Schotman, Tanja, McIntyre, Lauren M., van der Putten, Wim H., Biere, Arjen, van Dam, Nicole M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3679124/
https://www.ncbi.nlm.nih.gov/pubmed/23776489
http://dx.doi.org/10.1371/journal.pone.0065502
_version_ 1782272957869981696
author Tytgat, Tom O.G.
Verhoeven, Koen J. F.
Jansen, Jeroen J.
Raaijmakers, Ciska E.
Bakx-Schotman, Tanja
McIntyre, Lauren M.
van der Putten, Wim H.
Biere, Arjen
van Dam, Nicole M.
author_facet Tytgat, Tom O.G.
Verhoeven, Koen J. F.
Jansen, Jeroen J.
Raaijmakers, Ciska E.
Bakx-Schotman, Tanja
McIntyre, Lauren M.
van der Putten, Wim H.
Biere, Arjen
van Dam, Nicole M.
author_sort Tytgat, Tom O.G.
collection PubMed
description Plants respond to herbivore attack by rapidly inducing defenses that are mainly regulated by jasmonic acid (JA). Due to the systemic nature of induced defenses, attack by root herbivores can also result in a shoot response and vice versa, causing interactions between above- and belowground herbivores. However, little is known about the molecular mechanisms underlying these interactions. We investigated whether plants respond differently when roots or shoots are induced. We mimicked herbivore attack by applying JA to the roots or shoots of Brassica oleracea and analyzed molecular and chemical responses in both organs. In shoots, an immediate and massive change in primary and secondary metabolism was observed. In roots, the JA-induced response was less extensive and qualitatively different from that in the shoots. Strikingly, in both roots and shoots we also observed differential responses in primary metabolism, development as well as defense specific traits depending on whether the JA induction had been below- or aboveground. We conclude that the JA response is not only tissue-specific but also dependent on the organ that was induced. Already very early in the JA signaling pathway the differential response was observed. This indicates that both organs have a different JA signaling cascade, and that the signal eliciting systemic responses contains information about the site of induction, thus providing plants with a mechanism to tailor their responses specifically to the organ that is damaged.
format Online
Article
Text
id pubmed-3679124
institution National Center for Biotechnology Information
language English
publishDate 2013
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-36791242013-06-17 Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea Tytgat, Tom O.G. Verhoeven, Koen J. F. Jansen, Jeroen J. Raaijmakers, Ciska E. Bakx-Schotman, Tanja McIntyre, Lauren M. van der Putten, Wim H. Biere, Arjen van Dam, Nicole M. PLoS One Research Article Plants respond to herbivore attack by rapidly inducing defenses that are mainly regulated by jasmonic acid (JA). Due to the systemic nature of induced defenses, attack by root herbivores can also result in a shoot response and vice versa, causing interactions between above- and belowground herbivores. However, little is known about the molecular mechanisms underlying these interactions. We investigated whether plants respond differently when roots or shoots are induced. We mimicked herbivore attack by applying JA to the roots or shoots of Brassica oleracea and analyzed molecular and chemical responses in both organs. In shoots, an immediate and massive change in primary and secondary metabolism was observed. In roots, the JA-induced response was less extensive and qualitatively different from that in the shoots. Strikingly, in both roots and shoots we also observed differential responses in primary metabolism, development as well as defense specific traits depending on whether the JA induction had been below- or aboveground. We conclude that the JA response is not only tissue-specific but also dependent on the organ that was induced. Already very early in the JA signaling pathway the differential response was observed. This indicates that both organs have a different JA signaling cascade, and that the signal eliciting systemic responses contains information about the site of induction, thus providing plants with a mechanism to tailor their responses specifically to the organ that is damaged. Public Library of Science 2013-06-11 /pmc/articles/PMC3679124/ /pubmed/23776489 http://dx.doi.org/10.1371/journal.pone.0065502 Text en © 2013 Tytgat et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Tytgat, Tom O.G.
Verhoeven, Koen J. F.
Jansen, Jeroen J.
Raaijmakers, Ciska E.
Bakx-Schotman, Tanja
McIntyre, Lauren M.
van der Putten, Wim H.
Biere, Arjen
van Dam, Nicole M.
Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea
title Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea
title_full Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea
title_fullStr Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea
title_full_unstemmed Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea
title_short Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea
title_sort plants know where it hurts: root and shoot jasmonic acid induction elicit differential responses in brassica oleracea
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3679124/
https://www.ncbi.nlm.nih.gov/pubmed/23776489
http://dx.doi.org/10.1371/journal.pone.0065502
work_keys_str_mv AT tytgattomog plantsknowwhereithurtsrootandshootjasmonicacidinductionelicitdifferentialresponsesinbrassicaoleracea
AT verhoevenkoenjf plantsknowwhereithurtsrootandshootjasmonicacidinductionelicitdifferentialresponsesinbrassicaoleracea
AT jansenjeroenj plantsknowwhereithurtsrootandshootjasmonicacidinductionelicitdifferentialresponsesinbrassicaoleracea
AT raaijmakersciskae plantsknowwhereithurtsrootandshootjasmonicacidinductionelicitdifferentialresponsesinbrassicaoleracea
AT bakxschotmantanja plantsknowwhereithurtsrootandshootjasmonicacidinductionelicitdifferentialresponsesinbrassicaoleracea
AT mcintyrelaurenm plantsknowwhereithurtsrootandshootjasmonicacidinductionelicitdifferentialresponsesinbrassicaoleracea
AT vanderputtenwimh plantsknowwhereithurtsrootandshootjasmonicacidinductionelicitdifferentialresponsesinbrassicaoleracea
AT bierearjen plantsknowwhereithurtsrootandshootjasmonicacidinductionelicitdifferentialresponsesinbrassicaoleracea
AT vandamnicolem plantsknowwhereithurtsrootandshootjasmonicacidinductionelicitdifferentialresponsesinbrassicaoleracea