Arabidopsis MAPK Phosphatase 2 (MKP2) Positively Regulates Oxidative Stress Tolerance and Inactivates the MPK3 and MPK6 MAPKs

Two closely related Arabidopsis mitogen-activated protein kinases (MAPKs), MPK3 and MPK6, are rapidly but transiently activated in plants exposed to ozone. Although the contribution of these MAPKs to control of redox stress has been examined extensively, it remains unclear whether the dual-specificity MKPs play an essential role in the regulation of these processes. To explore this question, specific knockdown of each of the five putative MKPs in Arabidopsis was performed, and the ozone sensitivity phenotype of each MKP-suppressed line was assessed. Silencing of only one previously uncharacterized MKP, designated AtMKP2, rendered the plants hypersensitive to oxidative stress. AtMKP2-suppressed plants displayed significantly prolonged MPK3 and MPK6 activation during ozone treatment, and recombinant AtMKP2 was able to dephosphorylate both phospho-MPK3 and phospho-MPK6 in vitro, providing direct evidence that AtMKP2 may target these oxidant-activated MAPKs. In addition, the in vitro phosphatase activity of AtMKP2 was enhanced by co-incubation with either recombinant MPK3 or MPK6. In AtMKP2:YFP-expressing plants, the fusion protein was localized predominantly in the nucleus, the same compartment into which ozone-activated MPK3 and MPK6 have previously been shown to be translocated. Taken together, these data suggest that AtMKP2, a novel MKP protein in Arabidopsis, acts upon MPK3 and −6, and serves as a positive regulator of the cellular response to oxidant challenge. Two closely related Arabidopsis mitogen-activated protein kinases (MAPKs), MPK3 and MPK6, are rapidly but transiently activated in plants exposed to ozone. Although the contribution of these MAPKs to control of redox stress has been examined extensively, it remains unclear whether the dual-specificity MKPs play an essential role in the regulation of these processes. To explore this question, specific knockdown of each of the five putative MKPs in Arabidopsis was performed, and the ozone sensitivity phenotype of each MKP-suppressed line was assessed. Silencing of only one previously uncharacterized MKP, designated AtMKP2, rendered the plants hypersensitive to oxidative stress. AtMKP2-suppressed plants displayed significantly prolonged MPK3 and MPK6 activation during ozone treatment, and recombinant AtMKP2 was able to dephosphorylate both phospho-MPK3 and phospho-MPK6 in vitro, providing direct evidence that AtMKP2 may target these oxidant-activated MAPKs. In addition, the in vitro phosphatase activity of AtMKP2 was enhanced by co-incubation with either recombinant MPK3 or MPK6. In AtMKP2:YFP-expressing plants, the fusion protein was localized predominantly in the nucleus, the same compartment into which ozone-activated MPK3 and MPK6 have previously been shown to be translocated. Taken together, these data suggest that AtMKP2, a novel MKP protein in Arabidopsis, acts upon MPK3 and −6, and serves as a positive regulator of the cellular response to oxidant challenge. To survive, plant cells must maintain redox homeostasis in the face of a range of oxidative challenges from both internal and external sources, including potentially damaging “reactive oxygen species” (ROS) 2The abbreviations used are: ROSreactive oxygen speciesMAPKmitogen-activated protein kinaseMKPMAPK phosphataseMAPKKMAPK kinaseRNAiRNA interferenceDEXdexamethasoneRTreverse transcriptionERKextracellular signal-regulated kinaseGSTglutathione S-transferaseOMFP3-O-methylfluorescein phosphateYFPyellow fluorescent proteinDSPdual-specificity phosphataseCaMVcauliflower mosaic virusPTPphosphotyrosine phosphataseMKKplant MAPKK generated by high energy electron transfer systems in the chloroplasts, mitochondria, and peroxisomes and by environmental insults such as UV and ozone (1Pellinen R. Palva T. Kangasjarvi J. Plant J. 1999; 20: 349-356Crossref PubMed Scopus (168) Google Scholar, 2Boldt R. Scandalios J.G. Free Radic. Biol. Med. 1997; 23: 505-514Crossref PubMed Scopus (43) Google Scholar, 3Mittler R. Trends Plant Sci. 2002; 7: 405-410Abstract Full Text Full Text PDF PubMed Scopus (7996) Google Scholar). At the same time, there is good evidence that specific ROS can also act as signal transduction messengers, most notably in the detection and response processes by which plant cells deal with potential pathogens (4Lamb C. Dixon R.A. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997; 48: 251-275Crossref PubMed Scopus (2566) Google Scholar) and herbivores (5Leitner M. Boland W. Mithofer A. New Phytol. 2005; 167: 597-606Crossref PubMed Scopus (163) Google Scholar) but also in physiological processes such as control of stomatal aperture (6Zhang X. Zhang L. Dong F. Gao J. Galbraith D.W. Song C.P. Plant Physiol. 2001; 126: 1438-1448Crossref PubMed Scopus (551) Google Scholar). These seemingly contrasting scenarios require the cell to manage ROS levels through temporally and spatially modulated mechanisms that allow suppression of undesirable ROS accumulation while still permitting intra- or intercellular transmission of ROS-encoded information. The first step in these redox homeostatic mechanisms is the detection and signaling of ROS levels through an orchestrated sequence of intracellular signaling events. reactive oxygen species mitogen-activated protein kinase MAPK phosphatase MAPK kinase RNA interference dexamethasone reverse transcription extracellular signal-regulated kinase glutathione S-transferase 3-O-methylfluorescein phosphate yellow fluorescent protein dual-specificity phosphatase cauliflower mosaic virus phosphotyrosine phosphatase plant MAPKK Genes encoding mitogen-activated protein kinases (MAPKs) and their upstream activators (MAPK kinases and MAPK kinase kinases) form highly conserved families in eukaryotes, including plants (7Hamel L.P. Nicole M.C. Sritubtim S. Morency M.J. Ellis M. Ehlting J. Beaudoin N. Barbazuk B. Klessig D. Lee J. Martin G. Mundy J. Ohashi Y. Scheel D. Sheen J. Xing T. Zhang S. Seguin A. Ellis B.E. Trends Plant Sci. 2006; 11: 192-198Abstract Full Text Full Text PDF PubMed Scopus (405) Google Scholar, 8Hirt H. Results Probl. Cell Differ. 2000; 27: 1-9Crossref PubMed Scopus (31) Google Scholar, 9Wrzaczek M. Hirt H. Biol. Cell. 2001; 93: 81-87Crossref PubMed Scopus (71) Google Scholar), and these kinase-based signal transduction modules are known to regulate a host of cellular processes, including responses to oxidant stress (10Samuel M.A. Miles G.P. Ellis B.E. Plant J. 2000; 22: 367-376Crossref PubMed Google Scholar). In Arabidopsis, the MAPKs most implicated in oxidative stress signaling are MPK3 and MPK6. Suppression of the ozone-activated MAPK, MPK6, results in a marked ozone-hypersensitivity phenotype (11Miles G.P. Samuel M.A. Zhang Y. Ellis B.E. Environ. Pollut. 2005; 138: 230-237Crossref PubMed Scopus (71) Google Scholar), as does loss of its close homologue, MPK3 (11Miles G.P. Samuel M.A. Zhang Y. Ellis B.E. Environ. Pollut. 2005; 138: 230-237Crossref PubMed Scopus (71) Google Scholar), whereas constitutive activation of MPK6 in Arabidopsis by ectopic expression of a heterologous tobacco MAPKK, NtMEK, also induces rapid cell death (12Liu Y. Zhang S. Plant Cell. 2004; 16: 3386-3399Crossref PubMed Scopus (664) Google Scholar). Thus, it appears that either loss or unregulated activation of MPK3 and/or MPK6 makes plant cells more vulnerable to oxidative stress. The activation of MAPKs such as MPK3 and MPK6 is the result of MAPKK-catalyzed dual phosphorylation of a -TXY- motif in the activation loop near sub-domain VIII of the kinase domain (13Jonak C. Okresz L. Bogre L. Hirt H. Curr. Opin. Plant Biol. 2002; 5: 415-424Crossref PubMed Scopus (544) Google Scholar). ROS-elicited activation of these MAPKs is normally transient (14Desikan R. Hancock J.T. Ichimura K. Shinozaki K. Neill S.J. Plant Physiol. 2001; 126: 1579-1587Crossref PubMed Scopus (197) Google Scholar), indicating that the -pTXpY- phosphate groups are quickly removed, and the MAPK is deactivated, presumably through the action of phosphoprotein phosphatases. Although much is known about the activation and biological roles of MPK3 and MPK6 in plants (15Kovtun Y. Chiu W.L. Tena G. Sheen J. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 2940-2945Crossref PubMed Scopus (1200) Google Scholar), the process by which they are inactivated remains unclear. In mammalian systems, MAPK dephosphorylation is typically catalyzed by a group of specialized dual-specificity phosphotyrosine phosphatases known as MAPK phosphatases (MKPs) that regulate the activities of their MAPK targets through specific dephosphorylation of both phosphotyrosine and phosphothreonine residues (16Camps M. Nichols A. Arkinstall S. FASEB J. 2000; 14: 6-16Crossref PubMed Scopus (720) Google Scholar). Because both the magnitude and duration of MAPK activity can dictate the outcome of physiological responses, MKPs play important roles in modulating MAPK signaling processes. The 11 members of the mammalian MKP family exhibit differential specificities toward their MAPK substrates as well as distinct subcellular localization patterns (17Dickinson R.J. Keyse S.M. J. Cell Sci. 2006; 119: 4607-4615Crossref PubMed Scopus (279) Google Scholar), and they are collectively responsible for the regulated dephosphorylation and inactivation of the 14 presently identified mammalian MAPKs. In contrast, the Arabidopsis genome encodes five potential MKPs, based on the amino acid sequence similarity of the phosphatase catalytic domain to established animal MKPs (18Kerk D. Bulgrien J. Smith D.W. Barsam B. Veretnik S. Gribskov M. Plant Physiol. 2002; 129: 908-925Crossref PubMed Scopus (214) Google Scholar). This five member family of putative AtMKPs includes the previously reported members, and but only one has been shown to dephosphorylation activity an Arabidopsis MAPK R. Y. J. S. Plant J. 16: PubMed Google Scholar). physiological has been for on the was reported to with MAPK MPK6 in and the displayed of MPK6 activity in response to stress in R. G.P. N. J. Genes 2001; PubMed Scopus Google Scholar, R. Ichimura K. T. T. X. Shinozaki K. J. J. 2002; PubMed Scopus Google Scholar). these of a and MPK6, the of to dephosphorylation of activated MAPKs has been and that putative MKP, AtMKP2 in the regulation of cellular homeostasis in and can the activation of MPK3 and MPK6. Suppression of AtMKP2 a marked ozone sensitivity phenotype in Arabidopsis plants, and this is by prolonged activation of both MPK3 and MPK6. also that AtMKP2 is a MKP of the conserved motif of MPK3 and MPK6 in vitro and that its catalytic activity is significantly by with these MAPKs. these results that AtMKP2, the member of the putative MKP family in Arabidopsis, to the of plant cells by redox stress and that it may through its to dephosphorylate the oxidant-activated MPK3 and Plant and Arabidopsis and five and used in this on with or and for for and to and a for At this of each of the five potential MKPs in the was by the plants to with dexamethasone the ozone treatment, the plants exposed to ozone generated by a and with a ozone the treatment, the and on plants with recombinant a for protein and RNA these in and of Arabidopsis RNA interference a the from the of AtMKP2, and based on the and to the of MPK6 was into the The a that generated a on one and an or sequence on the of the The a that a and either or on the of the These into by a which the the control of the T. Plant J. 1997; 11: PubMed Scopus Google Scholar). the was in and Arabidopsis plants by the S.J. Plant J. 16: PubMed Google Scholar). RNA and the of expression by reverse RNA from plants the Plant to the The of RNA was by the transcription was a and of the used as for The used for AtMKP2 AtMKP2 and and in and in of for of in and The protein was a with as a was New or as and or as cell death was by with a in in of was as of the by from five plants in each of the of and for of and in which the was to activity for for and for or the activation phosphorylation with residues to a kinase and for and and for or the catalytic was by for such by with the the expression a or as The to the and the of to MPK6, AtMKP2, and by The and by the and in either the or which the recombinant protein with a to the and and expression into the host and expression of protein was by of on a glutathione to the activity of AtMKP2 was in a and 3-O-methylfluorescein phosphate in a The was by of of and the of was from the by and line of data from of In MPK3 and MPK6, recombinant was with either recombinant or in the kinase and for To recombinant was with recombinant The was on a to from the To dephosphorylate the MPK6, and of either recombinant or recombinant AtMKP2 and and with of MPK6, or and for The was by of by for on a and phosphorylation of and was by which the -pTXpY- motif in and fusion protein the To the AtMKP2 was and into the was into the of To the a AtMKP2 upstream of the was and the was into the of Arabidopsis each fusion in for was with for for and in for The examined a was used for with a aperture from cells the the encoding was to Lee J. Klessig T. Plant Cell. 2001; PubMed Scopus Google Scholar) of was used for the and and through to Silencing MKP-suppressed plants of the are and exposed to ozone for ozone results in rapid activation of MPK3 and MPK6 (11Miles G.P. Samuel M.A. Zhang Y. Ellis B.E. Environ. Pollut. 2005; 138: 230-237Crossref PubMed Scopus (71) Google Scholar, R. J. M. R. Scheel D. Kangasjarvi J. Plant J. 2004; PubMed Scopus Google Scholar), which to levels of activity but loss of for either kinase the of the and is by ozone sensitivity (11Miles G.P. Samuel M.A. Zhang Y. Ellis B.E. Environ. Pollut. 2005; 138: 230-237Crossref PubMed Scopus (71) Google Scholar). To whether of the five putative Arabidopsis MKP and play a role in this or the ozone examined the MKP first each of these five but able to with in either of a of for a or plants be in for of that target the highly of each of the five potential MKP To potentially damaging of also these the control of a A. plants with each of the and for In the of of these normally and displayed the of plants each with for and the expression of each MKP was by Suppression of from each of the five MKP was to from to of the most for each of the five MKP for of the and of the knockdown and used for Because high levels of expression of the in plants the have been reported to stress Y. Plant J. 1999; 20: PubMed Scopus Google Scholar), by for expression levels and only with to levels of expression to of five to ozone in the of plants whereas was on or on of the this cellular can be by of of an ozone that plants with ozone control of more rapidly plants from plants by and only a in this plants the also of ozone these these data that loss of the of Arabidopsis plants to control redox stress. MPK3 and MPK6 in MPK3 and in plants is on MKP that MKP MPK3 and MPK6 activation during ozone challenge. To expression of each was by treatment, and the plants with ozone. from to of the ozone and the of activation of MPK3 and MPK6 was on of an that only the form of these MAPKs. of was by the and with MPK6 levels are known to be by stress R. J. M. R. Scheel D. Kangasjarvi J. Plant J. 2004; PubMed Scopus Google Scholar). The ozone activation of both MPK3 and MPK6 in and in and plants but in plants, activation of both kinases be for to well the which both kinases been inactivated in the MKP-suppressed a encodes a protein with a well conserved dual-specificity phosphatase catalytic act on both and residues in protein and in and the of MKPs is in MAPK activity S.M. Curr. Opin. Cell Biol. 2000; PubMed Scopus Google Scholar, M. T. R. J. 1999; PubMed Scopus Google Scholar). To whether the encodes a MKP examined the catalytic of the recombinant protein was in and by the phosphatase the recombinant protein was shown to dephosphorylate in a and and is well established that of the conserved in the catalytic of by activity A. Cell. 2004; 16: PubMed Scopus Google Scholar). the was as a fusion protein this form of the was to phosphatase activity in the Taken together, data that the protein by can be a member of the MKP of and it AtMKP2 and in activity of a MAPK is on the phosphorylation of its -TXY- motif J. Physiol. Rev. 2001; PubMed Scopus Google Scholar), and these acid residues are also the target of MKP The that loss of AtMKP2 in plants is with inactivation of MPK3 and MPK6 that the AtMKP2 phosphatase be or responsible for these MAPKs. To this in vitro MAPK dephosphorylation recombinant MPK3 and MPK6 as To that MAPK activity with the phosphatase MPK3 and MPK6 first their to kinase These as recombinant fusion and and by with a recombinant activated form of the upstream MAPKK, The of AtMKP2 to dephosphorylate the motif of MPK3 and MPK6 in vitro was by of recombinant with phospho-MPK3 or phospho-MPK6 and the of the -pTXpY- signal by The phosphorylation of both MPK3 and MPK6 was upon with in a whereas of the with on their phosphorylation and To whether the of to dephosphorylate phospho-MPK3 and is a of phosphatase Arabidopsis MKP, was as a fusion and Although sequence similarity to AtMKP2, recombinant protein was to dephosphorylate either phospho-MPK3 or phospho-MPK6 recombinant was with to the Arabidopsis of the phosphatase was to this These results the that both MPK3 and MPK6 are direct and specific targets for AtMKP2 by with MPK3 and has been reported that the in vitro activity of mammalian MKPs is in the of their MAPK M. Nichols A. C. B. M. C. U. Arkinstall S. PubMed Scopus Google Scholar, D. X. M. R.J. Y. J. Biol. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). To the of Arabidopsis MAPKs on the catalytic activity of AtMKP2, recombinant in the and of recombinant MPK6, or The of either MPK3 or MPK6 significantly enhanced the phosphatase activity of whereas of the same of either recombinant or and on the The activation of AtMKP2 by with MPK3 or a in the of AtMKP2 for its in The of with MPK3 or MPK6 was to MAPK catalytic co-incubation of with of MPK3 and and in the same of of AtMKP2 phosphatase activity as been with the of AtMKP2 with as and of and of or in a AtMKP2 in the of MPK3 and MPK6 by ozone was reported to their to the in Arabidopsis R. J. M. R. Scheel D. Kangasjarvi J. Plant J. 2004; PubMed Scopus Google Scholar), a response that the activated MAPKs in close to potential target such as transcription R. Curr. Opin. Cell Biol. PubMed Scopus Google Scholar). AtMKP2 in dephosphorylation of and that this phosphatase be in the same To this question, generated plants fusion either a AtMKP2 and the AtMKP2 to or the AtMKP2 to control of the cauliflower mosaic virus of by with either predominantly in the nucleus, as by with the signal signal was plants with the same whereas plants displayed the and with the subcellular localization reported previously for protein Plant J. PubMed Scopus Google Scholar). These results that AtMKP2 is a MKP in Arabidopsis, which this regulator in the same subcellular as ozone-activated MPK3 and MPK6. AtMKP2-suppressed to an with the has been shown to both ROS accumulation M.A. H. M. K. J. Ellis B.E. Plant J. 2005; PubMed Scopus Google Scholar) and MPK3 and MPK6 activation (14Desikan R. Hancock J.T. Ichimura K. Shinozaki K. Neill S.J. Plant Physiol. 2001; 126: 1579-1587Crossref PubMed Scopus (197) Google Scholar) in plant to hypersensitive cell Because AtMKP2 appears to be with the control of cellular redox stress and and suppression of AtMKP2 expression the activation of MPK3 and MPK6 in response to oxidative whether loss of AtMKP2 also the response to with of of recombinant to the of plants response but to the of plants, the same rapid cell death and of AtMKP2 the of Arabidopsis plants to manage both oxidative stress and stress that is known to to ROS accumulation in the activation of one or both of the of MAPKs in plant cells is a response to a range of and that are also typically with ROS accumulation in the cells R. J. M. R. Scheel D. Kangasjarvi J. Plant J. 2004; PubMed Scopus Google Scholar, R. A. Hancock J.T. Neill S.J. 1999; PubMed Scopus Google Scholar). this it remains unclear the activity of these MAPKs is regulated in the of cellular the is by in to stress responses, MPK3 and/or MPK6 their putative are also in plant H. N. Y. Zhang S. Plant Cell. PubMed Scopus Google Scholar, J. M. A. F. J. D. Bogre L. F. Hirt H. J. 2002; PubMed Scopus Google Scholar) and signaling R. J. M. R. Scheel D. Kangasjarvi J. Plant J. 2004; PubMed Scopus Google Scholar) MAPK inactivation in can be catalyzed by of protein including protein phosphatases and phosphotyrosine phosphatases S.M. Curr. Opin. Cell Biol. 2000; PubMed Scopus Google Scholar). Because MAPK activation dual phosphorylation on both and the MAPK are to be the dual-specificity of the which have been designated MKPs (16Camps M. Nichols A. Arkinstall S. FASEB J. 2000; 14: 6-16Crossref PubMed Scopus (720) Google Scholar). The Arabidopsis genome encodes five MKPs and based on their catalytic domain sequence (18Kerk D. Bulgrien J. Smith D.W. Barsam B. Veretnik S. Gribskov M. Plant Physiol. 2002; 129: 908-925Crossref PubMed Scopus (214) Google Scholar), and of these have been implicated in biological of reported to to but to oxidant R. G.P. N. J. Genes 2001; PubMed Scopus Google Scholar), and to also be to levels in the that with MPK6 to a with MPK3 and in R. Ichimura K. T. T. X. Shinozaki K. J. J. 2002; PubMed Scopus Google Scholar). of displayed K. T. Plant Cell. 2004; 16: PubMed Scopus Google Scholar) and acid C. Y. C. R. Plant J. 2006; PubMed Scopus Google Scholar), whereas to and with plants M. B. Plant Cell. PubMed Scopus Google Scholar). has been to be of an Arabidopsis MAPK but in role for has been it remains whether the biological of in the and are in related to an of the to act as MKPs and dephosphorylate specific MAPKs. In the in of five putative Arabidopsis MKPs to that the family which have designated AtMKP2, both MPK3 and MPK6, and the of the plant to oxidative stress. The AtMKP2 appears to the of a cellular it is levels in Arabidopsis and and that expression is by either ozone or of the in the data The protein is more the essential phosphatase catalytic Although AtMKP2 is most closely related to amino acid sequence the catalytic the encoding these to have AtMKP2, expression is to the and in Arabidopsis In addition, the protein is to an that direct the protein to the and recombinant in vitro R. Y. J. S. Plant J. 16: PubMed Google Scholar), whereas AtMKP2 is localized to the and recombinant AtMKP2 is able to dephosphorylate MPK3 and MPK6, but and both in and in vitro data that AtMKP2 to regulation of the MPK3 and MPK6 activation it is that the activation of these MAPKs in AtMKP2-suppressed plants is related to the enhanced sensitivity of plants to activation of activation in mammalian cells has been reported to cell death M. Y. R. N. S. G. J. Biol. 2000; Full Text Full Text PDF PubMed Scopus Google Scholar) and activation of MPK3 and/or MPK6 also has been shown to be with cell death in plants (11Miles G.P. Samuel M.A. Zhang Y. Ellis B.E. Environ. Pollut. 2005; 138: 230-237Crossref PubMed Scopus (71) Google Scholar), but the loss of in AtMKP2-suppressed plants is normally to in plants that loss of AtMKP2 is also cellular in to MPK3 and MPK6 Because have been identified for this and in which AtMKP2 suppression has been it is that AtMKP2 activity is for regulation of either or through the of intracellular ROS Although the of MPK3 and MPK6 is in AtMKP2-suppressed plants, it is that the inactivation process is This that protein presumably to the MKPs, can in dephosphorylation of these MAPKs. In this it is that loss of in Arabidopsis only in stress sensitivity but also the of MPK6 activation by R. Ichimura K. T. T. X. Shinozaki K. J. J. 2002; PubMed Scopus Google Scholar), with the that may be of MPK6, in In a member of the of protein phosphatases was shown to be able to dephosphorylate the the -pTXpY- motif on a putative of Bogre L. W. J. M. K. G. Hirt H. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, A. A. C. H. Hirt H. J. Biol. Full Text Full Text PDF PubMed Scopus Google Scholar). MPK6 appears to only a in plant stress signaling but to be to regulation by The of recombinant AtMKP2 to dephosphorylate the in vitro to the of co-incubation of the phosphatase with its in MPK3 and MPK6. The activity of AtMKP2 was to be by such and this was of MAPK catalytic and of mammalian MKPs to their MAPKs was to significantly the in vitro phosphatase activity J. Physiol. Rev. 2001; PubMed Scopus Google Scholar, M. Nichols A. C. B. M. C. U. Arkinstall S. PubMed Scopus Google Scholar). The phosphatase activity of tobacco was also shown to be by co-incubation with tobacco MAPK of Arabidopsis whereas MAPK, protein kinase Arabidopsis MPK3 a S. H. S. K. Ohashi Y. J. Biol. 2006; Full Text Full Text PDF Scopus Google Scholar). of MKPs with their protein may the catalytic activity of MKPs in both and a to regulation of MKP for an about which is known the in In have shown that AtMKP2, the member of the putative MKP family in Arabidopsis, is a MAPK phosphatase that the to the Arabidopsis MPK3 and MPK6. The catalytic activity of AtMKP2 is enhanced in vitro by with its physiological MPK3 and MPK6, and evidence that AtMKP2 control the outcome of the cellular response to oxidant in The of in providing the M. Samuel of in providing the and H. of for of the recombinant is also for providing the and and J. G. for of the with

Fetched live from OpenAlex and de-inverted. Abstracts are not stored in this database: the inverted indexes are 8.6 GB of the frame’s 9.3 GB of text, and the host has 13 GB free.