Mitogen-Activated Protein Kinase Cascades in Plant Hormone Signaling

Abstract

Mitogen-activated protein kinase (MAPK) modules play key roles in the transduction of environmental and developmental signals through phosphorylation of downstream signaling targets, including other kinases, enzymes, cytoskeletal proteins or transcription factors, in all eukaryotic cells. A typical MAPK cascade consists of at least three sequentially acting serine/threonine kinases, a MAP kinase kinase kinase (MAPKKK), a MAP kinase kinase (MAPKK) and finally, the MAP kinase (MAPK) itself, with each phosphorylating, and hence activating, the next kinase in the cascade. Recent advances in our understanding of hormone signaling pathways have led to the discovery of new regulatory systems. In particular, this research has revealed the emerging role of crosstalk between the protein components of various signaling pathways and the involvement of this crosstalk in multiple cellular processes. Here we provide an overview of current models and mechanisms of hormone signaling with a special emphasis on the role of MAPKs in cell signaling networks. One-sentence summary: In this review we highlight the mechanisms of crosstalk between MAPK cascades and plant hormone signaling pathways and summarize recent findings on MAPK regulation and function in various cellular processes.

Keywords: MAP kinase cascade; abscisic acid; auxin; brassinosteroids; ethylene; gibberellin; jasmonic acid; salicilic acid.

FIGURE 1

Schematic representation of MAPK cascade.

FIGURE 2

A simplified overview of MAPK cascades involved in JA and SA signaling in plant species such as: A. thaliana (At), O. sativa (Os), Nicotiana tabacum (Nt), S. lycopersicum (Sl) and Z. mays (Zm). Activation of MAPKs by various stimuli causes phosphorylation of MAPK effectors (usually transcription factors) further triggering cellular responses. See text for details.

FIGURE 3

Schematic illustration of the GSK3-like kinase AtBIN2-mediated crosstalk between the AtYODA-AtMKK4/5-AtMPK3/6 cascade and BR signaling in cotyledons and in hypocotyls.

FIGURE 4

MAPKs in ET biosynthesis and signaling. (A) An external stimulus leads to activation of ET biosynthesis predominantly through the MKK9-MPK3/MPK6 cascade. Alternatively, MKK7 may also be involved in MPK3/MPK6 activation due to similarities with the MKK9 sequence and its activation mechanisms. MPK3 and MPK6 can also be activated by MKK4 and MKK5, which act in a redundant fashion upstream of MPK3/MPK6, especially after wounding-induced ET biosynthesis. SIMK (MsMPK6) and NSIPK(NtMPK6-1) are homologs of AtMPK6 from alfalfa and tobacco, respectively. Active MPK6 phosphorylates ACS2/ACS6, which initiates ET biosynthesis. (B) ET is perceived by five different receptors (ETR1, ETR2, ERS1, ERS2, EIN4) localized in the endoplasmic reticulum (ER) membrane and this leads to inhibition of CTR1 kinase activity, which is the primary negative regulator of ET signaling. As a consequence, MKK9 is released from CTR1 inhibition and translocates to the nucleus, where it activates MPK3 and MPK6. Moreover, inactive CTR1 is no longer able to phosphorylate the C-terminal domain (CEND) of EIN2. Dephosphorylated CEND moves to the nucleus and takes part in EIN3 stabilization. (C) In the nucleus, active MPK3/MK6 promotes the stability of the main plant-specific ET-dependent transcription factors (EIN3 and EIL1). Phosphorylation of EIN3 at the T174 position blocks its proteasomal degradation and enables it to activate ET-responsive genes.

FIGURE 5

ABA-regulated MAPKs in Arabidopsis and cotton. ABA promotes stomatal closing. The different cascades are distinguished by different colors in the scheme. Arrows with solid lines represent established signaling pathways, while arrows with dashed lines represent putative signaling pathways. In the presence of ABA, PYR/PYL/RCAR receptors bind the phytohormone and inhibit group A PP2Cs. These events result in activation of SnRK2s. Activated SnRK2s phosphorylate and activate downstream targets, including MAPKs, Respiratory Burst Oxidase Homolog (RBOH) and Slowly Activating Anion Conductance (SLAC S-type). Active RBOH mediates ROS production. Note that in guard cells crosstalk between ABA signaling and ROS signaling may coincide at the MAPK level and regulates stomatal closure.

FIGURE 6

Overview of MAPKs regulated by ABA in different plant species. A single ABA-activated MAPK cascade MAPKKK17/18-MKK3-MPK1/2/7/14 has been identified in Arabidopsis. This pathway is involved in drought resistance, senescence, stomatal development and signaling. In addition, MKK3 in both maize and cotton has been shown to function in response to ABA. In maize, MKK3 acts downstream of MEKK1 and transcripts for both kinases are upregulated on ABA treatment. In cotton, ABA and drought induce activation of a MAPK cascade composed of MKK3, MPK7 and PIP1. These two pathways, MEKK1–MKK3 in maize and MKK3–MPK7–PIP1 in cotton, are associated with drought resistance and stomatal signaling. Another module in cotton, MAPKKK49-MKK4/MKK5, is involved in the ABA-mediated response to abiotic stress. MPK17 is another well-characterized MAPK in cotton, which regulates the response to salt and osmotic stresses. ABA-inducible genes encoding cotton MAPK cascade components presented in the scheme are MKK3, MAP3K49 and MPK17, respectively. Some MAPK cascades have a similar function in different plant species. In Arabidopsis and apple, the MKK1-MPK6 module affects seed germination and early seedling growth. ABA treatment induces transcription of the genes encoding MKK1 and MPK6 in both plant species. In Arabidopsis, MKK1 mediates activation of MPK6, thereby regulating CATALASE1 expression in ROS homeostasis. Additionally, glucose treatment significantly increases MKK1 and MPK6 activities. In apple, ABA-responsive transcription factor ABI5 may act as a downstream target of this MAPK cascade. MPK5 and MPK3 in maize and MPK1 and MPK5 in rice are required for ABA-induced antioxidant defense and play a similar role to Arabidopsis MPK6. In maize, ABA treatment significantly increases MPK5 and MPK3 activities. In rice, ABA treatment induces MPK1 and MPK5 expression.