Abstract
The tonoplast mediates the transport of various ions and metabolites between the vacuole and cytosol by mechanisms that remain to be elucidated at the molecular level. The primary structure of only one tonoplast protein, the H(+)-ATPase, has been reported to date. Here we report the primary structure of tonoplast intrinsic protein (TIP), a 27-kilodalton intrinsic membrane protein that occurs widely in the tonoplasts of the protein storage vacuoles (protein bodies) of seeds [Johnson, K.D., et al. (1989). Plant Physiol. 91, 1006-1013]. Hydropathy plots and secondary structure analysis of the polypeptide predict six membrane-spanning domains connected by short loops and hydrophilic, cytoplasmically oriented N- and C-terminal regions. TIP displays significant homology with several other membrane proteins from diverse sources: major intrinsic polypeptide from bovine lens fiber plasma membrane; NOD 26, a peribacteroid membrane protein in the nitrogen-fixing root nodules of soybean; and interestingly, GIpF, the glycerol facilitator transport protein in the cytoplasmic membrane of Escherichia coli. Based on the homology between TIP and GIpF and the knowledge that the protein storage vacuolar membrane and the peribacteroid membrane are active in solute transport, we propose that TIP transports small metabolites between the storage vacuoles and cytoplasm of seed storage tissues.
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- Baker M. E., Saier M. H., Jr A common ancestor for bovine lens fiber major intrinsic protein, soybean nodulin-26 protein, and E. coli glycerol facilitator. Cell. 1990 Jan 26;60(2):185–186. doi: 10.1016/0092-8674(90)90731-s. [DOI] [PubMed] [Google Scholar]
- Barbier-Brygoo H., Renaudin J. P., Guern J. The vacuolar membrane of plant cells: a newcomer in the field of biological membranes. Biochimie. 1986 Mar;68(3):417–425. doi: 10.1016/s0300-9084(86)80009-8. [DOI] [PubMed] [Google Scholar]
- Blobel G. Intracellular protein topogenesis. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1496–1500. doi: 10.1073/pnas.77.3.1496. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
- Chou P. Y., Fasman G. D. Prediction of protein conformation. Biochemistry. 1974 Jan 15;13(2):222–245. doi: 10.1021/bi00699a002. [DOI] [PubMed] [Google Scholar]
- Chrispeels M. J., Baumgartner B., Harris N. Regulation of reserve protein metabolism in the cotyledons of mung bean seedlings. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3168–3172. doi: 10.1073/pnas.73.9.3168. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Friedlander M., Blobel G. Bovine opsin has more than one signal sequence. 1985 Nov 28-Dec 4Nature. 318(6044):338–343. doi: 10.1038/318338a0. [DOI] [PubMed] [Google Scholar]
- Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorin M. B., Yancey S. B., Cline J., Revel J. P., Horwitz J. The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning. Cell. 1984 Nov;39(1):49–59. doi: 10.1016/0092-8674(84)90190-9. [DOI] [PubMed] [Google Scholar]
- Hartmann E., Rapoport T. A., Lodish H. F. Predicting the orientation of eukaryotic membrane-spanning proteins. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5786–5790. doi: 10.1073/pnas.86.15.5786. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heller K. B., Lin E. C., Wilson T. H. Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J Bacteriol. 1980 Oct;144(1):274–278. doi: 10.1128/jb.144.1.274-278.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jackson R. J., Hunt T. Preparation and use of nuclease-treated rabbit reticulocyte lysates for the translation of eukaryotic messenger RNA. Methods Enzymol. 1983;96:50–74. doi: 10.1016/s0076-6879(83)96008-1. [DOI] [PubMed] [Google Scholar]
- Johnson K. D., Herman E. M., Chrispeels M. J. An abundant, highly conserved tonoplast protein in seeds. Plant Physiol. 1989 Nov;91(3):1006–1013. doi: 10.1104/pp.91.3.1006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muramatsu S., Mizuno T. Nucleotide sequence of the region encompassing the glpKF operon and its upstream region containing a bent DNA sequence of Escherichia coli. Nucleic Acids Res. 1989 Jun 12;17(11):4378–4378. [PMC free article] [PubMed] [Google Scholar]
- Nelson N., Taiz L. The evolution of H+-ATPases. Trends Biochem Sci. 1989 Mar;14(3):113–116. doi: 10.1016/0968-0004(89)90134-5. [DOI] [PubMed] [Google Scholar]
- Paul D. L., Goodenough D. A. In vitro synthesis and membrane insertion of bovine MP26, an integral protein from lens fiber plasma membrane. J Cell Biol. 1983 Mar;96(3):633–638. doi: 10.1083/jcb.96.3.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rapoport T. A. Extensions of the signal hypothesis--sequential insertion model versus amphipathic tunnel hypothesis. FEBS Lett. 1985 Jul 22;187(1):1–10. doi: 10.1016/0014-5793(85)81202-3. [DOI] [PubMed] [Google Scholar]
- Sandal N. N., Marcker K. A. Soybean nodulin 26 is homologous to the major intrinsic protein of the bovine lens fiber membrane. Nucleic Acids Res. 1988 Oct 11;16(19):9347–9347. doi: 10.1093/nar/16.19.9347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spencer D., Higgins T. J., Button S. C., Davey R. A. Pulse-labeling Studies on Protein Synthesis in Developing Pea Seeds and Evidence of a Precursor Form of Legumin Small Subunit. Plant Physiol. 1980 Sep;66(3):510–515. doi: 10.1104/pp.66.3.510. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Verner K., Schatz G. Protein translocation across membranes. Science. 1988 Sep 9;241(4871):1307–1313. doi: 10.1126/science.2842866. [DOI] [PubMed] [Google Scholar]
- Wessels H. P., Spiess M. Insertion of a multispanning membrane protein occurs sequentially and requires only one signal sequence. Cell. 1988 Oct 7;55(1):61–70. doi: 10.1016/0092-8674(88)90009-8. [DOI] [PubMed] [Google Scholar]
- Zampighi G. A., Hall J. E., Kreman M. Purified lens junctional protein forms channels in planar lipid films. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8468–8472. doi: 10.1073/pnas.82.24.8468. [DOI] [PMC free article] [PubMed] [Google Scholar]
- von Heijne G., Gavel Y. Topogenic signals in integral membrane proteins. Eur J Biochem. 1988 Jul 1;174(4):671–678. doi: 10.1111/j.1432-1033.1988.tb14150.x. [DOI] [PubMed] [Google Scholar]