Peculiar features of plant cell vacuolar H+-ATPase regulation

  • Аnastasia Kirpichnikova Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0001-5133-5175
  • Tingzhuo Chen Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0001-5143-6128
  • Daria Romanyuk Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0001-9576-1256
  • Vladislav Yemelyanov Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0003-2323-5235
  • Maria Shishova Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation

Abstract

Vacuolar Н+-АТPase is one of the most crucial and widely spread proton-transporting enzymes of eukaryotic cells. It fulfils many vital functions. The enzyme is represented as a multisubunit complex, organized in two domains, V1 and V0. The review summarizes modern data on plant cell H+-V-ATPase. Regulation of proton pump activity is analyzed for different level of plant organism complicity. A number of vacuolar Н+-АТPase subunits are encoded by more than one gene. Thus the importance of regulation at transcription level is discussed. Special attention is paid to analysis of different ways of regulating activity of the enzyme at post-translation level. Refs 60. Table 1.

Keywords:

vacuolar H -ATPase, VHAs gene family, activity regulation

Downloads

Download data is not yet available.
 

References

Merzendorfer H., Gräf R., Huss M. et al. Regulation of proton translocating V-ATPases. J. Exp. Biol, 1997, vol. 200, pp. 225‒235.

Ratajczak R. Structure, function and regulation of the plant vacuolar H+-translocating ATPase. Biochim. Biophys. Acta, 2000, vol. 1465, pp. 17‒36.

Gruber G., Wieczorek H., Harvey W. R., Muller V. Structure-function relationship of A-, F- and VATPases. J. Exp. Biol., 2001, vol. 204, pp. 2597‒2605.

Kluge C., Lahr J., Hanitzsch M., Bolte S., Golldack D., Dietz K. J. New insight into the structure and regulation of the plant vacuolar H+-ATPase. J. Bioenerg. Biomembr., 2003, vol. 35, pp. 377‒388.

Nelson N., Harvey W. R. Vacuolar and plasma membrane proton-adenosinetriphosphatases. Physiol. Rev., 1999, vol. 79, pp. 361‒385.

Ma B., Xiang Y., An L. Structural bases of physiological functions and roles of the vacuolar H+-ATPase. Cell. Signalling, 2011, vol. 23, pp. 1244‒1256.

Dettmer J., Liu T. Y., Schumacher K. Functional analysis of Arabidopsis V-ATPase subunit VHA-E isoforms. Eur. J. Cell Biol., 2010, vol. 89, pp. 152‒156.

Mauvezin C., Nagy P., GaborJuha S. Z., Neufeld T. P. Autophagosome-lysosome fusion is independent of V-ATPase-mediated acidification. Nature Communications, 2015, vol. 6. Art. 7007. https://doi.org/10.1038/ncomms8007

Marshansky V., Futai M. The V-type H+-ATPase in vesicular trafficking: targeting, regulation and function. Curr. Opin. Cell Biol., 2008, vol. 20, pp. 415–426.

Dettmer J., Hong-Hermesdorf A., Stierhof Y.-D., Schumacher K. Vacuolar H+-ATPase activity is regulated for endocytic and secretory trafficking in Arabidopsis. Plant Cell., 2006, vol. 18, pp. 715‒730.

Schumacher K. Endomembrane proton pumps: connecting membrane and vesicle transport. Curr. Opin. Plant Biol., 2006, vol. 9, pp. 595‒600.

Strompen G., Dettmer J., Stierhof Y. D., Schumacher K., Jürgens G., Mayer U. Arabidopsis vacuolar H+-ATPase subunit E isoform 1 is required for Golgi organization and vacuole function in embryogenesis. Plant J., 2005, vol. 41, pp. 125‒132.

Sze H., Schumacher K., Müller M. L., Padmanaban S., Taiz L. A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H+-ATPase. Trends Plant Sci., 2002, vol. 7, pp. 157‒161.

Schumacher K., Krebs M. The V-ATPase: small cargo, large effects. Curr. Opin. Plant Biol., 2010, vol. 13, pp. 724‒730.

Chen T., Mikhailova Iu. V., Shishova M. F. Molekuliarno-filogeneticheskii analiz sub’’edinits H+-ATFazy tonoplasta [Molecular phylogenetic analysis of H+-ATPase subunits of tonoplast]. Ekolog. genetika, 2015, vol. 13, pp. 78‒90. (In Russian)

Padmanaban S., Lin X., Perera I., Kawamura Y., Sze H. Differential expression of vacuolar H+-ATPase subunit c genes in tissues active in membrane trafficking and their roles in plant growth as revealed by RNAi. Plant Physiol., 2004, vol. 134, pp. 1514‒1526.

Hasenfratz M. P., Tsou C.-L., Wilkins T. A. Expression of two related vacuolar H+-ATPase 16 kD proteolipid genes is differentially regulated in a tissue-specific manner. Plant Physiol., 1995, vol. 108, pp. 1395‒1404.

Dettmer J., Schubert D., Calvo-Weimar O., Stierhof Y. D., Schmidt R., Schumacher K. Essential role of the V-ATPase in male gametophyte development. Plant J., 2005, vol. 41, pp. 117‒124.

Hanitzsch M., Schnitzer D., Seidel T., Golldack D., Dietz K. J. Transcript level regulation of the vacuolar H+-ATPase subunit isoforms VHA-a, VHA-E and VHA-G in Arabidopsis thaliana. Molecul. Membra. Biolog., 2007, vol. 24, pp. 507‒518.

Allen G. J., Chu S. P., Schumacher K., Shimazaki C. T., Vafeados D., Kemper A., Hawke S. D., Tallman G., Tsien R. Y., Harper J. F., Chory J., Schroeder J. I. Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science, 2000, vol. 289, pp. 2338‒2342.

Lüttge U., Fischer-Schliebs E., Ratajczak R. The H+-pumping V-ATPase of higher plants: a versatile eco-enzyme in response to environmental stress. Cell. Biol. Mol. Lett., 2001, vol. 6, pp. 356‒361.

Narasimhan M. L., Binzel M. L., Perez-Prat E., Chen Z., Nelson D. E., Singh N. K., Bressan R. A., Hasegawa P. M. NaCl Regulation of tonoplast ATPase 70-kilodalton subunit mRNA in tobacco cells. Plant Physiol., 1991, vol. 97, pp. 562‒568.

Binzel M. L. NaCl-induced accumulation of tonoplast and plasma membrane H+-ATPase message in tomato. Physiol. Plant., 1995, vol. 94, pp. 722‒728.

Kirsch M., An Z., Viereck R., Löw R., Rausch T. Salt stress induces an increased expression of V-type H+-ATPase in mature sugar beet leaves. Plant Mol. Biol., 1996, vol. 32, pp. 543‒547.

Lehr A., Kirsch M., Viereck R., Schiemann J., Rausch T. cDNA and genomic cloning of sugar beet V-type H+-ATPase subunit A and c isoforms: evidence for coordinate expression during plant development and coordinate induction in response to high salinity. Plant Mol. Biol., 1999, vol. 39, pp. 463‒475.

Rausch T., Kirsch M., Löw R., Lehr A., Viereck R., Zhigang A. Salt stress responses of higher plants: the role of proton pumps and Na+/H+-antiporters. J. Plant Physiol., 1996, vol. 148, pp. 425‒433.

Löw R., Rausch T. In suspension-cultured Daucus carota cells salt stress stimulates H+-transport but not ATP hydrolysis of the V-ATPase. J. Exp. Bot., 1996, vol. 47, pp. 1725‒1732.

PereraI. Y., Li X., Sze H. Several distinct genes encode nearly identical to 16 kDa proteolipids of the vacuolar H+-ATPase from Arabidopsis thaliana. Plant Mol. Biol., 1995, vol. 29, pp. 227‒244.

Löw R., Rockel B., Kirsch M., Ratajczak R., Hörtensteiner S., Martinoia E., Lüttge U., Rausch T. Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryanthemum crystallinum. Plant Physiol., 1996, vol. 110, pp. 259‒265.

Tsiantis M. S., Bartholomew D. M., Smith J. A. Salt regulation of transcript levels for the c subunit of a leaf vacuolar H+-ATPase in the halophyte Mesembryanthemum crystallinum. Plant J., 1996, vol. 9, pp. 729‒736.

Rockel B., Luttge U., Ratajczak R. Changes of message amount of V-ATPase subunits during saltstress induced C3-CAM transition in Mesembryanthemum crystallinum. Plant Physiol. Biochem., 1998, vol. 36, pp. 567‒573.

Dietz K. J., Arbinger B. cDNA sequence and expression of subunit E of the vacuolar H+-ATPase in the inducible Crassulacean acid metabolism plant Mesembryanthemum crystallinum. Biochim. Biophys. Acta, 1996, vol. 1281, pp. 134‒138.

Golldack D., Dietz K. J. Salt-induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiol., 2001, vol. 125, pp. 1643‒1654.

Cooley M. B., Yang H., Dahal P., Mella R. A., Downie A. B., Haigh A. M., Bradford K. J. Vacuolar H+-ATPase is expressed in response to gibberellin during tomato seed germination. Plant Physiol., 1999, vol. 121, pp. 1339‒1347.

Kasai M., Yamamoto Y., Maeshima M., Matsumoto H. Effects of in vivo treatment with abscisic acid and/or cytokinin on activities of vacuolar H+-pumps of tonoplast-enriched membrane vesicles prepared from barley roots. Plant Cell Physiol., 1993, vol. 34, pp. 1107‒1115.

Wang B., Lüttge U., Ratajczak R. Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J. Exp. Bot., 2001, vol. 52, pp. 2355‒2365.

Mariaux J. B., Fischer-Schliebs E., Luttge U., Ratajczak R. Dynamics of activity and structure of the tonoplast vacuolar-type H+-ATPase in plants with different CAM expression and in a C3 plant under salt stress. Protoplasma, 1997, vol. 196, pp. 181‒189.

Bremberger C., Lüttge U. Dynamics of tonoplast proton pumps and other tonoplast proteins of Mesembryanthemum crystallinum L. during the induction of Crassulacean acid metabolism. Planta, 1992, vol. 188, pp. 575‒580.

Ratajczak R., Richter J., Luttge U. Adaptation of the tonoplast V-type H+-ATPase of Mesembryanthemum crystallinum to salt stress, C3-CAM transition and plant age. Plant Cell Environm., 1994, vol. 17, pp. 1101‒1112.

Klink, R., Lüttge, U. Quantification of visible structural changes of the V0V1-ATPase in the leaf tonoplast of Mesembryanthemum crystallinum by freeze-fracture replicas prepared during the C3-photosynthesis to CAM transition. Bot. Acta, 1992, vol. 105, pp. 414‒420.

Rockel B., Ratajczak R., Becker A., Luttge U. Changed densities and diameters of intra-membrane tonoplast particles of Mesembryanthemum crystallinum in correlation with NaCl-induced CAM. J. Plant Physiol., 1994, vol. 143, pp. 318‒324.

Zhigang A., Löw R., Rausch T., Lüttge U., Ratajczak R. The 32 kDa tonoplast polypeptide Di associated with the V-type H+-ATPase of Mesembryanthemum crystallinum L. in the CAM state: A proteolytically processed subunit B? FEBS Letters, 1996, vol. 389, pp. 314‒318.

Krisch R., Rakowski K., Ratajczak R. Processing of V-ATPase subunit B of Mesembryanthemum crystallinum L. is mediated in vitro by a protease and/or active oxygen species. Biol. Chem., 2000, vol. 381, pp. 583‒592.

Kramer D., Mangold B., Hille A., Emig I., Hess A., Ratajczak R., Luttge U. The head of a higher plant V-type H+-ATPase is not always a hexamer but also a pentamer. J. Exp. Bot., 1995, vol. 46, pp. 1633‒1636.

Neuhaus H. E., Trentmann O. Regulation of transport processes across the tonoplast. Front. Plant Sci., 2014, vol. 5. Article 460, pp. 1‒8.

Tavakoli N., Kluge C., Golldack D., Mimura T., Dietz K. J. Reversible redox control of plant vacuolar H+-ATPase activity is related to disulfide bridge formation in subunit E as well as subunit A. Plant J., 2001, vol. 28, pp. 51‒59.

Seidel T., Scholl S., Krebs M., Rienmüller F., Marten I., Hedrich R., Hanitzsch M., Janetzki P., Dietz K. J., Schumacher K. Regulation of the V-type ATPase by redox modulation. Biochem. J., 2012, vol. 448, pp. 243‒251.

Fischer-Schliebs E., Drobny M., Ball E., Ratajczak R., Luttge U. Variation in nitrate nutrition leads to changes in the performance of the V-ATPase and immunological differences of proteolipid subunit C in tobacco (Nicotiana tabacum L.) leaves. Austr. J. Plant Physiol., 2000, vol. 27, pp. 639‒648.

Armbruster A., Hohl C., Hermesdorf A., Schumacher K., Borsh M., Gruber G. Evidence for major structureal changes in subunit C of the vacuolar ATPase due to nucleotide binding. FEBS Letters, 2005, vol. 579, pp. 1961‒1967.

Schnitzer D., Seidel Th., Sander T., Golldack D., Dietz K-J. The cellular energization state affects peripheral stalk stability of plant vacuolar H+-ATPase and impairs vacuolar acidification. Plant Cell Physiol., 2011. 52, pp. 946‒956.

Hong-Hermesdorf A., Brux A., Gruber A., Gruber G., Schumacher K. A WNK-kinase binds and phosphorylates V-ATP subunit C. FEBS Letters, 2006, vol. 580, pp. 932‒939.

Klyachnikov O. I., Li K. W., Lill H., de Boer A. H. The V-ATPase from etiolated barley (Hordeum vulgare L.) shoots is activated by blue light and interacts with 14–3–3 proteins. J. Exp. Bot., 2007, vol. 58, pp. 1013‒1023.

Cho Y. H., Yoo S. D., Sheen J. Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell., 2006, vol. 127, pp. 579‒589.

Yamaguchi M., Kasamo K. Modulation in the activity of purified tonoplast H+-ATPase by tonoplast glycolipids prepared from cultured rice (Oryza sativa L. var. boro) cells. Plant Cell Physiol., 2001, vol. 42, pp. 516‒523.

Zhang C., Hicks G. R., Raikhel N. V. Molecular composition of plant vacuoles: important but less understood regulations and roles of tonoplast lipids. Plants, 2015, vol. 4, pp. 320‒333.

Toei M., Saum R., Forgac M. Regulation and isoform function of the V-ATPases. Biochem., 2010, vol. 49, pp. 4715‒4723.

Jefferies K. C., Forgac M. Subunit H of the vacuolar H+-ATPase inhibits ATP hydrolysis by the free V1 domain by interaction with the rotary subunit F. J. Biol. Chem., 2008, vol. 283, pp. 4512‒4519.

Beyenbach K. W., Wieczorek H. The V-type H+-ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol., 2006, vol. 209, pp. 577‒589.

Diakov T. T., Kane P. M. Regulation of vacuolar proton-translocating ATPase activity and assembly by extracellular pH. J. Biol. Chem., 2010, vol. 285, pp. 23771‒23778.

Ward J. M., Reinders A., Hsu H.-T., Sze H. Dissociation and reassembly of the vacuolar H+-ATPase complex from oat roots. Plant Physiol., 1992, vol. 99, pp. 161‒169.
Published
2016-06-26
How to Cite
KirpichnikovaА., Chen, T., Romanyuk, D., Yemelyanov, V., & Shishova, M. (2016). Peculiar features of plant cell vacuolar H<sup>+</sup&gt;-ATPase regulation. Biological Communications, (2), 149–160. https://doi.org/10.21638/11701/spbu03.2016.212
Section
Full communications