Advertisement

Journal of Plant Research

, Volume 109, Issue 1, pp 119–125 | Cite as

Proton pumps of the vacuolar membrane in growing plant cells

  • Masayoshi Maeshima
  • Yoichi Nakanishi
  • Chie Matsuura-Endo
  • Yoshiyuki Tanaka
JPR Symposium

Abstract

Plant growth results from the division, enlargement and specialization of cells. The two processes of the enlargement and the differentiation of cells are not spatially separated in plant tissue. We focus our attention here on the enlargement and elongation of cells. In most cases, growing plant cells contain a large central vacuole. The acid growth theory is based on the space-filling function of the large vacuole. The active transport systems in the vacuolar membrane are essential for maintenance of high osmotic pressure and for the expansion of the vacuole. The secondary active transport systems of the vacuole for sugars and ions are driven by the proton-motive force which is generated by the vacuolar H+-ATPase and H+-translocating inorganic pyrophosphatase. In this review, the relationship between cell elongation and these enzymes of the vacuolar membrane is emphasized.

Key words

Cell elongation H+-ATPase H+-Pyrophosphatase Proton pump Vacuole Vigna radiata Water channel 

Abbreviations

kD

kilodalton

H+-PPase

proton-translocating inorganic pyrophosphatase

PPi

inorganic pyrophosphate

TIP

tonoplast intrinsic protein

VM23

an integral membrane protein of the radish vacuole with a molecular mass of 23 kD.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baltscheffsky, M. andNyrén, P. 1984. The synthesis and utilization of inorganic pyrophosphate.In L. Ernster, ed., New Comprehensive Biochemistry: Bioenergetics, vol. 9. Elsevier, Amsterdam, pp. 187–206.Google Scholar
  2. Boller, T. andWiemken, A. 1986. Dynamics of vacuolar compartmentation. Annu. Rev. Plant Physiol.37: 137–164.CrossRefGoogle Scholar
  3. Chrispeels, M.J. andAgre, P. 1994. Aquaporins: water channel proteins of plant and animal cells. Trends Biochem. Sci.19: 421–425.CrossRefPubMedGoogle Scholar
  4. Hager, A., Menzel, H. andKrauss, A. 1971. Experiments and hypotheis concerning the primary action of auxin in elongation growth. Planta100: 47–75.CrossRefGoogle Scholar
  5. Hedrich, R., Kurkdjian, A., Guern, J. andFlügge, U.I. 1989. Comparative studies on the electrical properties of the H+ translocating ATPase and pyrophosphatase of the vacuolar-lysosomal compartment. EMBO J.8: 2835–2841.PubMedGoogle Scholar
  6. Hedrich, R. andSchroeder, J.I. 1989. The physiology of ion channels and electrogenic pumps in higher plants. Annu. Rev. Plant Physiol.40: 539–569.Google Scholar
  7. Katou, K. andOkamoto, H. 1992. Symplast as a functional unit in plant growth. Internatl. Rev. Cytol.142: 263–304.Google Scholar
  8. Ludevid, D., Höfte, H., Himelblau, E. andChrispeels, M.J. 1992. The expression pattern of the tonoplast intrinsic protein γ-TIP inArabidopsis thaliana is correlated with cell enlargement. Plant Physiol.100: 1633–1639.Google Scholar
  9. Maeshima, M. 1990. Development of vacuolar membranes during elongation of cells in mung bean hypocotyls. Plant Cell Physiol.31: 311–317.Google Scholar
  10. Maeshima, M. 1991. H+-translocating inorganic pyrophosphatase of plant vacuoles: inhibition by Ca2+, stabilization by Mg2+ and immunological comparison with other inorganic pyrohosphatases. Eur. J. Biochem.196: 11–17.CrossRefPubMedGoogle Scholar
  11. Maeshima, M. 1992. Characterization of the major integral protein of vacuolar membrane. Plant Physiol.98: 1248–1254.Google Scholar
  12. Maeshima, M., Mimura, T. andSato, T. 1994. Distribution of vacuolar H+-pyrophosphatase and a membrane integral protein in a variety of green plants. Plant Cell Physiol.35: 323–328.Google Scholar
  13. Maeshima, M. andYoshida, S. 1989. Purification and properties of vacuolar membrane proton-translocating inorganic pyrophosphatase from mung bean. J. Biol. Chem.264: 20068–20073.PubMedGoogle Scholar
  14. Martinoia, E., Grill, E., Tommasini, R., Kreuz, K. andAmrhein, N. 1993. ATP-dependent glutathione S-conjugate ‘export’ pump in the vacuolar membrane of plants. Nature364: 247–249.CrossRefGoogle Scholar
  15. Matsuura-Endo, C., Maeshima, M. andYoshida, S. 1990. Subunit composition of vacuolar membrane H+-ATPase from mung bean. Eur. J. Biochem.187: 745–751.CrossRefPubMedGoogle Scholar
  16. Matsuura-Endo, C., Maeshima, M. andYoshida, S. 1992. Mechanism of the decline in vacuolar H+-ATPase activity in mung bean hypocotyls during chilling. Plant Physiol.100: 718–722.Google Scholar
  17. Maurel, C., Reizer, J., Schroeder, J.I. andChrispeels, M.J. 1993. The vacuolar membrane protein γ-TIP creates water specific channels inXenopus oocytes. EMBOJ.12: 2241–2247.Google Scholar
  18. Moriyama, Y. andNelson, N. 1989. Cold inactivation of vacuolar proton-ATPases. J. Biol. Chem.264: 3577–3582.PubMedGoogle Scholar
  19. Nakahori, K., Katou, K. andOkamoto, H. 1991. Auxin changes both the extendibility and the yield threshold of the cell wall ofVigna hypocotyls. Plant Cell Physiol.32: 121–129.Google Scholar
  20. Nishimura, M. andBeevers, H., 1979. Hydrolysis of protein in vacuoles isolated from higher plant tissue. Nature277: 412–413.CrossRefGoogle Scholar
  21. Nore, B.F., Sakai-Nore, Y., Maeshima, M., Baltscheffsky, M. andNyrén, P. 1991. Immunological cross-reactivity between proton-pumping inorganic pyrophosphatases of widely phylogenic separated species. Biochem. Biophys. Res. Commun.181: 962–967.CrossRefPubMedGoogle Scholar
  22. Rea, P.A. andPoole, R.J. 1993. Vacuolar H+-translocating pyrophosphatase. Annu. Rev. Plant Physiol. Plant Molec. Biol.44: 157–180.Google Scholar
  23. Sarafian, V., Kim, Y., Poole, R.J. andRea, P.A. 1992. Molecular cloning and sequence of cDNA encoding the pyrophosphate-energized vacuolar membrane proton pump (H+-PPase) ofArabidopsis thaliana. Proc. Natl. Acad. Sci. USA89: 1775–1779.PubMedGoogle Scholar
  24. Sze, H., Ward, J.M., Lai, S. andPerera, I. 1992. Vacuolar type H+-translocating ATPases in plant endomembranes: subunit organization and multigene families. J. Exp. Biol.172: 123–136.PubMedGoogle Scholar
  25. Taiz, L. 1992. The plant vacuole. J. Exp. Biol.172: 113–122.PubMedGoogle Scholar
  26. Taiz, L. 1994. Expansins: proteins that promote cell wall loosening in plants. Proc. Natl. Acad. Sci. USA91: 7387–7389.PubMedGoogle Scholar
  27. Takeshige, K. andTazawa, M. 1989. Determination of the inorganic pyrophosphate level and its subcellular locali zation inChara corallina. J. Biol. Chem.264: 3262–3266.PubMedGoogle Scholar
  28. Tanaka, Y., Chiba, K., Maeda, M. andMaeshima, M. 1993. Molecular cloning of cDNA for vacuolar membrane proton-translocating inorganic pyrophosphatase inHordeum vulgare. Biochem. Biophys. Res. Commun.190: 1110–1114.PubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan 1996

Authors and Affiliations

  • Masayoshi Maeshima
    • 1
  • Yoichi Nakanishi
    • 1
  • Chie Matsuura-Endo
    • 2
  • Yoshiyuki Tanaka
    • 3
  1. 1.Laboratory of Biochemistry, School of Agricultural SciencesNagoya UniversityNagoyaJapan
  2. 2.Center of Crop ScienceHokkaido National Agricultural Experiment StationHokkaidoJapan
  3. 3.Chemical Tolerance LaboratoryNational Institute of Agrobiological ResourcesIbarakiJapan

Personalised recommendations