Abiotic stress series
Emerging MAP kinase pathways in plant stress signalling

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Mitogen-activated protein kinase (MAPK) pathways transfer information from sensors to cellular responses in all eukaryotes. A surprisingly large number of genes encoding MAPK pathway components have been uncovered by analysing model plant genomes, suggesting that MAPK cascades are abundant players of signal transduction. Recent investigations have confirmed major roles of defined MAPK pathways in development, cell proliferation and hormone physiology, as well as in biotic and abiotic stress signalling. Latest insights and findings are discussed in the context of novel MAPK pathways in plant stress signalling.

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MAPK pathways – a common theme in eukaryotic signal transduction

Humans, yeast and plants share ∼60% of their genes with each other, including components of conserved protein kinase signalling pathways. In all eukaryotes, mitogen-activated protein kinase (MAPK) pathways serve as highly conserved central regulators of growth, death, differentiation, proliferation and stress responses.

A MAPK cascade minimally consists of a MAPKKK–MAPKK–MAPK module that is linked in various ways to upstream receptors and downstream targets. Receptor-mediated activation of a

Components of plant MAPK cascades

On the basis of the fully sequenced Arabidopsis genome, 20 MAPKs, 10 MAPKKs and 60 MAPKKKs were identified and a unified nomenclature for Arabidopsis MAPKs and MAPKKs was proposed [2]. By sequence comparison and signature motif searches, putative orthologues to most of the 20 MAPKs, 10 MAPKKs and 60 MAPKKKs can be identified in the available genomic or EST sequences of Medicago, tobacco and rice. However, in some cases, unequivocal definition of orthologues between different species is not

Logistics of plant MAPK pathways

Previous yeast two-hybrid and transient expression analyses of MAPK cascades in Arabidopsis, tobacco and Medicago have suggested that MAPK pathway components can function in different combinations and have distinct functions in different biological contexts. Recent genetic analyses have largely proven this unforeseen complexity to be correct. Depending on the stimulus, a given plant MAPKK can interact and activate several different MAPKs [9]. MAPKKKs can associate with different MAPKKs and

MAPK pathways in plant pathogen response

Plants respond to pathogen attack by activating multi-step defence responses, including rapid production of reactive oxygen species (ROS), strengthening of cell walls, induction of the hypersensitive response (HR) and the localized cell death at the sites of infection. Plant defence responses also include synthesis of pathogen-related proteins and phytoalexins. During the past couple of years, it has been firmly established that MAPKs play a central role in pathogen defence in Arabidopsis,

Tobacco MEK2–SIPK/WIPK pathway

Studies of the infection of tobacco leaves by TMV (tobacco mosaic virus) revealed that both SIPK and WIPK are activated in an N resistance gene-mediated fashion [13], preceding the HR-like cell death. Because expression and activation of WIPK was correlated with the onset of HR in response to various elicitors and TMV infection, it was assumed that WIPK might be a prime candidate for an HR inducer [14]. However, ectopic expression of SIPK was sufficient to yield active MAPK and induce HR,

Dual function of the tobacco NPK1–MEK1–NTF6 pathway in pathogen defence and cytokinesis

There appears to be at least one more tobacco MAPK pathway involved in pathogen defence. VIGS of MEK1 and its potential substrate MAPK NTF6 attenuated N-mediated resistance of tobacco to TMV [18]; silencing of the potential downstream target WRKY and MYB transcription factors equally compromised N-mediated resistance. MEK1 and NTF6 also play an important role in cytokinesis, a specific function in the cell division cycle [19]. Overexpression of kinase-deficient mutant MEK1 resulted in

Rice TEY and TDY MAPKs are involved in pathogen signalling

An increasing number of MAPK pathway components have been identified in Oryza sativa (reviewed in Ref. [26]). These MAPKs are either of the TEY type, belonging to the A and C groups, or of the D group, containing the TDY MAPKs. For most of the rice MAPKs, only expression data are available, indicating that almost all the genes respond to developmental and hormonal cues and/or various stresses. A more thorough functional investigation of rice MAPK5 (also called MSRMK2, MAPK2, MAP1 or BIMK1), the

Flagellin signalling by the Arabidopsis FLS2–MEKK1–MKK4/MKK5–MPK3/MPK6–WRKY22/WRKY20 pathway

In Arabidopsis, MPK3, MPK4 and MPK6 are all activated by bacterial and fungal PAMPs (pathogen-associated molecular patterns) 28, 29. Arabidopsis mpk4 mutants show a dwarf phenotype, exhibit increased resistance to virulent pathogens, have elevated salicylic acid levels, show systemic acquired resistance, and constitutive expression of pathogenesis-related genes [30]. Given that no induction of the jasmonic acid-response genes PDF1.2 and THI2.1 is observed after treatment with methyl jasmonate,

Are MAPKs the missing link between reactive oxygen species and pathogen signalling?

MAPKs are also involved in mediating oxidative stresses (Figure 2). In tobacco, SIPK and WIPK become activated by various ROS 34, 35 and overexpression or suppression of SIPK rendered plants hypersensitive to ozone treatment [36]. Ozone treatment of Arabidopsis activates MPK3 and MPK6 [37], the orthologues of tobacco SIPK and WIPK, respectively. Although ozone-induced activation of MPK3 and MPK6 was independent of ethylene, it was dependent on salicylic acid and resulted in nuclear

MAPKs in heavy metal signalling

ROS production and signalling is closely related to the topic of the response of plants to heavy metals (Figure 2). Although some of the heavy metals are required for metabolism, growth and development of plants, they are highly toxic in higher concentrations and can result in severe cellular damage. The toxicity of heavy metals is thought to result from the blocking of functional groups or the displacement of essential metal ions in biomolecules or by the autoxidation of redox-active heavy

Salt, cold, drought and wounding are mediated by overlapping sets of MAPKs

MAPKs are known to be activated by osmotic stresses in Medicago and tobacco (reviewed in Ref. [7]). Most progress on linking MAPKs to abiotic stress signalling has come from analysing Arabidopsis: MPK4 and MPK6 are activated by cold, salt, drought, wounding and touch [45]. MPK3 can also be activated by osmotic stress [46]. MEKK1 is transcriptionally induced by salt stress, drought, cold and wounding [47], but also mediates flagellin signalling through activation of MKK4 and MKK5 [10].

MAPKs are downstream of the wounding, UV-B and brassinosteroid receptor

Tomato MPK1, MPK2 and MPK3 are orthologues of Arabidopsis MPK3 and MPK6; they are activated by wounding, systemin, various elicitors and UV-B [50]. The wounding signalling peptide systemin binds SR160, a leucine-rich repeat membrane-spanning protein kinase that is identical to the brassinosteroid receptor BRI1 [51]. SR160 also affects UV-B signalling, suggesting that systemin, brassinosteroid and UV-B might be sensed by the same receptor [52]. Whether MAPKs are downstream components of all

Dual specificity phosphatase MKP1 targets MPK6 and is a negative regulator of genotoxic stress

Isolation of an Arabidopsis mutant with increased sensitivity to the chemical mutagen methyl methanesulfonate and UV-C resulted in the identification of the MKP1 gene, encoding a dual-specific phosphatase that affects genotoxic stress [53]. Surprisingly, although mkp1 mutants showed hypersensitivity to genotoxic stress they were more resistant to salt stress. Subsequent analysis revealed that MKP1 preferentially interacts with MPK6 and to a lesser extent with MPK3 and MPK4 [53]. Although these

Conclusions

The first complete MAPK modules have been identified for signalling biotic and abiotic stresses as well as for cytokinesis. These studies provided compelling evidence for the functioning of a partially overlapping set of MAPKs in different pathways, indicating that knowledge on the presence or absence of other signalling components will be indispensable. Therefore, a future important task will be to monitor the expression of all available MAPK components in a developmental-, tissue- and

Acknowledgements

This work was supported by grants from the Austrian Science Foundation and the Vienna Science and Technology Fund.

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