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Signaling through MAP kinase networks in plants

This paper is dedicated to Prof. Sudhir K. Sopory
https://doi.org/10.1016/j.abb.2006.05.001Get rights and content

Abstract

Protein phosphorylation is the most important mechanism for controlling many fundamental cellular processes in all living organisms including plants. A specific class of serine/threonine protein kinases, the mitogen-activated protein kinases (MAP kinases) play a central role in the transduction of various extra- and intracellular signals and are conserved throughout eukaryotes. These generally function via a cascade of networks, where MAP kinase (MAPK) is phosphorylated and activated by MAPK kinase (MAPKK), which itself is activated by MAPKK kinase (MAPKKK). Signaling through MAP kinase cascade can lead to cellular responses including cell division, differentiation as well as response to various stresses. In plants, MAP kinases are represented by multigene families and are organized into a complex network for efficient transmission of specific stimuli. Putative plant MAP kinase cascades have been postulated based on experimental analysis of in vitro interactions between specific MAP kinase components. These cascades have been tested in planta following expression of epitope-tagged kinases in protoplasts. It is known that signaling for cell division and stress responses in plants are mediated through MAP kinases and even auxin, ABA and possibly ethylene and cytokinin also utilize a MAP kinase pathway. Most of the biotic (pathogens and pathogen-derived elicitors) including wounding and abiotic stresses (salinity, cold, drought, and oxidative) can induce defense responses in plants through MAP kinase pathways. In this article we have covered the historical background, biochemical assay, activation/inactivation, and targets of MAP kinases with emphasis on plant MAP kinases and the responses regulated by them. The cross-talk between plant MAP kinases is also discussed to bring out the complexity within this three-component module.

Section snippets

Historical background

The MAPK was first discovered in 1986 from animal cells by Sturgill and Ray [15] and named as microtubule associated protein-2 kinase (MAP-2 kinase). Later this kinase was found to be related to a set of proteins that are phosphorylated at tyrosine residue in response to mitogens and it was renamed as mitogen-activated protein kinase (MAP kinase)

Biochemical assay

The assay for MAP kinase activity is based on the ability of this enzyme to phosphorylate a protein containing a consensus sequence, P-x-S/T-P (proline-x-serine/threonine-proline) [32]. Myelin basic protein (MBP) is the widely used substrate for MAP kinase assay [32]. A routine technique involves the incorporation of MBP into a polyacrylamide gel over which cellular proteins are separated. The kinasing reaction is carried out in the presence of [γ32P]ATP, followed by autoradiography. This

Activation of MAP kinases

In all eukaryotic cells MAP kinase can be regulated at the level of transcription, translation, and/or post-translation (by phosphorylation and dephosphorylation). The MAPKs are activated by dual specificity protein kinases that phosphorylate at the serine/threonine and tyrosine residues in the conserved threonine-x-tyrosine (T-x-Y) sequence of kinase domain [48], [49]. MAPKs also show some tyrosine kinase activity and may auto-phosphorylate on both threonine and tyrosine residues [50]. The

Inactivation of MAP kinases

The inactivation of MAP kinases involves dephosphorylation of threonine and tyrosine residues on T-x-Y motif within the activation loop. Like activation, the inactivation of MAP kinases is also tightly regulated and is catalyzed by protein phosphatases. These have different specificities and subcellular localization. Some phosphatases have been identified which inactivate different isoforms of MAPK, these are known as MAPK phosphatases, which include DSP (dual specificity phosphatase), PP2C

Targets of MAP kinases

In mammals and yeast, MAP kinase cascades are active downstream from G-protein coupled receptors or receptor tyrosine kinases (RTKs) or two-component histidine protein kinase. In response to a stimulus the receptors activate G-proteins like Ras or Rho1, by stimulating the exchange of guanosine triphosphate (GTP) for guanosine diphosphate (GDP). The activated G-proteins, inturn interact with a number of potential effectors such as PI-3-kinase or protein kinase C or MAPKKK like Raf [71]. The

Plant responses regulated by MAP kinases

MAP kinases are one of the largest family of serine-threonine kinases in higher plants that transduce extracellular signals by modulating the activity of other proteins. An activated MAPK, by phosphorylation, can regulate the function of the transcription factors, cytoskeletal components, and other kinases including the other MAP kinase components. MAPK pathway components can execute a wide variety of roles in plant cell signal transduction pathways such as osmoregulation, hormone signaling

Cross-talk between plant MAP kinases

As detailed above, MAP kinases play a central role in transduction of different types of signals. The complexity is enhanced when the activator of MAP kinase pathway is itself regulating diverse plant responses. This is best exemplified by phyto-hormones, which mediate developmental programmes in plants as well as plant responses to a large number of extracellular signals. Usually, more than one hormone is involved in regulating a physiological event. It is therefore evident that plant MAP

Future perspectives for MAP kinase research in plants

The involvement of MAP kinases in various metabolic processes in plant cells might have general implications. In plants the MAP kinase cascade is just beginning to be understood. The overall progress of research on MAP kinases in plant systems has been slow when compared to other systems. However, the increasing numbers of reports describing plant MAP kinase-signaling components reflect their central role in plant growth and development. So far the role of these kinases in stress and hormonal

Glossary

ABI1
ABA insensitive 1
ANP
Arabidopsis NPK1 homolog
AtDsPTP
Arabidopsis thaliana dual specificity protein tyrosine phosphatase
AtMRK
Arabidopsis thaliana MLK/Raf-related protein kinase
AtMPK
Arabidopsis thaliana mitogen-activated protein kinase
Avr
Avirulence
BWMK1
Blast- and wound-induced MAP kinase 1
Bck1
Bypass of C kinase 1
CD domain
Common docking domain
CKI1
Cytokinin histidine kinase sensor
CRE1
Cytokinin response 1
CTR1
Constitutive ethylene response mutant
DSP
Dual specificity phosphatase
EDR1
Enhanced disease

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