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

T. Tytgat, K.J.F. Verhoeven, J.J. Janssen, C.E. Raaijmakers, J.M.T. Bakx-Schotman, L.M. McIntyre, W.H. van der Putten, A. Biere, N.M. van Dam

Research output: Contribution to journalArticleAcademicpeer-review

46 Citations (Scopus)

Abstract

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.
Original languageEnglish
Article numbere65502
JournalPLoS ONE
Volume8
Issue number6
DOIs
Publication statusPublished - 2013

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Brassica
jasmonic acid
Brassica oleracea
Herbivory
shoots
herbivores
Secondary Metabolism
metabolism
Metabolism
Tissue

Keywords

  • gene-expression
  • arabidopsis-thaliana
  • jaz repressors
  • multitrophic interactions
  • 12-oxo-phytodienoic acid
  • stress responses
  • herbivory
  • dynamics
  • defenses
  • carbon

Cite this

Tytgat, T., Verhoeven, K. J. F., Janssen, J. J., Raaijmakers, C. E., Bakx-Schotman, J. M. T., McIntyre, L. M., ... van Dam, N. M. (2013). Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea. PLoS ONE, 8(6), [e65502]. https://doi.org/10.1371/journal.pone.0065502
Tytgat, T. ; Verhoeven, K.J.F. ; Janssen, J.J. ; Raaijmakers, C.E. ; Bakx-Schotman, J.M.T. ; McIntyre, L.M. ; van der Putten, W.H. ; Biere, A. ; van Dam, N.M. / Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea. In: PLoS ONE. 2013 ; Vol. 8, No. 6.
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title = "Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea.",
abstract = "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.",
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author = "T. Tytgat and K.J.F. Verhoeven and J.J. Janssen and C.E. Raaijmakers and J.M.T. Bakx-Schotman and L.M. McIntyre and {van der Putten}, W.H. and A. Biere and {van Dam}, N.M.",
year = "2013",
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Tytgat, T, Verhoeven, KJF, Janssen, JJ, Raaijmakers, CE, Bakx-Schotman, JMT, McIntyre, LM, van der Putten, WH, Biere, A & van Dam, NM 2013, 'Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea.', PLoS ONE, vol. 8, no. 6, e65502. https://doi.org/10.1371/journal.pone.0065502

Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea. / Tytgat, T.; Verhoeven, K.J.F.; Janssen, J.J.; Raaijmakers, C.E.; Bakx-Schotman, J.M.T.; McIntyre, L.M.; van der Putten, W.H.; Biere, A.; van Dam, N.M.

In: PLoS ONE, Vol. 8, No. 6, e65502, 2013.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea.

AU - Tytgat, T.

AU - Verhoeven, K.J.F.

AU - Janssen, J.J.

AU - Raaijmakers, C.E.

AU - Bakx-Schotman, J.M.T.

AU - McIntyre, L.M.

AU - van der Putten, W.H.

AU - Biere, A.

AU - van Dam, N.M.

PY - 2013

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KW - gene-expression

KW - arabidopsis-thaliana

KW - jaz repressors

KW - multitrophic interactions

KW - 12-oxo-phytodienoic acid

KW - stress responses

KW - herbivory

KW - dynamics

KW - defenses

KW - carbon

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