Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1997 Oct;115(2):753–761. doi: 10.1104/pp.115.2.753

A Vacuole-Associated Annexin Protein, VCaB42, Correlates with the Expansion of Tobacco Cells.

D F Seals 1, S K Randall 1
PMCID: PMC158535  PMID: 12223842

Abstract

A Ca-dependent membrane-binding protein of the annexin family, VCaB42, has previously been shown to associate with vacuolar vesicles at physiological levels of Ca. In this study we used suspension-cultured cells of tobacco (Nicotiana tabacum BY-2) to show that VCaB42 is enriched 4.5-fold in intact vacuoles, whereas evacuolated protoplasts show a 12-fold reduction in VCaB42. VCaB42 distribution is thus comparable to that of the vacuole-associated H+-ATPase but is distinct from the endoplasmic reticulum-localized protein calnexin. Because VCaB42 is a vacuole-associated annexin, and given the putative function of annexins in vesicle fusion, we hypothesize a role for this protein in the vacuolation process of expanding cells. Consistent with this hypothesis, we show that VCaB42 levels correlate with age-associated and hormonally induced changes in cell volume in tobacco suspension cultures. The association of VCaB42 with vacuoles and its correlative pattern of expression relative to the expansion of cells is consistent with a possible role for VCaB42 in the early events of vacuole biogenesis.

Full Text

The Full Text of this article is available as a PDF (2.6 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Battey N. H., James N. C., Greenland A. J. cDNA isolation and gene expression of the maize annexins p33 and p35. Plant Physiol. 1996 Nov;112(3):1391–1396. doi: 10.1104/pp.112.3.1391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bednarek S. Y., Reynolds T. L., Schroeder M., Grabowski R., Hengst L., Gallwitz D., Raikhel N. V. A small GTP-binding protein from Arabidopsis thaliana functionally complements the yeast YPT6 null mutant. Plant Physiol. 1994 Feb;104(2):591–596. doi: 10.1104/pp.104.2.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Binzel M. L., Hess F. D., Bressan R. A., Hasegawa P. M. Intracellular compartmentation of ions in salt adapted tobacco cells. Plant Physiol. 1988 Feb;86(2):607–614. doi: 10.1104/pp.86.2.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blackbourn H. D., Barker P. J., Huskisson N. S., Battey N. H. Properties and partial protein sequence of plant annexins. Plant Physiol. 1992 Jul;99(3):864–871. doi: 10.1104/pp.99.3.864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  6. Burgoyne R. D., Clague M. J. Annexins in the endocytic pathway. Trends Biochem Sci. 1994 Jun;19(6):231–232. doi: 10.1016/0968-0004(94)90143-0. [DOI] [PubMed] [Google Scholar]
  7. Calvert C. M., Gant S. J., Bowles D. J. Tomato annexins p34 and p35 bind to F-actin and display nucleotide phosphodiesterase activity inhibited by phospholipid binding. Plant Cell. 1996 Feb;8(2):333–342. doi: 10.1105/tpc.8.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chrispeels M. J., Raikhel N. V. Short peptide domains target proteins to plant vacuoles. Cell. 1992 Feb 21;68(4):613–616. doi: 10.1016/0092-8674(92)90134-x. [DOI] [PubMed] [Google Scholar]
  9. Clark G. B., Dauwalder M., Roux S. J. Immunolocalization of an annexin-like protein in corn. Adv Space Res. 1994;14(8):341–346. doi: 10.1016/0273-1177(94)90421-9. [DOI] [PubMed] [Google Scholar]
  10. Clark G. B., Dauwalder M., Roux S. J. Purification and immunolocalization of an annexin-like protein in pea seedlings. Planta. 1992;187:1–9. [PubMed] [Google Scholar]
  11. Clark G. B., Turnwald S., Tirlapur U. K., Haas C. J., von der Mark K., Roux S. J., Scheuerlein R. Polar distribution of annexin-like proteins during phytochrome-mediated initiation and growth of rhizoids in the ferns Dryopteris and Anemia. Planta. 1995;197(2):376–384. doi: 10.1007/BF00202660. [DOI] [PubMed] [Google Scholar]
  12. Coughlan S. J., Hastings C., Winfrey R. J., Jr Molecular characterisation of plant endoplasmic reticulum. Identification of protein disulfide-isomerase as the major reticuloplasmin. Eur J Biochem. 1996 Jan 15;235(1-2):215–224. doi: 10.1111/j.1432-1033.1996.00215.x. [DOI] [PubMed] [Google Scholar]
  13. Denecke J., Carlsson L. E., Vidal S., Höglund A. S., Ek B., van Zeijl M. J., Sinjorgo K. M., Palva E. T. The tobacco homolog of mammalian calreticulin is present in protein complexes in vivo. Plant Cell. 1995 Apr;7(4):391–406. doi: 10.1105/tpc.7.4.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Emans N., Gorvel J. P., Walter C., Gerke V., Kellner R., Griffiths G., Gruenberg J. Annexin II is a major component of fusogenic endosomal vesicles. J Cell Biol. 1993 Mar;120(6):1357–1369. doi: 10.1083/jcb.120.6.1357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Futter C. E., Felder S., Schlessinger J., Ullrich A., Hopkins C. R. Annexin I is phosphorylated in the multivesicular body during the processing of the epidermal growth factor receptor. J Cell Biol. 1993 Jan;120(1):77–83. doi: 10.1083/jcb.120.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gidrol X., Sabelli P. A., Fern Y. S., Kush A. K. Annexin-like protein from Arabidopsis thaliana rescues delta oxyR mutant of Escherichia coli from H2O2 stress. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):11268–11273. doi: 10.1073/pnas.93.20.11268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gogarten J. P., Fichmann J., Braun Y., Morgan L., Styles P., Taiz S. L., DeLapp K., Taiz L. The use of antisense mRNA to inhibit the tonoplast H+ ATPase in carrot. Plant Cell. 1992 Jul;4(7):851–864. doi: 10.1105/tpc.4.7.851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Griffing L. R. Comparisons of Golgi structure and dynamics in plant and animal cells. J Electron Microsc Tech. 1991 Feb;17(2):179–199. doi: 10.1002/jemt.1060170206. [DOI] [PubMed] [Google Scholar]
  19. Haas A., Scheglmann D., Lazar T., Gallwitz D., Wickner W. The GTPase Ypt7p of Saccharomyces cerevisiae is required on both partner vacuoles for the homotypic fusion step of vacuole inheritance. EMBO J. 1995 Nov 1;14(21):5258–5270. doi: 10.1002/j.1460-2075.1995.tb00210.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hauptmann R., Maurer-Fogy I., Krystek E., Bodo G., Andree H., Reutelingsperger C. P. Vascular anticoagulant beta: a novel human Ca2+/phospholipid binding protein that inhibits coagulation and phospholipase A2 activity. Its molecular cloning, expression and comparison with VAC-alpha. Eur J Biochem. 1989 Oct 20;185(1):63–71. doi: 10.1111/j.1432-1033.1989.tb15082.x. [DOI] [PubMed] [Google Scholar]
  21. Hohl I., Robinson D. G., Chrispeels M. J., Hinz G. Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. J Cell Sci. 1996 Oct;109(Pt 10):2539–2550. doi: 10.1242/jcs.109.10.2539. [DOI] [PubMed] [Google Scholar]
  22. Hoshino T., Mizutani A., Chida M., Hidaka H., Mizutani J. Plant annexin form homodimer during Ca(2+)-dependent liposome aggregation. Biochem Mol Biol Int. 1995 Apr;35(4):749–755. [PubMed] [Google Scholar]
  23. Höfte H., Hubbard L., Reizer J., Ludevid D., Herman E. M., Chrispeels M. J. Vegetative and Seed-Specific Forms of Tonoplast Intrinsic Protein in the Vacuolar Membrane of Arabidopsis thaliana. Plant Physiol. 1992 Jun;99(2):561–570. doi: 10.1104/pp.99.2.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hörtensteiner S., Martinoia E., Amrhein N. Factors affecting the re-formation of vacuoles in evacuolated protoplasts and the expression of the two vacuolar proton pumps. Planta. 1994;192(3):395–403. doi: 10.1007/BF00198576. [DOI] [PubMed] [Google Scholar]
  25. Ikonen E., Tagaya M., Ullrich O., Montecucco C., Simons K. Different requirements for NSF, SNAP, and Rab proteins in apical and basolateral transport in MDCK cells. Cell. 1995 May 19;81(4):571–580. doi: 10.1016/0092-8674(95)90078-0. [DOI] [PubMed] [Google Scholar]
  26. Iraki N. M., Bressan R. A., Hasegawa P. M., Carpita N. C. Alteration of the physical and chemical structure of the primary cell wall of growth-limited plant cells adapted to osmotic stress. Plant Physiol. 1989 Sep;91(1):39–47. doi: 10.1104/pp.91.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jäckle S., Beisiegel U., Rinninger F., Buck F., Grigoleit A., Block A., Gröger I., Greten H., Windler E. Annexin VI, a marker protein of hepatocytic endosomes. J Biol Chem. 1994 Jan 14;269(2):1026–1032. [PubMed] [Google Scholar]
  28. Kaplan R. S., Pedersen P. L. Determination of microgram quantities of protein in the presence of milligram levels of lipid with amido black 10B. Anal Biochem. 1985 Oct;150(1):97–104. doi: 10.1016/0003-2697(85)90445-2. [DOI] [PubMed] [Google Scholar]
  29. Kirsch T., Paris N., Butler J. M., Beevers L., Rogers J. C. Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3403–3407. doi: 10.1073/pnas.91.8.3403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kirsch T., Saalbach G., Raikhel N. V., Beevers L. Interaction of a potential vacuolar targeting receptor with amino- and carboxyl-terminal targeting determinants. Plant Physiol. 1996 Jun;111(2):469–474. doi: 10.1104/pp.111.2.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lloyd C. W., Lowe S. B., Peace G. W. The mode of action of 2,4-D in counteracting the elongation of carrot cells grown in culture. J Cell Sci. 1980 Oct;45:257–268. doi: 10.1242/jcs.45.1.257. [DOI] [PubMed] [Google Scholar]
  32. Ludevid D., Höfte H., Himelblau E., Chrispeels M. J. The Expression Pattern of the Tonoplast Intrinsic Protein gamma-TIP in Arabidopsis thaliana Is Correlated with Cell Enlargement. Plant Physiol. 1992 Dec;100(4):1633–1639. doi: 10.1104/pp.100.4.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Marty F. Cytochemical studies on GERL, provacuoles, and vacuoles in root meristematic cells of Euphorbia. Proc Natl Acad Sci U S A. 1978 Feb;75(2):852–856. doi: 10.1073/pnas.75.2.852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Maurel C., Reizer J., Schroeder J. I., Chrispeels M. J. The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes. EMBO J. 1993 Jun;12(6):2241–2247. doi: 10.1002/j.1460-2075.1993.tb05877.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. McClung A. D., Carroll A. D., Battey N. H. Identification and characterization of ATPase activity associated with maize (Zea mays) annexins. Biochem J. 1994 Nov 1;303(Pt 3):709–712. doi: 10.1042/bj3030709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Morehead T. A., Biermann B. J., Crowell D. N., Randall S. K. Changes in Protein Isoprenylation during the Growth of Suspension-Cultured Tobacco Cells. Plant Physiol. 1995 Sep;109(1):277–284. doi: 10.1104/pp.109.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Moss S. E. Annexins. Trends Cell Biol. 1997 Mar;7(3):87–89. doi: 10.1016/S0962-8924(96)10049-0. [DOI] [PubMed] [Google Scholar]
  38. Okita Thomas W., Rogers John C. COMPARTMENTATION OF PROTEINS IN THE ENDOMEMBRANE SYSTEM OF PLANT CELLS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):327–350. doi: 10.1146/annurev.arplant.47.1.327. [DOI] [PubMed] [Google Scholar]
  39. Proust J., Houlné G., Schantz M. L., Schantz R. Characterization and gene expression of an annexin during fruit development in Capsicum annuum. FEBS Lett. 1996 Apr 1;383(3):208–212. doi: 10.1016/0014-5793(96)00252-9. [DOI] [PubMed] [Google Scholar]
  40. Randall S. K. Characterization of vacuolar calcium-binding proteins. Plant Physiol. 1992 Oct;100(2):859–867. doi: 10.1104/pp.100.2.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rothman J. E. The protein machinery of vesicle budding and fusion. Protein Sci. 1996 Feb;5(2):185–194. doi: 10.1002/pro.5560050201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Saunders J. A. Investigations of vacuoles isolated from tobacco: I. Quantitation of nicotine. Plant Physiol. 1979 Jul;64(1):74–78. doi: 10.1104/pp.64.1.74. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Taiz L. THE PLANT VACUOLE. J Exp Biol. 1992 Nov 1;172(Pt 1):113–122. doi: 10.1242/jeb.172.1.113. [DOI] [PubMed] [Google Scholar]
  44. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Walker-Simmons M., Ryan C. A. Immunological Identification of Proteinase Inhibitors I and II in Isolated Tomato Leaf Vacuoles. Plant Physiol. 1977 Jul;60(1):61–63. doi: 10.1104/pp.60.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. 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 May;99(1):161–169. doi: 10.1104/pp.99.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES