Plant Biol (Stuttg) 2000; 2(1): 11-16
DOI: 10.1055/s-2000-9458
Original Paper
Georg Thieme Verlag Stuttgart ·New York

A Phosphopeptide Corresponding to the Cytosolic Stretch Connecting Transmembrane Segments 8 and 9 of the Plasma Membrane H+-ATPase Binds 14-3-3 Proteins and Inhibits Fusicoccin-Induced Activation of the H+-ATPase

M. Marra 1 , C. Olivari 2 , Sabina Visconti 3 , Cristina Albumi 2 , Patrizia Aducci 3 , Maria Ida De Michelis 2
  • 1 Università degli Studi del Sannio, Facoltà di Scienze M F N, Benevento, Italy
  • 2 Dipartimento di Biologia, Università di Milano, Centro di Studio del CNR per la Biologia Cellulare e Molecolare delle Piante, Milano, Italy
  • 3 Università di Roma “Tor Vergata” Via della Ricerca Scientifica, Roma, Italy
Further Information

Publication History

August 5, 1999

November 5, 1999

Publication Date:
31 December 2000 (online)

Abstract:

A putative consensus domain for binding of 14-3-3 proteins to the plasma membrane (PM) H+-ATPase was identified in the highly-conserved sequence RSR(p)SWSF [where (p)S is Ser776 of the maize isoform MHA2], localized in the cytosolic stretch connecting transmembrane segments 8 and 9. A 15 amino acid biotinylated phosphopeptide comprising this motif: i) bound a recombinant 14-3-3 protein, ii) inhibited fusicoccin-induced stimulation of the PM H+-ATPase activity both in PM isolated from germinating radish (Raphanus sativus L.) seedlings and in ER isolated from Saccharomyces cerevisiae expressing AHA1 (an isoform of Arabidopsis thaliana PM H+-ATPase), and iii) inhibited fusicoccin binding to PM isolated from germinating radish seedlings. The corresponding non-phosphorylated peptide was inactive in all the performed assays. Together, these results suggest that the cytosolic strand connecting transmembrane segments 8 and 9 of the PM H+-ATPase is a 14-3-3 binding site which might cooperate with the C-terminal domain of the’enzyme in generating a stable association between the H+-ATPase and 14-3-3 protein.

Abbreviations:

Brij 58: polyoxyethylene 20 cetyl ether BTP: bis-tris propane (1,3-bis[tris(hydroxymethyl)methylamino]propane) FC: fusicoccin HEPES: 4-(2-hydroxymethyl)-1-piperazineethanesulfonic acid MES: 2-(N-morpholino)ethanesulfonic acid MOPS: 3-(N-morpholino)propanesulfonic acid PM: plasma membrane

References

  • 01 Aducci,  P.,, Marra,  M.,, Fogliano,  V.,, and Fullone,  M. R.. (1995);  Fusicoccin receptors: perception and transduction of the fusicoccin signal.  J. Exp. Bot.. 46 1463-1478
  • 02 Aitken,  A.. (1996);  14-3-3 and its possible role in coordinating multiple signalling pathways.  Trends in Cell Biol.. 6 341-347
  • 03 Baunsgaard,  L.,, Fuglsang,  A. T.,, Jahn,  T.,, Korthout,  H. A. A. J.,, de Boer,  A. H.,, and Palmgren,  M. G.. (1998);  The 14-3-3 proteins associate with the plant plasma membrane H+-ATPase to generate a fusicoccin binding complex and a fusicoccin responsive system.  Plant J.. 13 661-671
  • 04 Cocucci,  M. C., and Marrè,  E.. (1991);  Co-sedimentation of one form of plasma membrane proton-ATPase and of the fusicoccin receptor from radish microsomes.  Plant Sci.. 73 45-49
  • 05 De Michelis,  M. I.,, Rasi-Caldogno,  F.,, Pugliarello,  M. C.,, and Olivari,  C.. (1991);  Fusicoccin binding to its plasma membrane receptor and the activation of the plasma membrane H+-ATPase. II. Stimulation of the H+-ATPase in a plasma membrane fraction purified by phase partitioning.  Bot. Acta. 104 265-271
  • 06 De Michelis,  M. I.,, Rasi-Caldogno,  F.,, Pugliarello,  M. C.,, and Olivari,  C.. (1996);  Fusicoccin binding to its plasma membrane receptor and the activation of the plasma membrane H+-ATPase. III. Is there a direct interaction between the fusicoccin receptor and the plasma membrane H+-ATPase?.  Plant Physiol.. 110 957-964
  • 07 De Michelis,  M. I., and Spanswick,  R. M.. (1986);  H+-pumping driven by the vanadate-sensitive ATPase in membrane vesicles from corn roots.  Plant Physiol.. 81 542-547
  • 08 Fullone,  M. R.,, Visconti,  S.,, Marra,  M.,, Fogliano,  V.,, and Aducci,  P.. (1998);  Fusicoccin effect on the in vitro interaction between plant 14-3-3 proteins and plasma membrane H+-ATPase.  J. Biol. Chem.. 273 7698-7702
  • 09 Jahn,  T.,, Fuglsang,  A. T.,, Drumm,  K.,, and Palmgren,  M. G.. (1998) Multiple interaction of 14-3-3 proteins with the plant plasma membrane H+-ATPase. Proceedings of the 11th International Workshop on Plant Membrane Biology. Tester, M., Morris, C., and Davies, J., eds. Cambridge, UK; 24
  • 10 Jahn,  T.,, Fuglsang,  A. T.,, Olsson,  A.,, Bruntrup,  I. M.,, Collinge,  D. B.,, Volkmann,  D.,, Sommarin,  M.,, Palmgren,  M. G.,, and Larsson,  C.. (1997);  The 14-3-3 protein interacts directly with the C-terminal region of the plant plasma membrane H+-ATPase.  Plant Cell. 9 1805-1814
  • 11 Johansson,  F.,, Sommarin,  M.,, and Larsson,  C.. (1993);  Fusicoccin activates the plasma membrane H+-ATPase by a mechanism involving the C-terminal inhibitory domain.  Plant Cell. 5 321-327
  • 12 Korthout,  H. A. A. J., and de Boer,  A. H.. (1994);  A fusicoccin binding protein belongs to the family of 14-3-3 brain protein homologs.  Plant Cell. 6 1681-1692
  • 13 Lanfermeijer,  F. C., and Prins,  H. B. A.. (1994);  Modulation of H+-ATPase activity by fusicoccin in plasma membrane vesicles from oat (Avena sativa L.) roots.  Plant Physiol.. 104 1277-1285
  • 14 Markwell,  M. A. K.,, Haas,  S. M.,, Bieber,  L. L.,, and Tolbert,  N. E.. (1978);  A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples.  Anal. Biochem.. 87 206-210
  • 15 Marra,  M.,, Fullone,  M. R.,, Fogliano,  V.,, Pen,  J.,, Mattei,  M.,, Masi,  S.,, and Aducci,  P.. (1994);  The 30-kilodalton protein present in purified fusicoccin receptor preparations is a 14-3-3-like protein.  Plant Physiol.. 106 1497-1501
  • 16 Marré,  E.. (1979);  Fusicoccin: a tool in plant physiology.  Annu. Rev. Plant Physiol.. 30 273-288
  • 17 Marré,  E.,, Bellando,  M.,, Beffagna,  N.,, Marré,  M. T.,, Romani,  G.,, and Vergani,  P.,. (1992) Synergisms, additive and non-additive factors regulating proton extrusion and intracellular pH. Current Topics in Plant Biochemistry and Physiology. Sharp, R., Novacky, A. J., and Randall, D. D., eds. 11: 230
  • 18 Muslin,  A. J.,, Tanner,  J. W.,, Allen,  P. M.,, and Shaw,  A. S.. (1996);  Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine.  Cell. 84 889-897
  • 19 Oecking,  C.,, Eckerskorn,  C.,, and Weiler,  E. W.. (1994);  The fusicoccin receptor of plants is a member of the 14-3-3 superfamily of eukaryotic regulatory proteins.  FEBS Lett.. 352 163-166
  • 20 Oecking,  C., and Hagemann,  K.. (1999);  Association of 14-3-3 proteins with the C-terminal autoinhibitory domain of the plant plasma membrane H+-ATPase generates a fusicoccin-binding complex.  Planta. 207 480-482
  • 21 Oecking,  C.,, Piotrowski,  M.,, Hagermeier,  J.,, and Hagemann,  K.. (1997);  Topology and target interaction of the fusicoccin-binding 14-3-3 homologs of Commelina communis. .  Plant J.. 12 441-453
  • 22 Olivari,  C.,, Meanti,  C.,, De Michelis,  M. I.,, and Rasi-Caldogno,  F.. (1998);  Fusicoccin binding to its plasma membrane receptor and the activation of the plasma membrane H+-ATPase. IV. Fusicoccin induces the association between the plasma membrane H+-ATPase and the fusicoccin receptor.  Plant Physiol.. 116 529-537
  • 23 Olsson,  A.,, Svennelid,  F.,, Ek,  B.,, Sommarin,  M.,, and Larsson,  C.. (1998);  A phosphothreonine residue at the C-terminal end of the plasma membrane H+-ATPase is protected by fusicoccin-induced 14-3-3 binding.  Plant Physiol.. 118 551-555
  • 24 Palmgren,  M. G.. (1990);  An H+-ATPase assay: proton pumping and ATPase activity determined simultaneously in the same sample.  Plant Physiol.. 94 882-886
  • 25 Palmgren,  M. G.. (1998);  Proton gradients and plant growth: role of the plasma membrane H+-ATPase.  Advances Botanical Research. 28 1-70
  • 26 Palmgren,  M. G., and Christensen,  G.. (1994);  Functional comparisons between plant plasma membrane H+-ATPase isoforms expressed in yeast.  J. Biol. Chem.. 269 3027-3033
  • 27 Palmgren,  M. G.,, Larsson,  C.,, and Sommarin,  M.. (1990);  Proteolytic activation of the plant plasma membrane H+-ATPase by removal of a terminal segment.  J. Biol. Chem.. 265 13423-13426
  • 28 Palmgren,  M. G.,, Sommarin,  M.,, Serrano,  R.,, and Larsson,  C.. (1991);  Identification of an autoinhibitory domain in the C-terminal region of the plant plasma membrane H+-ATPase.  J. Biol. Chem.. 266 20470-20475
  • 29 Pesci,  P.,, Cocucci,  S. M.,, and Randazzo,  G.. (1979);  Characterization of fusicoccin binding to receptor sites on cell membranes of maize coleoptile tissues.  Plant Cell Environ.. 2 205-209
  • 30 Piotrowsky,  M.,, Morsomme,  P.,, Boutry,  M.,, and Oecking,  C.. (1998);  Complementation of the Saccharomyces cerevisiae plasma membrane H+-ATPase by a plant H+-ATPase gene generates a highly abundant fusicoccin binding site.  J. Biol. Chem.. 273 30018-30023
  • 31 Rasi-Caldogno,  F.,, Carnelli,  A.,, and De Michelis,  M. I.. (1995);  Identification of the plasma membrane Ca2+-ATPase and its autoinhibitory domain.  Plant Physiol.. 108 105-113
  • 32 Rasi-Caldogno,  F., and Pugliarello,  M. C.. (1985);  Fusicoccin stimulates the H+-ATPase of plasmalemma in isolated membrane vesicles from radish.  Biochem. Biophys. Res. Comm.. 133 280-285
  • 33 Rasi-Caldogno,  F.,, Pugliarello,  M. C.,, Olivari,  C.,, and De Michelis,  M. I.. (1993);  Controlled proteolysis mimics the effect of fusicoccin on the plasma membrane H+-ATPase.  Plant Physiol.. 103 391-398
  • 34 Regenberg,  B.,, Villalba,  J. M.,, Lanfermeijer,  F. C.,, and Palmgren,  M. G.. (1995);  C-Terminal deletion analysis of plant plasma membrane H+-ATPase : yeast as a model for solute transport across the plasma membrane.  Plant Cell. 7 1655-1666
  • 35 Villalba,  J. M.,, Palmgren,  M. G.,, Berberian,  G. E.,, Ferguson,  C.,, and Serrano,  R.. (1992);  Functional expression of plant plasma membrane H+-ATPase in yeast endoplasmic reticulum.  J. Biol. Chem.. 267 12341-12349
  • 36 Yaffe,  M. B.,, Rittinger,  K.,, Volinia,  S.,, Caron,  P. R.,, Aitken,  A.,, Leffers,  H.,, Gamblin,  S. J.,, Smerdon,  S. K.,, and Cantley,  L. C.. (1997);  The structural basis for 14-3-3:phosphopeptide binding specificity.  Cell. 91 961-971

Maria Ida De
Michelis

Dipartimento di Biologia „L. Gorini” Università di Milano

via G. Celoria 26

20133 Milano

Italy

Section Editor: U. Lüttge

Email: midemic@mailserver.unimi.it

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