Evaluation of Oxidative and Salt Stress Induced Mitogen Activated Protein Kinase Genes in Arabidopsis thaliana by Bioinformatical Approach

Research Article

Evaluation of Oxidative and Salt Stress Induced Mitogen Activated Protein Kinase
Genes in Arabidopsis thaliana by Bioinformatical Approach

Corresponding author:  Dr. Melike Bor, University of Ege, Faculty of Science Department of Biology 35100 Bornova/Izmir TURKEY, Tel: +90 232 3112433 ; Email: melike.bor@ege.edu.tr

 

Abstract

Mitogen activated protein kinases (MAPKs) are known to be involved in many stress signaling pathways, including oxidative and salt stresses. In the current study, MAPK genes of A. thaliana were selected from UniProt database, their expression levels were analyzed by AtGenExpress Microarray database and classified with DAVID Bioinformatics on-line software according to their molecular functions in response to oxidative and salt stresses. Activation of oxidative and salt stress response genes which belong to MAPK signal cascade were investigated using gene ontology (GO) terms and expression profiles. Functional classification of 77 MAPK genes using DAVID Bioinformatics database revealed that, a total number of ten genes were associated with these stresses and, MPK6 was a common induced gene. Besides this gene, MPK3, MPK7, MEK1 and NP1 were induced by oxidative stress while, MPK4, MEKK1, ABI5, MKK2 and MKP1 were induced by salt stress. This is the first report which used a bioinformatical approach to analyze oxidative and salt stress-inducible MAPK genes in A.thaliana.

Keywords: MAPKs; Abiotic Stress; Bioinformatics

Introduction

Plants are affected by various abiotic and biotic stress factors and, because they are sesile, they have evolved multiple adaptations for overcoming these stresses. Mitogen activated protein kinases (MAPKs) play important roles in abiotic stress signaling pathways due to their protein phosphorylation activites [1]. Phosphorylation consists of three associated protein components, including MAPK kinase kinase (MEKK, MAPKKK), MAPK kinase (MKK, MAPKK) and terminal MAPK. MAPKs phosphorylate transcription factors, other protein kinases, and cytoskeleton-associated proteins [2]. MAPKKK-MAPKK-MAPK signaling module is involved in signal transduction that is related to transfer information from receptors to targets. MAPKKs are activated by MAPKKKs which are known to include phosphorylation of two serine/threonine residues, revealed the function of MAPKKKs as serine/threonine kinases while MAPKKs phosphorylate the threonine/tyrosine residues of MAPKs [2]. MAPK cascade components including 20 MPKs, 10 MAPKKs, and 80 MAPKKKs are encoded by 110 genes in the Arabidopsisgenome which is the highest number of genes found in all eukaryotes so far. Efforts for characterization and identification of all these MAPKs by classical approaches have revealed some information about the role and function of these genes in relation to environmental stresses (Table 1). However, the characterized genes presented here consisted only a small portion of whole MAPKs family and their interaction with other stress responsive pathways are still unclear.

Salt stress causes negative effects on plant productivity and growth in many regions of the world [9]. The MAP kinase kinase AtMEK1 from A. thaliana seedlings subjected to salt stress showed an increased kinase activity towards the substrate MPK4 [10]. Ulm et. al. [11] identified MKP1-interacting MAPKs and genes with expression affected with MKP1 levels. They concluded that MKP1 acts as a cross talk point of stress signalling pathways due to different levels of salt stress resistance in mkp1 mutant (loss of phosphatase activity). They showed that this MKP protein is involved in salt stress response and thatArabidopsis MAP kinase MPK6 was regulated in vivo by MAP kinase phosphatase 1, which interacts with MPKs 3 and 4 as well as MPK6 [6]. Both MPK3 and MPK6 can be activated by MKK4 and MKK5 in Arabidopsis [12]. Moreover studies using yeast complementation assays have found that MKK1 can also activate MPK4 [3,10,13]. Ichimura et al. [4] indicated that several extracellular stress stimuli such as low temperature, wounding, hyper-osmolarity and touch in A. thaliana, activated MAP kinases ATMPK4 and ATMPK6. A reverse genetic approach used by Teige et al. [5] confirmed that over expression of wild-type or constitutively active MKK2 resulted in increased MAPK kinase activity of MKK2 resulting in enhanced freezing and salt tolerance. On the contrary they also showed that mkk2 null mutant plants exhibited hypersensitivity to freezing and germination on salt-containing media; as a result, the authors suggested that MKK2 has an important role in protecting the plant from cold and salt stress.

Table 1. MAPK cascade components regulated by salt and osmotic stresses which were characterized in A. thaliana.

Production of reactive oxygen species (ROS) under abiotic stress can cause oxidative stress [14] that can stimulate differentMAPKs cascades [15]. Exogenous H2O2 treatment leads to oxidative stress that can trigger MPK1 and MPK2 [16] MPK3 and MPK6 [17], MPK4 [2] and MPK7 [18] in Arabidopsis. Kovtun et al. [17] reported the H2O2 can induce ANP1, which begins a MAPK cascade that can trigger at least two MAPKs, AtMPK3 and AtMPK6 in Arabidopsis. Moreover, Xing et al. [19]demonstrated the ABA-dependent MKK1-mediated activation of MPK6 to regulate catalase 1 (CAT1) expression in ROS homeostasis. In another assay, a double knockout mutant of the MAPK-interacting phosphatases, pp2c5/ap2c1, showed induced ABA-dependent activation of MPK3 and MPK6, resulting in ABA insensitivity and hence implying that a MAPK cascadeinvolving MPK3/MPK6 negatively controls ABA signaling in plants [20]. MPK7 interacts with MKK3, and also MKK3 phosphorylates MPK7 which is activated by H2O2 and this activation is noticeably induced by coexpression with MKK3 [18]. Itwas also shown that H2O2 can specifically activate Arabidopsis NPK1-related protein kinase which induces phosphorylationcascade via MPK3 and MPK6 activation [17]. Phenotypic and molecular analysis showed that MKK1 and MKK2 involved in regulating ROS and salicylic acid (SA) accumulation [14].

Although recent studies indicate that plant MAPKs are induced by abiotic and biotic stress factors, the involvement of MAPKs in plant oxidative and salt stress responses utilizing a bioinformatic approach has been reported. In this study, the role of MAPK cascade genes, which responds to oxidative and salt stresses, was investigated. To understand how MAPK signalcascade is involved in plant responses to oxidative and salt stresses in the model plant, A. thaliana, we focused on GO (Gene Ontology) annotations and microarray data. MAPK encoding genes in A. thaliana were achieved from Uniprot database).Among all 77 MAPK cascade genes, we found five oxidative stress- (MPK3, MPK6, MPK7, MEK1, NP1) and six salt stress-inducible genes (MPK6, MPK4, MEKK1, ABI5, MKK2, MKP1) using DAVID bioinformatics tool [22]. Annotations of these genes were obtained from National Center for Biotechnology Information [23] and transfered to Microsoft Excel (Microsoft,Redmond, WA). AtGenExpress was used to create and analyze expression profiles of these genes which enabled us to visualize gene expression data from Arabidopsis roots and seedlings.

Methods

Analysis of mitogen activated protein kinase genes of A. thaliana were obtained from Uniprot database [21] and included GOTERM_BP_FAT, GOTERM_CC_FAT and GOTERM_MF_FAT. A total of 77 MAPK genes were selected from Uniprot and ten of these genes were found to be associated to salt and oxidative stress response characteristics based on DAVID Bioinformatics Resources 6.7. DAVID bioinformatics is a web accessible program that is used for systematic and integrative analysis of large gene lists. Salt and oxidative stress related MAPK genes of A. thaliana in GOTERM_MF_FAT were used to determine and clasify their molecular functions [24]. Genes involved in salt and oxidative stress related to MAPKs were extracted from UniProt and then, copied into AtGenExpress Microarray database to analyze the expression levels of these genes. For all genes which were extracted from UniProt, AtGenExpress Visualization Tool [25] was used to analyze their microarray expression values in the Arabidopsis seedlings and roots under salt/oxidative stress conditions.

Results

Functional Classification of Oxidative and Salt Stress Related MAPK Genes in A.thaliana

We screened all the known A. thaliana MAPK genes in UniProt Database and then formed a gene list comprising a total of 77MAPK genes (Table 2). The list of accession numbers of these genes was integrated into DAVID Bioinformatics database, andthen abiotic stress related genes were categorized into ‘response to oxidative stress’ and ‘response to salt stress’ by usingkeywords from GOTERM_BP_FAT of DAVID Bioinformatics Database. Two gene lists were also analysed independently using the by gene functional classification tool of the programme and genes which were not related to either of the stress classessubsequently removed from the input gene list. Ten of 77 MAPK genes which have salt and oxidative stress responsecharacteristics share MAPK6 as a common gene according to the results of the analysis (Figure 1). Besides the commonresponsive gene, MAPK6; MPK3, MEK1, MKY7 and NP1 were found out to be related to oxidative stress while, MPK4, MEKK1,ABI5, MKK2 and MKP1 were related to salt stress (Figure 1). Functional classification of five oxidative stress response and six salt stress response genes which belong to MAPK cascade, revealed that these genes were associated with protein serine/threonine kinase activity, protein kinase activity, ATP binding, etc. (Figure 1, Table 3). Previous data shown on table 1 provided information about functionally characterized MAPK genes related to oxidative and salt stress responses. We found that other components of MAPK cascade; MEK1, MKY1, NP1, ABI5, MKK2 and MKP1 were also associated with oxidative and salt stress responses in A. thaliana by using a bioinformatic approach.

Figure 1. Salt and oxidative stress induced MAPK genes in A.thaliana analyzed by DAVID Bioinformatics software.

Expression Levels of Oxidative and Salt Stress MAPK Genes of A.thaliana

Oxidative and salt stress associated MAPK genes were not only identified but also subjected to comparative analysis according to their expression patterns in different plant organs by bioinformatic approach (Figure 2 and 3). These results were given as time-course expression values derived from AtGenExpress Microarray database for MPK3 (At3g45640), MPK7 (At2g18170), MKP6 (At2g43790), MEK1 (At4g26070), NP1 (At1g09000) under oxidative stress (Figure 2) and MKP1 (At3g5527), MPK4 (At4g01370), MPK6 (At2g43790), MKK2 (At4g29810), MEKK1 (At4g08500), ABI5 (At2g36270) under salt stress treatments (Figure 3).

In roots of methyl viologen-exposed plants, MPK3 expression was detected and the highest rate observed in the first 0.5hours and expression reached to its maximum after approxiametly three hours (Figure 2). Additionaly after oxidative stress treatment, the highest expression value of MPK6 in Arabidopsis root was determined in the first three hours. Root or seedlingprotein extracts with MAPK-specific antibodies immunoprecipitated MPK3, MPK4, or MPK6, and while all three MAP kinasesdisplayed below basal kinase activity in root extracts, they were all strongly induced by H2O2 treatment in wild type Col-0 plants. MPK6 expression value in roots showed significantly increased gene expressions at 0.5, 1 h after initiation by exposure to methyl viologen. In methyl viologen-exposed seedlings, expression of the MPK6 gene was initially significantlyreduced after exposure (0.5 h) but a significant increase was observed from one h and later (Figure 3). In roots, expressionof MPK7 was significantly upregulated after six h exposure to methyl viologen; moreover, MPK7 gene expression value was lower in above-ground structures compared to roots. Under oxidative stress treatments, MPK7 expression value in roots displayed induced gene expressions in the first six h after starting exposure to methyl viologen. In seedlings, MPK7expression reached the highest value in the first six h. MEK1 expression in seedlings was substantially affected by oxidativestress conditions and methyl viologen on MEK1 expression in seedlings produced the highest expression after 12 h of oxidative stress treatment. Gene expression of NP1 was studied in root and above-ground parts in. There was very little expression of NP1 in within the first three hours of oxidative stress. The gene expression increased at 12 h after methyl viologen treatment in seedlings. Higher expression of NP1 in root was found after 12 h oxidative stress and oxidative stress-induced expression of NP1 reached its highest level after 12 h.

Cellular component analysis of salt stress responsive genes indicated that MKK2 is localized to the plasma membrane. MKK2gene expression increased to its highest level after 12 h in salt stressed seedlings. Expression value reached its minimum after 3 h (Figure 3). After salt stress the highest expression of MKK2 in root occured after six h then levels decreased. Geneexpression declined to the lowest level 3 h after salt stress in seedlings. Higher expression of MPK4 in root was found after 12 h of salt stress. Salt stress-induced expression of MPK4 reached its highest level after 12 h in roots, while the highestexpression value of MPK6 occured 3 h post-salt stress in seedlings. Highest expression of MPK6 was detected after 0.5 h saltstress treatment in roots and then it declined. MKK2 gene expression increased to its highest level 12 h of after application of salt stress in seedlings and its expression value was at its minimum after 3 h. Six hours post-salt stress, expression of MKK2reached a maximum and then decreased. Response of MKK1 to salt stress started at 0.5 h post treatment, decreased slightly at three hours and peaked at 24 h. Expression of the protein in roots increased gradually to three hours and peaked at six hours post treatment. Salt stress-induced expression of ABI5 reached to its highest level after three hours in seedlings, while it gradually decreased after six hours in the salt-treated roots.

Figure 2. Expression values of MPK3 (At3g45640), MPK6 (At2g43790), MPK7 (At2g18170), MEK1 (At4g26070) and ANP1 (At1g09000) under oxidative stress treatments in A. thaliana analyzed by AtGenExpress Microarray database. Expression values were measured at six time points (0.5-24h) and labelled as (x).

Figure 3. Expression values of MKP1 (At3g55270), MPK4 (At4g01370), MPK6 (At2g43790), MKK2 (At4g29810), MEKK1 (At4g08500) and (ABI5) (At2g36270) under salt stress treatments in A. thaliana analyzed by AtGenExpress Microarray database. Expression values were measured at six time points (0.5-24h) and labelled as (x).

Table 2. N ames and annotations of MAPK genes in A. thaliana extracted from Uniprot Database.

Table 3. Functional classification of MAP kinase genes related to osmotic and salt stress responses in A. thaliana.

Discussion

MAPK cascades are important players of abiotic stress signaling pathways [2]. Studies demonstrated links between MAPKs and abiotic stress signalling using the model plant A. thaliana. All the five genes related to oxidative stress have functions in the protein serine/threonine kinase activity, protein kinase activity, ATP binding, adenyl ribonucleotide binding, etc. (Table 2; Figure 2). Under anoxia and reoxygenation circumstances, H2O2 accumulates in the apoplast in association with the plasma membrane in roots of rice and wheat seedlings [26]. Roots and/or leaves reduce mitotic activity, cell numbers or cell division rates in response to many abiotic stress conditions [27,28]. Pitzschke and Hirt [14] reported ROS signal pathway interfere root hair development and a number of protein kinases depends on ROS signaling pathway. Roots replied to abiotic stresses via rapid MAPK activation that has been detected in other plant tissues [29].

According to our molecular classification of salt stress related MAPK genes, all of the salt stress responsive genes have functions in protein serine/threonine kinase activity, protein kinase activity, ATP binding, adenyl ribonucleotide binding, purine nucleosideha [30] reported the overexpression of OsMKK6 under 200 mM salt stress in rice increased root/shoot length, weight, MAPK activity and reduced chlorophyl bleaching compared to wild type plants. OsMAPK5 overexpression caused enhanced plant tolerance to salt, drought and cold stresses. MEKK1 is transcriptionally induced after salt, drought, cold and wounding stress treatments. MPK3 expression in Arabidopsis plants, increased significantly in response to cold, touch, and salinity stress. MPK4 and MPK6 have functions in distinct signal transduction pathways responding to different environmental stresses. Matsuoka et al. [10] proved the function of MKK1 as a MAPK kinase, which is involved in abiotic stress signaling. The fact that MEKK1 functions upstream of MKK1, MKK2 and MPK4 in yeast was shown by Ichimura et al. [4] and in cold and salt stress a role for the MAPK module consisting of MEKK1–MKK2–MPK4/MPK6 has been confirmed. In alfalfa cells, high salt concentration or hyperosmotic conditions activate SIMK (salt-induced MAPK), and in tobacco cells activate SIPK (salicylic acid-inducible protein kinase). López-Bucio et al. [31] characterized the role of MAPK 6 in embryo development and in post-embryonic root system architecture of Arabidopsis. They also identified MPK6 as a repressor of primary and lateral root development in this plant. No significant changes in the protein levels of the three MAPKs were found in roots of mekk1 plants but the analysis of the kinase activities was highly disparate in seedlings protein amounts [2]. Under stress conditions seedling growth was associated with the compensatory activation of MPK3 [32].

Oxidative and salt stress responsive MAPK genes were analysed also to identify common associated genes and, only one gene; MPK6was found. This gene was reported to be induced in many abiotic and biotic stress signaling pathways in different plant species [4,33].MPK3, MPK4 and MPK6 are the most extensively studied MAPK signalling components in Arabidopsis and crop plants [34]. TheArabidopsis MKK1/MKK2-MPK4/MPK6 cascades were reported to have functions in the responses to salt and cold stresses and pathogen attack [5,35]. The expression levels of oxidative and salt stress induced MAPK genes in A. thaliana were analysed by a bioinformatical approach and their role in response to these stressors were confirmed. These results suggest that with the aid of bioinformatic tools, complex plant signalling cascades such as; MAPK cascade might be analysed by its sub-components which could provide clues for their involvement in common stress responses. This kind of information would also be useful for targeting and characterizing the components of complex networks by experimental approach.

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