Molecular phylogenetic analysis of the tonoplast H+-ATPase subunits

Cover Page

Cite item

Full Text

Abstract

Vacuolar H+-ATPase is a multi-subunit protein complex, which fulfills a number of crucial functions in plant cell. Different mechanisms are known to be important for the regulation of proton-transporting enzyme activity at transcriptional and post-translational levels. In this investigation we performed a comparison analysis of molecular phylogeny of different subunits of vacuolar H+-ATPase directed in the elucidation of conservative rate of membrane and peripheral complexes of the enzyme. High rate of conservatism was shown for subunits c, d and В, as well as ancient duplications of subunit a.

About the authors

Tingzhuo Chen

Saint Petersburg State University

Email: ctz1985@mail.ru
PhD student, Department of plant physiology and biochemistry

Yulia Vladimirovna Mikhaylova

Komarov Botanical Institute, Russian Academy of Sciences

Email: YMikhaylova@binran.ru
junior reseacher, Laboratory of Biosystematics and Cytology

Maria Fiodorovna Shishova

Saint Petersburg State University

Email: mshishova@mail.ru
Professor, Department of plant physiology and biochemistry

References

  1. Adachi J., Waddell P. J., Martin W., Hasegawa M. (2000) Plastid genome phylogeny and a model of amino acid substitution for proteins encoded by chloroplast DNA. J. Mol. Evol. V. 50: P. 348-358.
  2. Angiosperm Phylogeny Website, version 13. Cited 10.12.2015. URL: http://www.mobot.org/MOBOT/research/APweb/.
  3. Anisimova M., Gascuel O. (2006) Approximate likelihood ratio test for branchs: A fast, accurate and powerful alternative. Systematic Biology. V. 55 (4): P. 539-552.
  4. Armbrüster A., Hohn C., Hermesdorf A. et al. (2005) Evidence for major structural changes in subunit C of the vacuolar ATPase due to nucleotide binding. FEBS Letters. V. 579: Р. 1961-1967.
  5. Bageshwar U. K., Taneja-Bageshwar S., Moharram H. M., Binzel M. L. (2005) Two isoforms of the A subunit of the vacuolar H+-ATPase in Lycopersicon esculentum: highly similar proteins but divergent patterns of tissue localization. Planta. V. 220: P. 632-643.
  6. Basak S., Gayen S., Thaker Y. R. et al. (2011) Solution structure of subunit F (Vma7p) of the eukaryotic V1VO ATPase from Saccharomyces cerevisiae derived from SAXS and NMR spectroscopy. Biochimica et Biophysica Acta. V. 1808: Р. 360-368.
  7. Beyenbach K. W., Wieczorek H. (2006) The V-type H+-ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol. V. 209: Р. 577-589.
  8. BLAST. Cited 10.12.2015. URL: http://blast.ncbi.nlm.nih.gov/Blast.cgi.
  9. Bremberger C., Lüttge U. (1992) Dynamics of tonoplast proton pumps and other tonoplast proteins of Mesembryanthemum crystallinum L. during the induction of Crassulacean acid metabolism. Planta. V. 188 (4). Р. 575-580.
  10. Cipriano D. J., Wang Y., Bond S. et al. (2008) Structure and regulation of the vacuolar ATPases. Biochimica et Biophysica Acta. V. 1777: Р. 599-604.
  11. Dayhoff M. O., Schwarz R. M., Orcut B. C. (1978) A model of Evolutionary change in proteins In Dayhoff M. O., editor. Atlas of protein sequences. 5. National Biomedical Research Foundation; p. 345-352.
  12. Dettmer J., Liu T. Y., Schumacher K. (2010) Functional analysis of Arabidopsis V-ATPase subunit VHA-E isoforms. Eur. J. Cell Biol. V. 89: Р. 152-156.
  13. Diakov T. T., Kane P. M. (2010) Regulation of vacuolar proton-translocating ATPase activity and assembly by extracellular pH. J. Biol. Chem. V. 285: Р. 23771-23778.
  14. EMBL EBI MUSCLE. Cited 10.12.2015. URL: http://www.ebi.ac.uk/Tools/msa/muscle.
  15. FigTree. Cited 10.12.2015. URL: http:/tree.bio.ed.ac.uk/software/figtree
  16. Finbow M. E., Harrison M. A. (1997) The vacuolar H+-ATPase: a universal proton pump of eukaryotes. Biochem. J. V. 324: P. 697-712.
  17. Gaxiola R. A., Palmgren M. G., Schumacher K. (2007) Plant proton pumps. FEBS Letters. V. 581: Р. 2204-2214.
  18. Gene Bank. Cited 13.07.2015. URL: http://www.ncbi.nlm.nih.gov.
  19. Gogarten J. P., Starke T., Kibak H. et al. (1992) Evolution and isoforms of V-ATPase Subunits. J. Exp. Biol. V. 172: P. 137-147.
  20. Goodstein D. M., Shu S., Howson R. et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. V. 40 (D1): D1178-D1186.
  21. Guindon S., Gascuel O. (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology. V. 52 (5): P. 696-704.
  22. Hanitzsch M., Schnitzer D., Seidel T. et al. (2007) Transcript level regulation of the vacuolar H+-ATPase subunit isoforms VHA-a, VHA-E and VHA-G in Arabidopsis thaliana. Molecular Membrane Biology. V. 24: Р. 507-518.
  23. Hertweck K. L., Kinney M. S., Stuart S. A. et al. (2015) Phylogenetics, divergence times and diversification from three genomic partitions in monocots. Botanical Journal of the Linnean Society. V. 178: P 375-393.
  24. Hirata T., Iwamoto-Kihara A., Sun-Wada G. H. et al. (2003) Subunit rotation of vacuolar-type proton pumping ATPase: relative rotation of the G and C subunits. J. Biol. Chem. V. 278: Р. 23714-23719.
  25. Hong-Hermesdorf A., Brüx A., Grüber A. et al. (2006) A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Letters. V. 580: Р. 932-939.
  26. Huelsenbeck J. P., Ronquist F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics. V. 17: P. 754-755.
  27. Jefferies K. C., Forgac M. (2008) 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. V. 283: Р. 4512-4519.
  28. Jones D. T., Taylor W. R., Thornton J. M. (1992) The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences. V. 8: P. 275-282.
  29. Kibak H., Taiz L., Starke T. et al. (1992) Evolution of Structure and Function of V-ATPases. J. Bioenerg. Biomembr. V. 24 (4): P. 415-424.
  30. Klink R., Lüttge U. (1992) 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. V. 105: Р. 414-420.
  31. Kluge C., Lahr J., Hanitzsch M. et al. (2003) New insight into the structure and regulation of the plant vacuolar H+-ATPase. J. Bioenerg. Biomembr. V. 35: Р. 377-388.
  32. Kramer D., Mangold B., Hille A. et al. (1995) The head of a higher plant V-type H+-ATPase is not always a hexamer but also a pentamer. J. Exp. Bot. V. 46: Р. 1633-1636.
  33. Krisch R., Rakowski K., Ratajczak R. (2000) Processing of V-ATPase subunit B of Mesembryanthemum crystallinum L. is mediated in vitro by a protease and/or active oxygen species. Biol. Chem. V. 381: Р. 583-592.
  34. Lai S. P., Watson J. C., Hansen J. N., Sze H. (1991) Molecular cloning and sequencing of cDNAs encoding the proteolipid subunit of the vacuolar H+-ATPase from a higher plant. J. Biol. Chem. V. 266: Р. 16078-16084.
  35. Le S. Q., Gascuel O. (2008) LG: An Improved, General Amino-Acid Replacement Matrix Mol. Biol. Evol. V. 25 (7): P. 1307-1320.
  36. Lehr A., Kirsch M., Viereck R. et al. (1999) 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. V. 39: P. 463-475.
  37. Liu Q., Kane P. M., Newman P. R., Forgac M. (1996) Site-directed mutagenesis of the yeast V-ATPase B subunit (Vma2p). J. Biol. Chem. V. 271: P 2018-22.
  38. Lüttge U., Fischer-Schliebs E., Ratajczak R. (2001) The H+-pumping V-ATPase of higher plants: a versatile eco-enzyme in response to environmental stress. Cell Biol. Mol. Lett. V. 6: Р. 356-361.
  39. Madden T. (2000) The BLAST Sequence Analysis Tool. In: J. McEntyre, J. Ostell, editors. The NCBI Handbook. Bethesda (MD). National Center for Biotechnology Information. Cited 10.12.2015. URL: http://www.ncbi.nlm.nih.gov/books/NBK21097/.
  40. Manolson M. F., Rea P. A., Poole R. J. (1985) Identification of 3-O-(4-benzoyl)benzoyladenosine 5'-triphosphate- and N, N'-dicyclohexylcarbodiimide-binding subunits of a higher plant H+-translocating tonoplast ATPase. J. Biol. Chem. V. 260: Р. 12273-12279.
  41. Martinoia E., Maeshima M., Neuhaus H. E. (2007) Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. V. 58: Р. 83-102.
  42. Martiny-Baron G., Manolson M. F., Poole R. J. et al. (1992) Proton transport and phosphorylation of tonoplast polypeptides from zucchini are stimulated by the phospholipid platelet-activating factor. Plant Physiol. V. 99: P. 1635-1641.
  43. Nelson N. (1992) Structural conservation and functional diversity of V-ATPases. J. Bioenerg. Biomembr. V. 24 (4): P. 407-414.
  44. Okonechnikov K., Golosova O., Fursov M., the UGENE team. (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics. V. 28: P. 1166-1167.
  45. Ouyang Z., Li Z., Zhang X. (2008) Cloning and sequencing of V-ATPase subunit d from mung bean and its function in passive proton transport. J Bioenerg Biomembr. V. 40: Р. 569-576.
  46. Padmanaban S., Lin X., Perera I. et al. (2004) 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. V. 134: Р. 1514-1526.
  47. Rambaut A., Suchard M. A., Xie D., Drummond A. J. (2014) Tracer v1.6. Cited 10.12.2015. URL: http://beast.bio.ed.ac.uk/Tracer.
  48. Randall S. K., Sze H. (1987) Probing the catalytic subunit of the tonoplast H+-ATPase from oat roots. Binding of 7-chloro-4-nitrobenzo-2-oxa-1,3, - diazole to the 72-kilodalton polypeptide. J. Biol. Chem. V. 262: Р. 7135-7141.
  49. Ratajczak R. (2000) Structure, function and regulation of the plant vacuolar H+-translocating ATPase. Biochimica et Biophysica Acta. V. 1465: Р. 17-36.
  50. Ratajczak R., Richter J., Luttge U. (1994) Adaptation of the tonoplast V-type H+-ATPase of Mesembryanthemum crystallinum to salt stress, C3-CAM transition and plant age. Plant Cell Environm. V. 17: Р. 1101-1112.
  51. Rockel B., Luttge U., Ratajczak R. (1998) Changes of message amount of V-ATPase subunits during salt-stress induced C3-CAM transition in Mesembryanthemum crystallinum. Plant Physiol. Biochem. V. 36: Р. 567-573.
  52. Rockel B., Ratajczak R., Becker A., Luttge U. (1994) Changed densities and diameters of intra-membrane tonoplast particles of Mesembryanthemum crystallinum in correlation with NaCl-induced CAM. J. Plant Physiol. V. 143: Р. 318-324.
  53. Schnitzer D., Seidel T., Sander T. et al. (2011) The cellular energization state affects peripheral stalk stability of plant vacuolar H+-ATPase and impairs vacuolar acidification. Plant Cell Physiol. V. 52: P. 946-956.
  54. Schumacher K., Krebs M. (2010) The V-ATPase: small cargo, large effects. Current Opinion in Plant Biology. V. 13: Р. 724-730.
  55. Seidel T., Schnitzer D., Golldack D. et al. (2008) Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis. BMC Cell Biology. V. 9: P. 28.
  56. Silvestro D., Cascales-Miñana B., Bacon C. D., Antonelli A. (2015) Revisiting the origin and diversification of vascular plants through a comprehensive Bayesian analysis of the fossil record. New Phytologist. V. 207: P. 425-436.
  57. Song C. F., Papachristos K., Rawson S. et al. (2013) Flexibility within the rotor and stators of the vacuolar H+-ATPase. PLoS One. V. 8: e82207.
  58. Starke T., Gogarten J. P. (1993) A conserved intron in the V-ATPase A subunit genes of plants and algae. FEBS Letters. V. 3: P. 252-258.
  59. Strompen G., Dettmer J., Stierhof Y. D. et al. (2005) Arabidopsis vacuolar H+-ATPase subunit E isoform 1 is required for Golgi organization and vacuole function in embryogenesis. Plant J. V. 41: Р. 125-132.
  60. Sze H., Schumacher K., Müller M. L. et al. (2002) A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H+-ATPase. Trends Plant Sci. V. 7 (4): Р. 157-161.
  61. Tamura K., Stecher G., Peterson D. et al. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. V. 30: P. 2725-2729.
  62. The UniProt Consortium. (2015) UniProt: a hub for protein information. Nucleic Acids Res. V. 43: D204-D212.
  63. Toei M., Saum R., Forgac M. (2010) Regulation and isoform function of the V-ATPases. Biochemistry. V. 49: Р. 4715-4723.
  64. Tzeng C. M., Hsu L. H., Pan R. L. (1992) Inhibition of tonoplast ATPase from etiolated mung bean seedlings by fluorescein 5'-isothiocyanate. Biochem J. V. 285 (3): Р. 737-743.
  65. Vasilyeva E., Liu Q., MacLeod K. J. et al. (2000) Cysteine scanning mutagenesis of the noncatalytic nucleotide binding site of the yeast V-ATPase. J. Biol. Chem. V. 275: P. 255-260.
  66. Wang B., Lüttge U., Ratajczak R. (2001) Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J. Exp. Bot. V. 52 (365): P. 2355-2365.
  67. Wang Y., Sze H. (1985) Similarities and differences between the tonoplast-type and the mitochondrial H+-ATPases of oat roots. J. Biol. Chem. V. 260 (19): Р. 10434-10443.
  68. Ward J. M., Sze H. (1992) Subunit Composition and Organization of the Vacuolar H+-ATPase from Oat Roots. Plant Physiol. V. 99 (1): Р. 170-179.
  69. Zhigang A., Löw R., Rausch T. et al. (1996) 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. V. 389: Р. 314-318.

Copyright (c) 2015 Chen T., Mikhaylova Y.V., Shishova M.F.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies