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

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

doi:10.1105/tpc.19.00917

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 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 (Arabidopsis thaliana), unlike its orthologs in tobacco. We also demonstrate that a second MAPK module, composed of MKK3 and the clade-C MAPKs MPK1/2/7, is activated by wounding in a MKK4/5-independent manner. We provide evidence that the activation of this MKK3-MPK1/2/7 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-MPK1/2/7 module is involved in counteracting insect feeding.

Highlights

Wounding is a common stress for plants that can be caused by abiotic factors such as wind, heavy rain, hail and snow or during biotic interactions, mostly with herbivorous organisms such as insects
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
We introduced a version of the MPK2 gene cloned in-frame with a HA tag in both Col-0 and mkk3-1 genetic backgrounds

Summary

Introduction

Wounding is a common stress for plants that can be caused by abiotic factors such as wind, heavy rain, hail and snow or during biotic interactions, mostly with herbivorous organisms such as insects. Injury may cause severe damage to plant tissues and facilitate the entry of pathogens (Savatin et al, 2014) Plants respond to these challenges by activating several mechanisms to rapidly heal tissues and restrict potential pathogen entry. Living cells surrounding wounded sites can sense mechanical disturbances through the activation of mechanosensitive channels that activate signaling cascades and local responses (Farmer et al, 2014). Such responses are mediated by efficient and complex intracellular signaling mechanisms involving phosphorylation, lipids, Reactive Oxygen Species (ROS) and calcium (Ca2+) signaling, as well as the biosynthesis of phytohormones leading to gene expression reprogramming and longdistance signaling (Savatin et al, 2014). The isoleucine conjugate of JA, (+)-7-iso-jasmonoyl-L-isoleucine (JA-Ile), is the bioactive form of jasmonates (Fonseca et al, 2009)

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