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ZmMPK6, a Novel Maize MAP Kinase that Interacts with 14-3-3 Proteins

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Abstract

Although an increasing body of evidence indicates that plant MAP kinases are involved in a number of cellular processes, such as cell cycle regulation and cellular response to abiotic stresses, hormones and pathogen attack, very little is known about their biochemical properties and regulation mechanism. In this paper we report on the identification and characterization of a novel member of the MAP kinase family from maize, ZmMPK6. The amino acid sequence reveals a high degree of identity with group D plant MAP kinases. Recombinant ZmMPK6, expressed in Escherichia coli, is an active enzyme able to autophosphorylate. Remarkably, ZmMPK6 interacts in vitro with GF14-6, a maize 14-3-3 protein and the interaction is dependent on autophosphorylation. The interacting domain of ZmMPK6 is on the C-terminus and is comprised between amino acid 337 and amino acid 467. Our results represent the first evidence of an interaction between a plant MAP kinase and a 14-3-3 protein. Possible functional roles of this association in vivo are discussed.

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Abbreviations

ERK:

Extracellular-signal Regulated Kinase

GST:

glutathione S-transferase

MAPK:

mitogen-activated protein kinase

MAPKKK:

mitogen-activated protein kinase kinase kinase

MEK:

Mitogen-activated protein kinase/Extracellular signal-regulated kinase Kinase)

MHA2:

Maize H +-ATPase isoform 2

PAGE:

polyacrylamide gel electrophoresis

PVDF:

polyvinylidene fluoride

RT-PCR:

reverse transcriptase polimerase chain reaction

References

  • P. Aducci L. Camoni M. Marra S. Visconti (2002) ArticleTitleFrom cytosol to organelles: 14-3-3 proteins as multifunctional regulators of plant cell IUBMB Life 53 49–55 Occurrence Handle12018408

    PubMed  Google Scholar 

  • T. Berberich H. Sano T. Kusano (1999) ArticleTitleInvolvement of a MAP kinase, ZmMPK5, in senescence and recovery from␣low-temperature stress in maize Mol. Gen. Genet. 262 534–542 Occurrence Handle10.1007/s004380051115 Occurrence Handle10589842

    Article  PubMed  Google Scholar 

  • RA Bhat M. Riehl G. Santandrea R. Velasco S. Slocombe G. Donn H.H. Steinbiss R.D. Thompson H.A. Becker (2003) ArticleTitleAlteration of GCN5 levels in maize reveals dynamic responses to manipulating histone acetylation Plant J. 33 455–469 Occurrence Handle10.1046/j.1365-313X.2003.01642.x Occurrence Handle12581304

    Article  PubMed  Google Scholar 

  • M.M. Bradford (1976) ArticleTitleA rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein-dye binding Anal. Biochem. 72 248–254 Occurrence Handle942051

    PubMed  Google Scholar 

  • O. Calderini L. Bogre O. Vicente P. Binarova E. Heberle-Bors C. Wilson (1998) ArticleTitleA novel tobacco mitogen-activated protein (MAP) kinase kinase, NtMEK1, activates the cell cycle-regulated p43Ntf6 MAP kinase J. Cell Sci. 111 3091–3100 Occurrence Handle9739082

    PubMed  Google Scholar 

  • Y.H. Cheong B.C. Moon J.K. Kim C.Y. Kim I.H. Kim C.Y. Park J.C. Kim B.O. Park S.C. Koo H.W. Yoon W.S. Chung C.O. Lim S.Y. Lee M.J. Cho (2003) Plant Physiol. 132 1961–1972 Occurrence Handle10.1104/pp.103.023176 Occurrence Handle12913152

    Article  PubMed  Google Scholar 

  • I. Clark-Lewis J.S. Sanghera S.L. Pelech (1991) ArticleTitleDefinition of a consensus sequence for peptide substrate recognition by p44mpk, the meiosis-activated myelin basic protein kinase J. Biol. Chem. 266 15180–15184 Occurrence Handle1907971

    PubMed  Google Scholar 

  • M.H. Cobb E.J. Goldsmith (1995) ArticleTitleHow MAP kinases are regulated J. Biol. Chem. 270 14843–14846 Occurrence Handle10.1074/jbc.270.25.14843 Occurrence Handle7797459

    Article  PubMed  Google Scholar 

  • R.J. Davis (2000) ArticleTitleSignal transduction by the JNK group of MAP kinases Cell 103 239–252 Occurrence Handle10.1016/S0092-8674(00)00116-1 Occurrence Handle11057897

    Article  PubMed  Google Scholar 

  • G.R. Fanger C. Widmann A.C. Porter S. Sather G.L. Johnson R.R Vaillancourt (1998) ArticleTitle14-3-3 proteins interact with specific MEK kinases J. Biol. Chem. 273 3476–3483 Occurrence Handle10.1074/jbc.273.6.3476 Occurrence Handle9452471

    Article  PubMed  Google Scholar 

  • C. Finnie J. Borch D.B. Collinge (1999) ArticleTitle14-3-3 proteins: eukaryotic regulatory proteins with many functions Plant Mol. Biol. 40 545–554 Occurrence Handle10.1023/A:1006211014713 Occurrence Handle10480379

    Article  PubMed  Google Scholar 

  • H. Fu R.R. Subramanian S.C. Masters (2000) ArticleTitle14-3-3 proteins: structure, function and regulation Annu. Rev. Pharmacol. Toxicol. 40 617–647 Occurrence Handle10.1146/annurev.pharmtox.40.1.617 Occurrence Handle10836149

    Article  PubMed  Google Scholar 

  • A.T. Fuglsang S. Visconti K. Drumm T. Jahn A. Stensballe B. Mattei O.N. Jensen P. Aducci M.G. Palmgren (1999) ArticleTitleBinding of 14-3-3 protein to the plasma membrane H+-ATPase AHA2 involves the three Cterminal residues Tyr(946)-Thr-Val and requires phosphorylation of Thr(947) J. Biol. Chem. 274 36774–36780 Occurrence Handle10.1074/jbc.274.51.36774 Occurrence Handle10593986

    Article  PubMed  Google Scholar 

  • M.R. Fullone S. Visconti M. Marra V. Fogliano P. Aducci (1998) ArticleTitleFusicoccin effect on the in vitro interaction between plant 14-3-3 proteins and plasma membrane H+-ATPase J. Biol. Chem. 273 7698–7702 Occurrence Handle10.1074/jbc.273.13.7698 Occurrence Handle9516476

    Article  PubMed  Google Scholar 

  • R. Gupta Y. Huang J. Kieber S. Luan (1998) ArticleTitleIdentification of a dual specificity protein phosphatase that inactivates a MAP kinase from Arabidopsis Plant J. 16 581–589 Occurrence Handle10.1046/j.1365-313x.1998.00327.x Occurrence Handle10036776

    Article  PubMed  Google Scholar 

  • Y. Huang H. Li R. Gupta P.C. Morris S. Luan J.J. Kieber (2000) ArticleTitleATMPK4, an Arabidopsis homolog of mitogen-activated protein kinase, is activated in vitro by AtMEK1 through threonine phosphorylation Plant Physiol. 122 1301–1310 Occurrence Handle10.1104/pp.122.4.1301 Occurrence Handle10759527

    Article  PubMed  Google Scholar 

  • K. Ichimura T. Mizoguchi R. Yoshida T. Yuasa K. Shinozaki (2000) ArticleTitleVarious abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6 Plant J. 24 655–665 Occurrence Handle10.1046/j.1365-313x.2000.00913.x Occurrence Handle11123804

    Article  PubMed  Google Scholar 

  • K. Ichimura K. Shinozaki G. Tena J. Sheen H. Henry A. Champion M. Kreis S. Zhang H. Hirt C. Wilson E. Heberle-Bors B.E. Ellis P.C. Morris R.W. Innes J.R. Ecker D. Scheel D.F. Klessig Y. Machida J. Mundi Y. Ohashi J.C. Walker (2002) ArticleTitleMitogen-activated protein kinase cascades in plants: a new nomenclature Trends Plant Sci. 7 301–308 Occurrence Handle10.1016/S1360-1385(02)02302-6 Occurrence Handle12119167

    Article  PubMed  Google Scholar 

  • D. Igarashi S. Ishida J. Fukazawa Y. Takashi (2001) ArticleTitle14-3-3 proteins regulate intracellular localization of the bZIP␣transcriptional activator RSG Plant Cell 13 2483–2497 Occurrence Handle10.1105/tpc.13.11.2483 Occurrence Handle11701883

    Article  PubMed  Google Scholar 

  • C. Jonak S. Kiegerl W. Ligterink P.J. Barker N.S. Huskinsson H. Hirt (1996) ArticleTitleStress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought Proc. Natl. Acad. Sci. USA 93 11274–11279 Occurrence Handle10.1073/pnas.93.20.11274 Occurrence Handle8855346

    Article  PubMed  Google Scholar 

  • C. Jonak L. Okresz L. Bogre H. Hirt (2002) ArticleTitleComplexity, cross talk and integration of plant MAP kinase signalling Curr. Opin. Plant Biol. 5 415–424 Occurrence Handle10.1016/S1369-5266(02)00285-6 Occurrence Handle12183180

    Article  PubMed  Google Scholar 

  • J.J. Kieber M. Rothenberg G. Roman K.A. Feldmann J.R. Ecker (1993) ArticleTitleCTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases Cell 72 427–441 Occurrence Handle10.1016/0092-8674(93)90119-B Occurrence Handle8431946

    Article  PubMed  Google Scholar 

  • N.O. Ku J. Liao M.B. Omary (1998) ArticleTitlePhosphorylation of human keratin 18 serine 33 regulates binding to 14-3-3 proteins EMBO J. 17 1892–1906 Occurrence Handle10.1093/emboj/17.7.1892 Occurrence Handle9524113

    Article  PubMed  Google Scholar 

  • D. Kultz (1998) ArticleTitlePhylogenetic and functional classification of mitogen and stress-activated protein kinases J. Mol. Evol. 46 571–588 Occurrence Handle9545468

    PubMed  Google Scholar 

  • U.K. Laemmli (1970) ArticleTitleCleavage of the structural proteins during the assembly of the head of the bacteriophage T4 Nature 277 680–685 Occurrence Handle10.1038/227680a0

    Article  Google Scholar 

  • Y.C. Liu Y. Liu C. Elli H. Yoshida S. Lipkowitz A. Altman (1997) ArticleTitleSerine phosphorylation of Cbl induced by phorbol ester enhances its association with 14-3-3 proteins in T cells via a novel serine-rich 14-3-3-binding motif J. Biol. Chem. 272 9979–9985 Occurrence Handle10.1074/jbc.272.15.9979 Occurrence Handle9092538

    Article  PubMed  Google Scholar 

  • K. Mockaitis S.H. Howell (2000) ArticleTitleAuxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings Plant J. 24 785–796 Occurrence Handle10.1046/j.1365-313x.2000.00921.x Occurrence Handle11135112

    Article  PubMed  Google Scholar 

  • A.J. Muslin J.W. Tanner P.M. Allen A.S. Shaw (1996) ArticleTitleInteraction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine Cell 84 889–897 Occurrence Handle10.1016/S0092-8674(00)81067-3 Occurrence Handle8601312

    Article  PubMed  Google Scholar 

  • F. Ouaked W. Rozhon D. Lecourieux H. Hirt (2003) ArticleTitleA MAPK pathway mediates ethylene signaling in plants EMBO J. 22 1282–1288 Occurrence Handle10.1093/emboj/cdg131 Occurrence Handle12628921

    Article  PubMed  Google Scholar 

  • W.R. Pearson (1990) ArticleTitleRapid and sensitive sequence comparison␣with FASTP and FASTA Method. Enzymol. 183 63–98

    Google Scholar 

  • R.L. Roberts H.U. Mosch G.R. Fink (1997) ArticleTitle14-3-3 proteins are essential for RAS/MAPK cascade signaling during pseudohyphal development in S. cerevisiae Cell 89 1055–1065 Occurrence Handle10.1016/S0092-8674(00)80293-7 Occurrence Handle9215628

    Article  PubMed  Google Scholar 

  • M.J. Robinson M.H. Cobb (1997) ArticleTitleMitogen-activated protein kinase pathways Curr. Opin. Cell Biol. 9 180–186 Occurrence Handle10.1016/S0955-0674(97)80061-0 Occurrence Handle9069255

    Article  PubMed  Google Scholar 

  • F. Song R.M. Goodman (2002) ArticleTitleOsBIMK1, a rice MAP kinase gene involved in disease resistance responses Planta 215 997–1005 Occurrence Handle10.1007/s00425-002-0794-5 Occurrence Handle12355160

    Article  PubMed  Google Scholar 

  • G. Tena T. Asai W.L. Chiu J. Sheen (2001) ArticleTitlePlant mitogen-activated protein kinase signaling cascades Curr. Opin. Plant Biol. 4 392–400 Occurrence Handle10.1016/S1369-5266(00)00191-6 Occurrence Handle11597496

    Article  PubMed  Google Scholar 

  • J.D. Thompson D.G. Higgins T.J. Gibson (1994) ArticleTitleCLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucl. Acids Res. 22 4673–4680 Occurrence Handle7984417

    PubMed  Google Scholar 

  • G. Tzivion J. Avruch (2002) ArticleTitle14-3-3 proteins: active cofactors in cellular regulation by serine/threonine phosphorylation J. Biol. Chem. 277 3061–3064 Occurrence Handle10.1074/jbc.R100059200 Occurrence Handle11709560

    Article  PubMed  Google Scholar 

  • M.J. Hemert Particlevan H.Y. Steensma G.P.H. Heusden Particlevan (2001) ArticleTitle14-3-3 proteins: key regulator of cell division, signalling and apoptosis BioEssays 23 936–946 Occurrence Handle10.1002/bies.1134 Occurrence Handle11598960

    Article  PubMed  Google Scholar 

  • S. Visconti L. Camoni M.R. M. Fullone Lalle M. Marra P. Aducci (2003) ArticleTitleMutational analysis of the interaction between 14-3-3 proteins and plant plasma membrane H+-ATPase J. Biol. Chem. 278 8172–8178 Occurrence Handle10.1074/jbc.M211039200 Occurrence Handle12509351

    Article  PubMed  Google Scholar 

  • C.R. Weston R.J. Davis (2002) ArticleTitleThe JNK signal transduction pathway Curr. Opin. Genet. Dev. 12 14–21 Occurrence Handle10.1016/S0959-437X(01)00258-1 Occurrence Handle11790549

    Article  PubMed  Google Scholar 

  • H. Xing S. Zhang C. Weinheimer A. Kovacs A.J. Muslin (2000) ArticleTitle14-3-3 proteins block apoptosis and differentially regulate MAPK cascades EMBO J. 19 349–358 Occurrence Handle10.1093/emboj/19.3.349 Occurrence Handle10654934

    Article  PubMed  Google Scholar 

  • M.B. Yaffe K. Rittinger S. Volinia P.R. Caron A. Aitken H. Leffers S.J. Gamblin S.J. Smerdon L.C. Cantley (1997) ArticleTitleThe structural basis for 14-3-3: phosphopeptide binding specificity Cell 91 961–971 Occurrence Handle10.1016/S0092-8674(00)80487-0 Occurrence Handle9428519

    Article  PubMed  Google Scholar 

  • S. Zhang D.F. Klessig (2001) ArticleTitleMAPK cascades in plant defense signaling Trends Plant Sci. 6 520–527 Occurrence Handle10.1016/S1360-1385(01)02103-3 Occurrence Handle11701380

    Article  PubMed  Google Scholar 

  • Q. Zheng G. Yin C. Yan M. Cavet B.C. Berk (2004) ArticleTitle14-3-3beta binds to big mitogen-activated protein kinase 1 (BMK1/ERK5) and regulates BMK1 function J. Biol. Chem. 279 8787–8791 Occurrence Handle10.1074/jbc.M310212200 Occurrence Handle14679215

    Article  PubMed  Google Scholar 

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Author notes

  1. Riccardo Velasco

    Present address: Istituto Agrario San Michele all’Adige, via Mach 1, 38010, San Michele a/Adige, (TN), Italy

Authors and Affiliations

  1. Department of Biology, University of Rome “Tor Vergata”, via della Ricerca Scientifica, 100133, Rome, Italy

    Marco Lalle, Sabina Visconti, Lorenzo Camoni & Patrizia Aducci

  2. Department of Infectious, Parasitic and Immuno-mediated Diseases, Istituto Superiore di Sanita’, Viale Regina Elena 299, 00161, Rome, Italy

    Marco Lalle

  3. Department of Biological and Environmental Studies, University of Sannio, via Port’Arsa 11, 82100, Benevento, Italy

    Mauro Marra

  4. Max Planck Institut fuer Zuechtungsforschung, Carl-von-Linne-Weg 10, 50829, Koeln, Germany

    Riccardo Velasco

Authors
  1. Marco Lalle
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  2. Sabina Visconti
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  3. Mauro Marra
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  4. Lorenzo Camoni
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  6. Patrizia Aducci
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Correspondence to Patrizia Aducci.

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Lalle, M., Visconti, S., Marra, M. et al. ZmMPK6, a Novel Maize MAP Kinase that Interacts with 14-3-3 Proteins. Plant Mol Biol 59, 713–722 (2005). https://doi.org/10.1007/s11103-005-0862-x

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