Wounding and Insect Feeding Trigger two Independent MAPK Pathways with Distinct Regulation and Kinetics.

Cécile Sözen; Sebastian Timo Schenk; Marie Boudsocq; Camille Chardin; Marilia Almeida-Trapp; Anne Krapp; Heribert Hirt; Axel Mithöfer; Jean Colcombet

doi:10.1105/tpc.19.00917

Wounding and Insect Feeding Trigger two Independent MAPK Pathways with Distinct Regulation and Kinetics.

Cécile Sözen, Sebastian Timo Schenk, Marie Boudsocq, Camille Chardin, Marilia Almeida-Trapp, Anne Krapp, Heribert Hirt, Axel Mithöfer, Jean Colcombet

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71 Scopus citations

Abstract

Abiotic and biotic factors cause plant wounding and trigger complex short- and long-term responses at the local and systemic levels. These responses are under the control of complex signaling pathways, which are still poorly understood. Here, we show that the rapid activation of clade-A Mitogen Activated Protein Kinases (MAPKs) MPK3 and MPK6 by wounding depends on the upstream MAPK Kinases (MAP2Ks) MKK4 and MKK5 but is independent of jasmonic acid (JA) signaling. In addition, this fast module does not control wound-triggered JA accumulation in Arabidopsis, unlike its orthologues in tobacco. We also demonstrate that a second MAPK module, composed of MKK3 and the clade-C MAPKs MPK½/7, is activated by wounding in a MKK4/5-independent manner. We provide evidence that the activation of this MKK3-MPK½/7 module occurs mainly through wound-induced JA production via the transcriptional regulation of upstream clade-III MAP3Ks, particularly MAP3K14. We show that mkk3 mutant plants are more susceptible to herbivory from larvae of the generalist lepidopteran herbivore Spodoptera littoralis, indicating that the MKK3-MPK½/7 module is involved in counteracting insect feeding.

Original language	English (US)
Pages (from-to)	tpc.00917.2019
Journal	The Plant Cell
Volume	32
Issue number	6
DOIs	https://doi.org/10.1105/tpc.19.00917
State	Published - Apr 9 2020

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank the Stress Signaling group for critical discussion of this work. We also thank Shuqun Zhang and Edward Farmer for providing mkk4 mkk5 and coi1-34 seeds. This work has benefited from a French State grant (LabEx Saclay Plant Sciences-SPS, ANR-10-LABX-0040-SPS), managed by the French National Research Agency under an "Investments for the Future"program (ANR-11-IDEX-0003-02). C.S. and C.C. were funded by SPS PhD fellowships. Marilia Almeida-Trapp gratefully acknowledges financial support by a Capes-Humboldt Research Fellowship. This publication has been written with the support of the AgreenSkills+fellowship program which has received funding from the EU’s Seventh Framework Program under grant agreement No. FP7-609398 (AgreenSkills+ contract) to STS

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10.1105/tpc.19.00917

https://repository.kaust.edu.sa/bitstream/10754/662500/1/Wounding%20and.pdf

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@article{0526d036110543ea8a338b80281374ae,

title = "Wounding and Insect Feeding Trigger two Independent MAPK Pathways with Distinct Regulation and Kinetics.",

abstract = "Abiotic and biotic factors cause plant wounding and trigger complex short- and long-term responses at the local and systemic levels. These responses are under the control of complex signaling pathways, which are still poorly understood. Here, we show that the rapid activation of clade-A Mitogen Activated Protein Kinases (MAPKs) MPK3 and MPK6 by wounding depends on the upstream MAPK Kinases (MAP2Ks) MKK4 and MKK5 but is independent of jasmonic acid (JA) signaling. In addition, this fast module does not control wound-triggered JA accumulation in Arabidopsis, unlike its orthologues in tobacco. We also demonstrate that a second MAPK module, composed of MKK3 and the clade-C MAPKs MPK½/7, is activated by wounding in a MKK4/5-independent manner. We provide evidence that the activation of this MKK3-MPK½/7 module occurs mainly through wound-induced JA production via the transcriptional regulation of upstream clade-III MAP3Ks, particularly MAP3K14. We show that mkk3 mutant plants are more susceptible to herbivory from larvae of the generalist lepidopteran herbivore Spodoptera littoralis, indicating that the MKK3-MPK½/7 module is involved in counteracting insect feeding.",

author = "C{\'e}cile S{\"o}zen and Schenk, {Sebastian Timo} and Marie Boudsocq and Camille Chardin and Marilia Almeida-Trapp and Anne Krapp and Heribert Hirt and Axel Mith{\"o}fer and Jean Colcombet",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank the Stress Signaling group for critical discussion of this work. We also thank Shuqun Zhang and Edward Farmer for providing mkk4 mkk5 and coi1-34 seeds. This work has benefited from a French State grant (LabEx Saclay Plant Sciences-SPS, ANR-10-LABX-0040-SPS), managed by the French National Research Agency under an {"}Investments for the Future{"}program (ANR-11-IDEX-0003-02). C.S. and C.C. were funded by SPS PhD fellowships. Marilia Almeida-Trapp gratefully acknowledges financial support by a Capes-Humboldt Research Fellowship. This publication has been written with the support of the AgreenSkills+fellowship program which has received funding from the EU{\textquoteright}s Seventh Framework Program under grant agreement No. FP7-609398 (AgreenSkills+ contract) to STS",

year = "2020",

month = apr,

day = "9",

doi = "10.1105/tpc.19.00917",

language = "English (US)",

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T1 - Wounding and Insect Feeding Trigger two Independent MAPK Pathways with Distinct Regulation and Kinetics.

AU - Sözen, Cécile

AU - Schenk, Sebastian Timo

AU - Boudsocq, Marie

AU - Chardin, Camille

AU - Almeida-Trapp, Marilia

AU - Krapp, Anne

AU - Hirt, Heribert

AU - Mithöfer, Axel

AU - Colcombet, Jean

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank the Stress Signaling group for critical discussion of this work. We also thank Shuqun Zhang and Edward Farmer for providing mkk4 mkk5 and coi1-34 seeds. This work has benefited from a French State grant (LabEx Saclay Plant Sciences-SPS, ANR-10-LABX-0040-SPS), managed by the French National Research Agency under an "Investments for the Future"program (ANR-11-IDEX-0003-02). C.S. and C.C. were funded by SPS PhD fellowships. Marilia Almeida-Trapp gratefully acknowledges financial support by a Capes-Humboldt Research Fellowship. This publication has been written with the support of the AgreenSkills+fellowship program which has received funding from the EU’s Seventh Framework Program under grant agreement No. FP7-609398 (AgreenSkills+ contract) to STS

PY - 2020/4/9

Y1 - 2020/4/9

N2 - Abiotic and biotic factors cause plant wounding and trigger complex short- and long-term responses at the local and systemic levels. These responses are under the control of complex signaling pathways, which are still poorly understood. Here, we show that the rapid activation of clade-A Mitogen Activated Protein Kinases (MAPKs) MPK3 and MPK6 by wounding depends on the upstream MAPK Kinases (MAP2Ks) MKK4 and MKK5 but is independent of jasmonic acid (JA) signaling. In addition, this fast module does not control wound-triggered JA accumulation in Arabidopsis, unlike its orthologues in tobacco. We also demonstrate that a second MAPK module, composed of MKK3 and the clade-C MAPKs MPK½/7, is activated by wounding in a MKK4/5-independent manner. We provide evidence that the activation of this MKK3-MPK½/7 module occurs mainly through wound-induced JA production via the transcriptional regulation of upstream clade-III MAP3Ks, particularly MAP3K14. We show that mkk3 mutant plants are more susceptible to herbivory from larvae of the generalist lepidopteran herbivore Spodoptera littoralis, indicating that the MKK3-MPK½/7 module is involved in counteracting insect feeding.

AB - Abiotic and biotic factors cause plant wounding and trigger complex short- and long-term responses at the local and systemic levels. These responses are under the control of complex signaling pathways, which are still poorly understood. Here, we show that the rapid activation of clade-A Mitogen Activated Protein Kinases (MAPKs) MPK3 and MPK6 by wounding depends on the upstream MAPK Kinases (MAP2Ks) MKK4 and MKK5 but is independent of jasmonic acid (JA) signaling. In addition, this fast module does not control wound-triggered JA accumulation in Arabidopsis, unlike its orthologues in tobacco. We also demonstrate that a second MAPK module, composed of MKK3 and the clade-C MAPKs MPK½/7, is activated by wounding in a MKK4/5-independent manner. We provide evidence that the activation of this MKK3-MPK½/7 module occurs mainly through wound-induced JA production via the transcriptional regulation of upstream clade-III MAP3Ks, particularly MAP3K14. We show that mkk3 mutant plants are more susceptible to herbivory from larvae of the generalist lepidopteran herbivore Spodoptera littoralis, indicating that the MKK3-MPK½/7 module is involved in counteracting insect feeding.

UR - http://hdl.handle.net/10754/662500

UR - http://www.plantcell.org/lookup/doi/10.1105/tpc.19.00917

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U2 - 10.1105/tpc.19.00917

DO - 10.1105/tpc.19.00917

M3 - Article

C2 - 32265268

SN - 1040-4651

VL - 32

SP - tpc.00917.2019

JO - The Plant Cell

JF - The Plant Cell

IS - 6

ER -

Wounding and Insect Feeding Trigger two Independent MAPK Pathways with Distinct Regulation and Kinetics.

Abstract

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