User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

The two major plant plasma membrane H+-ATPases display different regulatory properties.

Primary tabs

Dambly, S Boutry, Marc [UCL]

The major plant plasma membrane H(+)-ATPases fall into two gene categories, subfamilies I and II. However, in many plant tissues, expression of the two subfamilies overlaps, thus precluding individual characterization. Yeast expression of PMA2 and PMA4, representatives of the two plasma membrane H(+)-ATPase subfamilies in Nicotiana plumbaginifolia, has previously shown that (i) the isoforms have distinct enzymatic properties and that (ii) PMA2 is regulated by phosphorylation of its penultimate residue (Thr) and binds regulatory 14-3-3 proteins, resulting in the displacement of the autoinhibitory C-terminal domain. To obtain insights into regulatory differences between the two subfamilies, we have constructed various chimeric proteins in which the 110-residue C-terminal-encoding region of PMA2 was progressively substituted by the corresponding sequence from PMA4. The PMA2 autoinhibitory domain was localized to a region between residues 851 and 915 and could not be substituted by the corresponding region of PMA4. In contrast to PMA2, PMA4 was poorly phosphorylated at its penultimate residue (Thr) and bound 14-3-3 proteins weakly. The only sequence difference around the phosphorylation site is located two residues upstream of the phosphorylated Thr. It is Ser in PMA2 (as in most members of subfamily I) and His in PMA4 (as in most members of subfamily II). Substitution of His by Ser in PMA4 resulted in an enzyme showing increased phosphorylation status, 14-13-3 binding, and ATPase activity, as well as improved yeast growth. The reverse substitution of Ser by His in PMA2 resulted in the failure of this enzyme to complement the absence of yeast H(+)-ATPases. These results show that the two plant H(+)-ATPase subfamilies differ functionally in their regulatory properties.

Document type Article de périodique (Journal article) – Article de recherche – Journal Article, Research Support, Non-U.S. Gov't
Access type Accès restreint
Publication date 2001
Language Anglais
Journal information "The Journal of biological chemistry" - Vol. 276, no. 10, p. 7017-22 (2001)
Peer reviewed yes
issn 0021-9258
Publication status Publié
Affiliation UCL - AGRO/CABI - Département de chimie appliquée et des bio-industries
MESH Subject 14-3-3 Proteins ; Adenosine Triphosphatases - metabolism ; Amino Acid Sequence ; Binding Sites ; Blotting, Western ; Cell Membrane - enzymology ; Electrophoresis, Polyacrylamide Gel ; Fungal Proteins - chemistry ; Histidine - chemistry ; Molecular Sequence Data ; Multigene Family ; Mutation ; Phosphorylation ; Plant Proteins - chemistry ; Plants - enzymology ; Plants, Toxic ; Plasmids - metabolism ; Protein Binding ; Protein Isoforms ; Protein Structure, Tertiary ; Proton-Translocating ATPases - chemistry - metabolism ; Recombinant Fusion Proteins - metabolism ; Saccharomyces cerevisiae Proteins ; Sequence Homology, Amino Acid ; Serine - chemistry ; Threonine - chemistry ; Tobacco - genetics ; Tyrosine 3-Monooxygenase - chemistry - metabolism
Links
  1. Palmgren, J. Biol. Chem., 266, 20470 (1991)
  2. Sussman M R, Molecular Analysis of Proteins in the Plant Plasma Membrane, 10.1146/annurev.pp.45.060194.001235
  3. Olsson Anne, Svennelid Fredrik, Ek Bo, Sommarin Marianne, Larsson Christer, A Phosphothreonine Residue at the C-Terminal End of the Plasma Membrane H+-ATPase Is Protected by Fusicoccin-Induced 14–3–3 Binding, 10.1104/pp.118.2.551
  4. Finnie Christine, Borch Jonas, Collinge David B., 10.1023/a:1006211014713
  5. Regenberg B., C-Terminal Deletion Analysis of Plant Plasma Membrane H+-ATPase: Yeast as a Model System for Solute Transport across the Plant Plasma Membrane, 10.1105/tpc.7.10.1655
  6. Axelsen K. B., Venema K., Jahn T., Baunsgaard L., Palmgren M. G., Molecular Dissection of the C-Terminal Regulatory Domain of the Plant Plasma Membrane H+-ATPase AHA2:  Mapping of Residues that When Altered Give Rise to an Activated Enzyme†, 10.1021/bi982482l
  7. Morsomme, EMBO J., 15, 5513 (1996)
  8. Morsomme Pierre, Dambly Stéphanie, Maudoux Olivier, Boutry Marc, Single Point Mutations Distributed in 10 Soluble and Membrane Regions of theNicotiana plumbaginifoliaPlasma Membrane PMA2 H+-ATPase Activate the Enzyme and Modify the Structure of the C-terminal Region, 10.1074/jbc.273.52.34837
  9. Maudoux Olivier, Batoko Henri, Oecking Claudia, Gevaert Kris, Vandekerckhove Joel, Boutry Marc, Morsomme Pierre, A Plant Plasma Membrane H+-ATPase Expressed in Yeast Is Activated by Phosphorylation at Its Penultimate Residue and Binding of 14-3-3 Regulatory Proteins in the Absence of Fusicoccin, 10.1074/jbc.m909690199
  10. Sikorski, Genetics, 122, 19 (1989)
  11. Treco, Current Protocols in Molecular Biology, 2, 13.1.1 (1994)
  12. Palmgren Michael Gjedde, Harper Jeffrey F., Pumping with plant P-type ATPases, 10.1093/jxb/50.special_issue.883
  13. Fuglsang Anja T., Visconti Sabina, Drumm Katrine, Jahn Thomas, Stensballe Allan, Mattei Benedetta, Jensen Ole N., Aducci Patrizia, Palmgren Michael G., Binding of 14-3-3 Protein to the Plasma Membrane H+-ATPase AHA2 Involves the Three C-terminal Residues Tyr946-Thr-Val and Requires Phosphorylation of Thr947, 10.1074/jbc.274.51.36774
  14. Svennelid F., Phosphorylation of Thr-948 at the C Terminus of the Plasma Membrane H+-ATPase Creates a Binding Site for the Regulatory 14-3-3 Protein, 10.1105/tpc.11.12.2379
  15. Holtman Wessel L., Roberts Michael R., Oppedijk Berry J., Testerink Christa, van Zeijl Mieke J., Wang Mei, 14-3-3 proteins interact with a 13-lipoxygenase, but not with a 9-lipoxygenase, 10.1016/s0014-5793(00)01575-1
  16. Muslin Anthony J, Tanner J.William, Allen Paul M, Shaw Andrey S, Interaction of 14-3-3 with Signaling Proteins Is Mediated by the Recognition of Phosphoserine, 10.1016/s0092-8674(00)81067-3
  17. Yaffe Michael B, Rittinger Katrin, Volinia Stefano, Caron Paul R, Aitken Alastair, Leffers Henrik, Gamblin Steven J, Smerdon Stephen J, Cantley Lewis C, The Structural Basis for 14-3-3:Phosphopeptide Binding Specificity, 10.1016/s0092-8674(00)80487-0
  18. Kinoshita T., Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells, 10.1093/emboj/18.20.5548
  19. Zhao R., Cosuppression of a Plasma Membrane H+-ATPase Isoform Impairs Sucrose Translocation, Stomatal Opening, Plant Growth, and Male Fertility, 10.1105/tpc.12.4.535
  20. Camoni Lorenzo, Iori Valentina, Marra Mauro, Aducci Patrizia, Phosphorylation-dependent Interaction between Plant Plasma Membrane H+-ATPase and 14-3-3 Proteins, 10.1074/jbc.275.14.9919
  21. Morsomme Pierre, Boutry Marc, The plant plasma membrane H+-ATPase: structure, function and regulation, 10.1016/s0005-2736(00)00128-0
  22. Moriau Luc, Michelet Baudouin, Bogaerts Pierre, Lambert Laurence, Michel Alain, Oufattole Mohammed, Boutry Marc, Expression analysis of two gene subfamilies encoding the plasma membrane H+-ATPase in Nicotiana plumbaginifolia reveals the major transport functions of this enzyme, 10.1046/j.1365-313x.1999.00495.x
  23. Oufattole Mohammed, Arango Miguel, Boutry Marc, Identification and expression of three new Nicotiana plumbaginifolia genes which encode isoforms of a plasma-membrane H + -ATPase, and one of which is induced by mechanical stress, 10.1007/s004250050672
  24. Ewing N. N., Bennett A. B., Assessment of the Number and Expression of P-Type H+-ATPase Genes in Tomato, 10.1104/pp.106.2.547
  25. Palmgren, J. Biol. Chem., 269, 3027 (1994)
  26. d'Exaerde Alban de Kerchove, Supply Philip, Dufour Jean-Pierre, Bogaerts Pierre, Thinès Denyse, Goffeau André, Boutry Marc, Functional Complementation of a Null Mutation of the YeastSaccharomyces cerevisiaePlasma Membrane H+-ATPase by a Plant H+-ATPase Gene, 10.1074/jbc.270.40.23828
  27. Luo Hong, Morsomme Pierre, Boutry Marc, The Two Major Types of Plant Plasma Membrane H+-ATPases Show Different Enzymatic Properties and Confer Differential pH Sensitivity of Yeast Growth, 10.1104/pp.119.2.627
Bibliographic reference Dambly, S ; Boutry, Marc. The two major plant plasma membrane H+-ATPases display different regulatory properties.. In: The Journal of biological chemistry, Vol. 276, no. 10, p. 7017-22 (2001)
Permanent URL http://hdl.handle.net/2078.1/8685