Abstract
The vacuolar H+-translocating ATPase (V-type ATPase) plays a central role in the growth and development of plant cells. In a mature cell, the vacuole is the largest intracellular compartment, occupying about 90% of the cell volume. The proton electrochemical gradient (acid inside) formed by the vacuolar ATPase provides the primary driving force for the transport of numerous ions and metabolites against their electrochemical gradients. The uptake and release of solutes across the vacuolar membrane is fundamental to many cellular processes, such as osmoregulation, signal transduction, and metabolic regulation. Vacuolar ATPases may also reside on endomembranes, such as Golgi and coated vesicles, and thus may participate in intracellular membrane traffic, sorting, and secretion.
Plant vacuolar ATPases are large complexes (400–650 kDa) composed of 7–10 different subunits. The peripheral sector of 5–6 subunits includes the nucleotide-binding catalytic and regulatory subunits of ∼ 70 and ∼ 60 kDa, respectively. Six copies of the 16-kDa proteolipid together with 1–3 other subunits make up the integral sector that forms the H+ conducting pathway. Isoforms of plant vacuolar ATPases are suggested by the variations in subunit composition observed among and within plant species, and by the presence of a small multigene family encoding the 16-kDa and 70-kDa subunits. Multiple genes may encode isoforms with specific properties required to serve the diverse functions of vacuoles and endomembrane compartments.
Similar content being viewed by others
Abbreviations
- DCCD:
-
N,N′-dicyclohexylcarbodiimide
- CAM:
-
Crassulacean acid metabolism
- Nbd-Cl:
-
7-chloro-4-nitrobenzo-2-oxa-1,3-diazole
- Bz-ATP:
-
3-O-(4-benzoyl)benzolyadenosine 5′-triphosphate
- DIDS:
-
4,4′-diisothiocyanostilbene-2,2′-disulfonic acid
- NEM:
-
N-ethylmaleimide
- IP3 :
-
inositol-1,4,5-triphosphate
- H+-PPase:
-
H+-translocating pyrophosphatase
- V-type:
-
vacuolar-type
- P-type:
-
phosphorylated intermediate- or plasma membrane-type
- F-type:
-
F1Fo-type
- V-ATPase:
-
vacuolar-type H+-ATPase
References
Adachi, I., Arai, H., Pimental, R., and Forgac, M. (1990).J. Biol. Chem. 265, 960–966.
Alexandre, J., Lassalles, J. P., and Kado, R. T. (1990).Nature (London)343, 567–570.
Ali, M. S., and Akazawa, T. (1986).Plant Physiol. 81, 222–227.
Arai, H., Terres, G., Pink, S., and Forgac, M. (1988).J. Biol. Chem. 263, 8796–8802.
Arai, H., Pink, S., and Forgac, M. (1989).Biochemistry 28, 3075–3082.
Assmann, S. M., Simoncini, L., and Schroeder, J. I., (1985).Nature (London)318, 285–287.
Bennett, A. B., and Spanswick, R. M. (1983).J. Membr. Biol. 75, 21–31.
Bennett, A. B., and Spanswick, R. M. (1984).Plant Physiol.,74, 545–548.
Blackford, S., Rea, P. A., and Sanders, D. (1990).J. Biol. Chem. 265, 9617–9620.
Blumwald, E., and Poole, R. J. (1987).Plant Physiol. 83, 884–887.
Boller, T., and Wiemken, A. (1986).Ann. Rev. Plant Physiol. 37, 137–164.
Bowman, B. J., Allen, R., Wechser, M. A., and Bowman, E. J. (1988).J. Biol. Chem. 263, 14002–14007.
Bowman, E. J., Siebers, A., and Altendorf, K. (1988a).Proc. Natl. Acad. Sci. USA 85, 7972–7976.
Bowman, E. J., Tenney, K., and Bowman, B. J. (1988b).J. Biol. Chem. 263, 13994–14001 [67kDa].
Bremberger, C., Haschke, H.-P., and Luttge, U. (1988).Planta 175, 465–470.
Briskin, D. P., Thornley, R. W., and Wyse, R. E. (1985).Plant Physiol. 78, 871–875.
Chanson, A., and Taiz, L. (1985).Plant Physiol. 78, 232–240.
Churchill, K. A., and Sze, H. (1984).Plant Physiol. 76, 490–497.
Depta, H., Holstein, S. E. H., Robinson, D. G., Lutzelschwab, M., and Michalke, W. (1991).Planta 183, 434–442.
Dupont, F. M., and Morrissey, P. J. (1992).Arch. Biochem. Biophys. 294, 341–346.
DuPont, F. M., Tanada, C. K., and Hurkman, W. J. (1988).Plant Physiol. 86, 717–724.
Evans, D. E., Briars, S. A., and Williams, L. E. (1991).J. Exp. Bot. 42, 285–303.
Forgac, M. (1989).Physiol. Rev. 69, 765–796.
Foury, F. (1990).J. Biol. Chem. 265, 18554–18560.
Getz, H.-P. (1991).Planta 185, 261–268.
Gogarten, J. P., Kibak, H., Dittrich, P., Taiz, L., Bowman, E. J., Bowman, B. J., Manolson, M. F., Poole, R. J., Date, T., Oshima, T., Konishi, J., Denda, K., and Yoshida, M. (1989).Proc. Natl. Acad. Sci. USA 86, 6661–6665.
Guern, J., Mathieu, Y., Kurkdjian, A., Manigault, P., Gillet, B., Beloeil, J.-C., and Lallemand, J.-Y. (1989).Plant Physiol. 89, 27–36.
Guern, J., Felle, H., Mathieu, Y., and Kurkdjian, A. (1991).Int. Rev. Cytol. 127, 111–73.
Harley, S. M., and Beevers, L. (1989).Plant Physiol. 91, 674–678.
Harris, N. (1986).Annu. Rev. Plant Physiol. 37, 73–92.
Hedrich, R., and Neher, E. (1987).Nature (London)329, 833–836.
Hedrich, R., and Schroeder, J. I. (1989).Annu. Rev. Plant Physiol. 40, 539–569.
Hedrich, R., Kurkdjian, A., Guern, J., and Flugge, U. I. (1989).EMBO J. 8, 2835–2841.
Hirata, R., Ohsumi, Y., Nakano, A., Kawasaki, H., Suzuki, K., and Anraku, Y. (1990).J. Biol. Chem. 265, 6726–6733.
Homeyer, U., Litek, K., Huchzermeyer, B., and Schultz, G. (1989).Plant Physiol. 89, 1388–1393.
Hurley, D., and Taiz, L. (1989).Plant Physiol. 89, 391–395.
Inatomi, K. I., Eya, S., Maeda, M., and Futai, M. (1989).J. Biol. Chem. 264, 10954–10959.
Johannes, E., Brosnan, J. M., and Sanders, D. (1991).BioEssays 13, 331–336.
Kaestner, K. H., and Sze, H. (1987).Plant Physiol. 83, 483–489.
Kaestner, K. H., Randall, S. K., and Sze, H. (1988).J. Biol. Chem. 263, 1282–1287.
Klink, R., and Luttge, U. (1991).Biot. Acta 104, 122–131.
Lai, S., Randall, S. K., and Sze, H. (1988).J. Biol. Chem. 263, 16731–16737.
Lai, S., Watson, J. C., Hansen, J. N., and Sze, H. (1991).J. Biol. Chem. 266, 16078–16084.
Luttge, U. (1987).New Phytol. 106, 593–629.
Luttge, U., and Higinbotham, N. (1979).Transport in Plants, Springer-Verlag, New York.
MacRobbie, E. A. C. (1979). InPlant organelles (Reid, E., ed.), Wiley, New York, pp. 61–67.
Mandala, S., and Taiz, L. (1985).Plant Physiol. 78, 327–333.
Mandala, S., and Taiz, L. (1986).J. Biol. Chem. 261, 12850–12855.
Manolson, M. F., Rea, P. A., and Poole, R. J. (1985).J. Biol. Chem. 260, 12273–12279.
Manolson, M. F., Ouellette, B. F. F., Filion, M., and Poole, R. J. (1988).J. Biol. Chem. 263, 17987–17994.
Martinoia, E., Thume, M., Vogt, E., Rentsch, D., and Dietz, K.-J. (1991).Plant Physiol. 97, 664–650.
Matsuura-Endo, C., Maeshima, M., and Yoshida, S. (1990).Eur. J. Biochem. 187, 745–751.
Moriyama, Y., and Nelson, N. (1989).J. Biol. Chem. 264, 3577–3582.
Morre, D. J., Liedtke, C., Brightman, A. O., and Scherer, G. F. E. (1991).Planta 184, 343–349.
Narasimhan, M. L., Binzel, M. L., Perez-Prat, E., Chen, Z., Nelson, D. E., Singh, N. K., Bressan, R. A., and Hasegawa, P. M. (1991).Plant Physiol. 97, 562–568.
Nelson, H., and Nelson, N. (1989).FEBS Lett. 247, 147–153.
Nelson, H., and Nelson, N. (1990).Proc. Natl. Acad. Sci. USA 87, 3503–3507.
Noumi, T., Beltran, C., Nelson, H., and Nelson, N. (1991).Proc. Natl. Acad. Sci. USA 88, 1938–1942.
Parry, R. V., Turner, J. C., and Rea, P. A. (1989).J. Biol. Chem. 264, 20025–20032.
Pope, A. J., and Leigh, R. A. (1990).Planta 181, 406–413.
Puopolo, K., and Forgac, M. (1990).J. Biol. Chem. 265, 14836–14841.
Randall, S. K., and Sze, H. (1986).J. Biol. Chem. 261, 1364–1371.
Randall, S. K., and Sze, H. (1987).J. Biol. Chem. 262, 7135–7141.
Randall, S., and Sze, H. (1989).Plant Physiol. 89, 1292–1298.
Raschke, K., Hedrich, R., Beckmann, U., and Schroeder, J. I. (1988).Bot. Acta 101, 283–294.
Rea, P. A., and Sanders, D. (1987).Physiol. Plant. 71, 131–141.
Rea, P. A., Griffith, C. J., Manolson, M. F., and Sanders, D. (1987a).Biochim. Biophys. Acta 904, 1–12.
Rea, P. A., Griffith, C. J., and Sanders, D. (1987b).J. Biol. Chem. 262, 14745–14752.
Reuveni, M., Bennett, A. B., Bressan, R. A., and Hasegawa, P. M. (1990).Plant Physiol. 94, 524–530.
Ryan, C. A. (1990).Annu. Rev. Phytopathol. 28, 425–449.
Sanchez-Aguayo, I., Gonzalez-Utor, A. L., and Medina, A. (1991).Plant Physiol. 96, 153–158.
Schroeder, J. I., and Hedrich, R. (1989).Trend Biochem. Sci. 14, 187–192.
Schumaker, K. S., and Sze, H. (1986).J. Biol. Chem. 261, 12172–12178.
Schumaker, K. S., and Sze, H. (1987).J. Biol. Chem. 262, 3944–3946.
Struve, I., Rausch, T., Bernasconi, P., and Taiz, L. (1990).J. Biol. Chem. 265, 7927–7932.
Sze, H. (1985).Annu. Rev. Plant. Physiol. 36, 175–208.
Taiz, S. L., and Taiz, L. (1991).Bot. Acta 104, 117–121.
Tiedge, H., and Schafer, G. (1989).Biochim Biophys Acta 977, 1–9.
Walker, J. E., Saraste, M., Runswick, M., and Gay, N. J. (1982).EMBO J. 8, 945–951.
Wang, Y., and Sze, H. (1985).J. Biol. Chem. 260, 10434–10443.
Wang, Z. Q., and Gluck, S. (1990).J. Biol. Chem. 265, 21957–21965.
Ward, J. M., and Sze, H. (1992a).Plant Physiol. 99, 70–179.
Ward, J. M., and Sze, H. (1992b).Plant Physiol., in press.
Ward, J. M., Reinders, A., Hsu, H.-T., and Sze, H. (1992).Plant Physiol. 99, 161–169.
White, P. J., and Smith, J. A. C. (1989).Planta 179, 265–274.
Yoshida, S. (1991).Plant Physiol. 95, 456–460.
Zhen, R.-G., Koyro, H.-W., Leigh, R. A., Tomos, A. D., and Miller, A. J. (1991).Planta 185, 356–361.
Zimniak, K., Dittrich, P., Gogarten, J. P., Kibak, H., and Taiz, L. (1988).J. Biol. Chem. 263, 9102–9112.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sze, H., Ward, J.M. & Lai, S. Vacuolar H+-translocating ATPases from plants: Structure, function, and isoforms. J Bioenerg Biomembr 24, 371–381 (1992). https://doi.org/10.1007/BF00762530
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00762530