Structure and function of plasma membrane amino acid, oligopeptide and sucrose transporters from higher plants

Journal of Membrane Biology

Volumn 162, Issue 3, 1998, Pages 177-190

  Rentsch, D ^a   Boorer, K J ^b   Frommer, W B ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amino acid permease; Amino acid transport; Arabidopsis; Expression cloning; Membrane proteins; Peptide transporter; Plant; Solanaceae; Sucrose transporter; Xenopus oocytes; Yeast

Indexed keywords

AMINO ACID; CARRIER PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; OLIGOPEPTIDE; SUCROSE;

AMINO ACID SEQUENCE; AMINO ACID TRANSPORT; ANIMAL CELL; CARBOHYDRATE TRANSPORT; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EUKARYOTE; HIGHER PLANT; MEMBRANE TRANSPORT; NONHUMAN; OOCYTE; PROTEIN ANALYSIS; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; XENOPUS;

EID: 0032055430     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s002329900355     Document Type: Review

References (124)

1. Albritton, L.M., Tseng, L., Scadden, D., Cunningham, J.M. 1989. A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 57:659-666
2. Aldrich, R. 1993. Potassium channels-advent of a new family. Nature 362:107-108
3. +/peptide symporter PEPT1 expressed in Xenopus laevis oocytes. J. Membrane Biol. 155:247-256
4. Anderson, J.A., Huprikar, S.S., Kochian, L.V., Lucas, W.J., Gaber, R.F. 1992. Functional expression of a probable potassium channel in Saccharomyces cerevisiae Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 89:3736-3740
5. André B. 1995. An overview of membrane transport proteins in Saccharomyces cerevisiae. Yeast 11:1575-1611
6. Bennett, M.J., Marchant, A., Green, H.G., May, S.T., Ward, S.P., Millner, P.A., Walker, A.R., Schulz, B., Feldmann, K.A. 1996. The Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science 273:948-950
7. + channel from Arabidopsis thaliana, and comparison with endogenous yeast channels and carriers. Proc. Natl. Acad. Sci. USA 92:2701-2705
8. Bissig, M., Hagenbuch, B., Stieger, B., Koller, T., Meier, P. 1994. Functional expression cloning of the canalicular sulfate transport system of rat hepatocytes. J. Biol Chem. 269:3017-3021
9. +/hexose cotransporter (STP1) from Arabidopsis thaliana expressed in Xenopus oocytes. J. Biol. Chem. 269:20417-20424
10. +/amino acid transporter from Arabidopsis thaliana. J. Biol. Chem. 271:2213-2220
11. +/sucrose cotransporter StSUC1. J. Biol. Chem. 271:25139-25144
12. +/amino acid transporter AAP5. J. Biol. Chem. 272:13040-13046
13. Bush, D.R. 1990. Electrogenicity, pH-dependence, and stoichiometry of the proton-sucrose symport. Plant Physiol. 93:1590-1596
14. Bush, D.R. 1993. Proton-coupled sugar and amino acid transporters in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:513-542
15. Chrispeels, M.J., Agre, P. 1994. Aquaporins: water channel proteins of plant and animal cells. Trends Biochem. Sci. 19:421-425
16. Closs, E.I., Lyons, C.R., Kelly, C., Cunningham, J.M. 1993. Characterization of the third member of the MCAT family of cationic amino acid transporters. J. Biol. Chem. 268:20796-20800
17. Deisenhofer, J., Epp, O., Sinning, I., Michel, H. 1995. Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J. Mol. Biol. 246:429-457
18. Delrot, S. 1981. Proton fluxes associated with sugar uptake in Vicia faba leaf tissue. Plant Physiol. 68:706-711
19. Delrot, S. 1989. Phloem loading. In: Transport of Photoassimilates. D.A. Baker and J.A. Milburn, editors. pp. 167-205. Longman Scientific, London
20. Deuvreux, J., Haeberli, P., Smithies, O. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395
21. DeWitt, N.D., Harper, J.F., Sussman, M.R. 1991. Evidence for a plasma membrane proton pump in phloem cells of higher plants. Plant J. 1:121-128
22. Fei, Y.J., Kanai, Y., Nussberger, S., Ganapathy, V., Leibach, F.H., Romero, M.F., Singh, S.K., Boron, W.F., Hediger, M.A. 1994. Expression cloning of a mammalian proton-coupled oligopeptide transporter. Nature 368:563-566
23. Felsenstein, J. 1993. PHYLIP (Phylogeny Interference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle
24. Fischer, W.N., Kwart, M., Hummel, S., Frommer, W.B. 1995. Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J. Biol Chem. 270:16315-16320
25. Frillingos, S., Kaback, H.R. 1996. Probing the conformation of the lactose permease of Escherichia coli by in situ site-directed sulfhydryl modification. Biochem. 35:3950-3956
26. Frommer, W.B., Hummel, S., Riesmeier, J.W. 1993. Yeast expression cloning of a cDNA encoding a broad specificity amino-acid permease from Arabidopsis thaliana. Proc. Natl. Acad. Sci USA 90:5944-5948
27. Frommer, W.B., Hummel, S., Rentsch, D. 1994a. Cloning of an Arabidopsis histidine transporting protein related to nitrate and peptide transporters. FEBS Lett. 347:185-189
28. Frommer, W.B., Kwart, M., Hirner, B., Fischer, W.N., Hummel, S., Ninnemann, O. 1994b. Transport of nitrogenous compounds in plants. Plant Mol. Biol. 26:1651-1670
29. Frommer, W.B., Ninnemann, O. 1995. Heterologous hosts as expression systems for plant genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46:419-444
30. Frommer, W.B., Hummel, S., Unseld, M., Ninnemann, O. 1995. Seed and vascular expression of a high affinity transporter for cationic amino acids in Arabidopsis. Proc. Natl. Acad. Sci. USA 92:12036-12040
31. + symporter from Plantago major L. supports the model of apoplastic phloem loading. Plant J. 6:697-706
32. Gahrtz, M., Schmelzer, E., Stolz, J., Sauer, N. 1996. Expression of the PmSUC1 sucrose carrier gene from Plantago major L. is induced during seed development. Plant J. 9:93-100
33. Gallet, O., Lemoine, R., Gaillard, C., Larsson, C., Delrot, S. 1992. Selective inhibition of active uptake of sucrose into plasma membrane vesicles by polyclonal sera directed against a 42 kilodalton plasma membrane polypeptide. Plant Physiol. 98:17-23
34. +-ATPase isoforms expressed in yeast. J. Biol. Chem. 269:3027-3033
35. Grimes, H.D., Overvoorde, P.J., Ripp, K., Franceschi, V.R., Hitz, W.D. 1992. A 62-kD sucrose binding protein is expressed and localized in tissues actively engaged in sucrose transport. Plant Cell 4:1561-1574
36. +-ATPase. Planta 185:527-537
37. Hare, J.F. 1990. Mechanism of protein turnover. Biophys. Acta 1031:71-90
38. +-ATPase genes from potato. Plant Mol. Biol. 26:979-988
39. Harrington, G.N., Franceschi, V.R., Offler, C.E., Patrick, J.W., Harper, J.F., Frommer, W.B., Tegeder, M., Hitz, W.D. 1997. Cell specific expression of three genes involved in plasma membrane sucrose transport in developing Vicia faba seed. Protoplasma 197:160-173
40. Hästbacka, J., de la Chapelle, A., Mahtani, M.M., Clines, G., Reeve-Daly, M.P., Daly, M., Hamilton, B.A., Kusumi, K., Trivedi, B., Weaver, A., Coloma, A., Lovett, M., Buckler, A., Kaitila, I., Lander, E.S. 1994. The diastrophic dysplasia gene encodes a novel sulfate transporter: positional cloning by fine-structure linkage disequilibrium mapping. Cell 78:1073-1087
41. Hechenberger, M., Schwappach, B., Fischer, W.N., Frommer, W.B., Jentsch, T.J., Steinmeyer, K. 1996. A family of putative chloride channels from Arabidopsis and functional complementation of a yeast strain with a CLC gene disruption. J. Biol. Chem. 271:33632-33638
42. +/glucose cotransporter. Nature 330:379-381
43. Hein, C., Springael, J.Y., Volland, C., Haguenauer-Tsapis, R., André, B. 1995. NPI1, an essential yeast gene involved in induced degradation of Gap 1 and Fur4 permeates, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18:77-87
44. Henderson, P.J. 1990. Proton-linked sugar transport systems in bacteria. J. Bioenerg. Biomembr. 22:525-69
45. Higgins, C.E., Payne, J.W. 1978. Peptide transport by germinating barley embryos. Planta 138:217-221
46. Higgins, C.F., Hyde, S.C., Mimmack, M.M., Gileadi, U., Gill, D.R., Gallagher, M.P. 1990. Binding protein-dependent transport systems. J. Bionenerg. Biomembr. 22:571-592
47. 2+ exchange current magnitudes determined from channel-like noise and charge movements of ion transport. Biophys. J. 71:759-768
48. +/glucose cotransporter (SGLT1). J. Biol. Chem. 269:21407-21410
49. +/glucose cotransporter. J. Biol. Chem. 272:2110-2115
50. +/amino acid permease gene expression during seed development of Arabidopsis. Plant J. (in press)
51. +/glucose cotransporter expression by protein kinases in Xenopus laevis oocytes. J. Biol. Chem. 271:14740-14746
52. Hsu, L., Chiou, T., Chen, L., Bush, D.R. 1993. Cloning a plant amino acid transporter by functional complementation of a yeast amino acid transport mutant. Proc. Natl. Acad. Sci. USA 90:7441-7445
53. Jauch, P., Luger, P. 1986. Electrogenic properties of the sodium-alanine cotransporter in pancreatic acinar cells. II. Comparison with transport models. J. Membrane Biol. 94:117-127
54. Jauniaux, J.C., Vandenbol, M., Vissers, S., Broman, K., Grenson, M. 1987. Nitrogen catabolite regulation of proline permease in Saccharomyces cerevisiae. Cloning of the PUT4 gene and study of PUT4 RNA levels in wild-type and mutant strains. Eur. J. Biochem. 164:601-606
55. Jentsch, T.J. 1996. Chloride channels: a molecular perspective. Curr. Opin. Neurobiol. 6:303-10
56. Kasahara, T., Kasahara, M. 1996. Expression of the rat GLUT1 glucose transporter in the yeast Saccharomyces cerevisiae. Biochem. J. 315:177-182
57. Kim, J.W., Closs, E.I., Albritton, L.M., Cunningham, J.M. 1991. Transport of cationic amino acids by the mouse ecotropic retrovirus receptor. Nature 352:725-728
58. Koo, K., Stuart, W.D. 1991. Sequence and structure of mtr, an amino acid transport gene of Neurospora crassa. Genome 34:644-651
59. Kühn, C., Quick, W.P., Schulz, A., Sonnewald, U., Frommer, W.B. 1996. Companion cell-specific inhibition of the potato sucrose transporter SUT1. Plant Cell Envir. 19:1115-1123
60. Kühn, C., Franceschi, V.R., Schulz, A., Lemoine, R., Frommer, W.B. 1997. Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Saence 275:1298-1300
61. Kuehn, M.J., Schekman, R., Ljungdahl, P.O. 1996. Amino acid permeases require COPII components and the ER resident membrane protein Shr3p for packaging into transport vesicles in vitro. J. Cell Biol. 135:585-595
62. Kwart, M., Hirner, B., Hummel, S., Frommer, W.B. 1993. Differential expression of two related amino-acid transporters with differing substrate specificity in Arabidospsis thaliana. Plant J. 4:993-1002
63. Lauter, F.R., Ninnemann, O., Bucher, M., Riesmeier, J.W., Frommer, W.B. 1996. Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. Proc. Natl. Acad. Sci. USA 93:8139-8144
64. Leggewie, G., Willmitzer, L., Riesmeier, J.W. 1997. Two cDNAs from potato are able to complement a phosphate uptake deficient yeast mutant: identification of phosphate transporters from higher plants. Plant Cell 9:381-392
65. Lemoine, R., Gallet, O., Gaillard, C., Frommer, W., Delrot, S. 1992. Plasma membrane vesicles from source and sink leaves: Changes in solute transport and polypeptide composition. Plant Physiol. 100:1150-1156
66. Lemoine, R., Kühn, C., Thiele, N., Delrot, S., Frommer, W.B. 1996. Antisense inhibition of the sucrose transporter in potato: Effects on amount and activity. Plant Cell Environ. 19:1124-1131
67. Li, Z.S., Gallet, O., Gaillard, C., Lemoine, R., Delrot, S. 1992. The sucrose carrier of the plant plasmalemma: III. Partial purification and reconstitution of active sucrose transport in liposomes. Biochim. Biophys. Acta 1103:259-267
68. Li, Z., Bush, D.R. 1990. ΔpH-dependent amino acid transport into plasma membrane vesicles isolated from sugar beet leaves. Plant Physiol. 94:268-277
69. Li, Z., Bush, D.R. 1991. ΔpH-dependent amino acid transport into plasma membrane vesicles isolated from sugar beet (Beta vulgaris L.) leaves. Plant Physiol. 96:1338-1344
70. Li, Z., Bush, D.R. 1992. Structural determinants in substrate recognition by proton-amino acid symports in plasma membrane vesicles isolated from sugar beet leaves. Arch. Biochem. Biophys. 294:519-526
71. Ljungdahl, P.O., Gimeno, C.J., Styles, C.A., Fink, G.R. 1992. SHR3, a novel component of the secretory pathway specifically required for localization of amino acid permeases in yeast. Cell 71:463-478
72. Lomax, T.L., Muday, G.K Rubery, P.H. 1995. Auxin transport. In: Plant Hormones. P.J. Davies, editor. pp. 509-530 Kluwer Publ. Dordrecht
73. Loo, D.D.F., Hirsch, J.R., Sarkar, H.K., Wright, E.M. 1996. Regulation of the mouse retinal taurine transporter (TAUT) by protein kinases in Xenopus oocytes. FEBS Lett. 392:250-254
74. Lu, C.C., Kabakov, A., Markin, V.S., Mager, S., Frazier, G.A., Hilgemann, D.W. 1995. Membrane transport mechanisms probed by capacitance measurements with megahertz voltage clamp. Proc. Natl. Acad. Sci. USA 92:11220-11224
75. Malandro, M.S., Kilberg, M.S. 1996. Molecular biology of mammalian amino acid transporters. Annu. Rev. Biochem. 65:305-336
76. Marger, M.D., Saier Jr., M.H. 1993. A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem. Sci. 18:13-20
77. Maynard, J.W., Lucas, W.J. 1982. Sucrose and glucose uptake in Beta vulgaris leaf tissue. A case for a general (apoplastic) retrieval system. Plant Physiol. 70:1436-1443
78. Medintz, I., Jiang, H., Han, E.K., Cui, W., Michels, C.A. 1996. Characterization of the glucose-induced inactivation of maltose permease in Saccharomyces cerevisiae. J. Bact. 178:2245-2254
79. Milpetz, F., Argos, P. 1995. TMAP: a new email and WWW service for membrane-protein structural predictions. TIBS 20:204-205
80. Murer, H., Biber, J. 1996. Molecular mechanisms of renal apical Na/phosphate cotransport. Annu. Rev. Physiol. 58:607-18
81. Nakamura, S., Hayashi, H., Mori, S., Chino, M. 1993. Protein phosphorylation in the sieve tubes of rice plants. Plant Cell Physiol. 34:927-933
82. Ninnemann, O.W., Jauniaux, J.C., Frommer, W.B. 1994. Identification of a high affinity ammonium transporter from plants. EMBO J. 13:3464-3471
83. Offler, C.E., Patrick, J.W. 1993. Pathway of photosynthate transfer in the developing seed of Vicia faba L: A structural assessment of the role of transfer cells in unloading from the seed coat. J. Exp. Biol. 44:711-724
84. Ooi, C.E., Rabinovich, E., Dancis, A., Bonifacino, J.S., Klausener, R.D. 1996. Copper-dependent degradation of the Saccharomyces cerevisiae plasma membrane copper transporter Ctr1p in the apparent absence of endocytosis. EMBO J. 15:3515-3523
85. Ostermeier, C., Iwata, S., Ludwig, B., Michel, H. 1995. Fv fragment-mediated crystallization of the membrane protein bacterial cytochrome c oxidase. Nat. Struct. Biol. 2:842-846
86. Overall, R.L., Blackman, L.M. 1996. A model of the macromolecular structure of plasmodesmata. Trends Plant Sci. 1:307-311
87. Overvoorde, P.J., Frommer, W.B., Grimes, H.D. 1996. A soybean sucrose binding protein independently mediates nonsaturable sucrose uptake in yeast. Plant Cell 8:271-280
88. Panayotova-Heiermann, M., Loo, D.D.F., Lostao, M.P., Wright, E.M. 1994. Sodium/D-glucose cotransporter charge movements involve polar residues. J. Biol. Chem. 269:21016-21020
89. Perry, J.R., Basrai, M.A., Steiner, H.Y., Peer, F., Becker, J.M. 1994. Isolation and characterization of a Saccharomyces cerevisiae peptide transport gene. Mol. Cell. Biol. 14:104-115
90. Prive, G.G., Kaback, H.R. 1996. Engineering the lac permease for purification and crystallization. J. Bioenerg. Biomembr. 28:29-34
91. Reizer, J., Finley, K., Kakuda, D., MacLeod, C., Reizer, A., Saier, M.H. 1993. Mammalian integral membrane receptors are homologous to facilitators and antiporters of yeast, fungi and eubacteria. Protein Sci. 2:20-30
92. Rentsch, D., Laloi, M., Rouhara, I., Schmelzer, E., Delrot, S., Frommer, W.B. 1995. NTR1 encodes a high affinity oligopeptide transporter in Arabidopsis. FEBS Lett. 370:264-268
93. Rentsch, D., Hirner, B., Schmelzer, E., Frommer, W.B. 1996. Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permease genes identified by suppression of an amino acid transport targeting mutant. Plant Cell 8:1437-1446
94. Rentsch, D., Frommer, W.B. 1996. Molecular approaches towards an understanding of loading and unloading of assimilates in higher plants. J. Exp. Bot. 47:1199-1204
95. Riesmeier, J.W., Willmitzer, L., Frommer, W.B. 1992. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 11:4705-4713
96. Riesmeier, J.W., Hirner, B., Frommer, W.B. 1993. Expression of the sucrose transporter from potato correlates with the sink-to-source transition in leaves. Plant Cell 5:1591-1598
97. Riesmeier, J.W., Willmitzer, L., Frommer, W.B. 1994. Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J. 13:1-7
98. Ripp, K.G., Viitanen, P.V., Hitz, W.D., Franceschi, V.R. 1988. Identification of a membrane protein associated with sucrose transport into cells of developing soybean cotyledons. Plant Physiol. 88:1435-1445
99. Rubio, R., Gassmann, W., Schroeder, J.I. 1995. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660-1663
100. Sauer, N., Friedländer, K., Gräml-Wicke, U. 1990. Primary structure, genomic organization and heterologous expression of a glucose transporter from A. thaliana. EMBO J. 9:3045-3050
101. Sauer, N., Stolz, J. 1994. SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana: expression and characterization in baker's yeast and identification of the histidine-tagged protein. Plant J. 6:67-77
102. Sauer, N., Gahrtz, M., Stadler, R., Stolz, J., Truernit, E. 1994a. Molecular biology of sugar transporters of the plant plasma membrane. Symp. Soc. Exp. Biol. 48:155-165
103. Sauer, N., Baier, K., Gahrtz, M., Stadler, R., Stolz, J., Truernit, E. 1994b. Sugar transport across the plasma membranes of higher plants. Plant Mol. Biol. 26:1671-1679
104. Schobert, C., Grossmann, P., Gottschalk, M., Komor, E., Pecsvaradi, A., Nieden, U.Z. 1995. Sieve-tube exudate from Ricinus communis L. seedlings contains ubiquitin and chaperones. Planta 196:205-210
105. Segel, G.B., Boal, T.R., Cardillo, T.S., Murant, F.C., Lichtman, M.A., Sherman, F. 1992. Isolation of a gene encoding a chaperonin-like protein by complementation of yeast amino acid transport mutants with human cDNA. Proc. Natl. Acad. Sci. USA 89:6060-6064
106. Sentenac, H., Bonneaud, N., Minet, M., Lacroute, F., Salmon, J.M., Gaymard, F., Grignon, C. 1992. Cloning and expression in yeast of a plant potassium ion transport system. Science 256:663-665
107. Slone, J.H., Buckhout, T.J. 1991. Sucrose-dependent proton transport in plasma-membrane vesicles isolated from sugar-beet leaves (Beta vulgaris L.): Evidence in support of the proton-symport model for sucrose transport. Planta 183:584-589
108. Smith, F.W., Ealing, P.M., Hawkesford, M.J., Clarkson, D.T. 1995. Plant members of a family of sulfate transporters reveal functional subtypes. Proc. Natl. Acad. Sci. USA 92:9373-9377
109. Song, W., Steiner, H.Y., Zhang, L., Naider, F., Stacey, G., Becker, J.M. 1996. Cloning of a second arabidopsis peptide transport gene. Plant Physiol. 110:171-178
110. Sopanen, T. 1979. Development of peptide transport activity in barley scutellum during germination. Plant Physiol. 64:570-574
111. Steiner, H.Y., Song, W., Zhang, L., Naider, F., Becker, J.M., Stacey, G. 1994. An Arabidopsis peptide transporter is a member of a novel family of membrane transport proteins. Plant Cell 6:1289-1299
112. Stolz, J., Darnhofer-Demar, B., Sauer, N. 1995. Rapid purification of a functionally active plant sucrose carrier from transgenic yeast using a bacterial biotin acceptor domain. FEBS Lett. 377:167-171
113. Taglialatella, M., Toro, L., Stefani, E. 1992. Novel voltage clamp to record small, fast currents from ion channels expressed in Xenopus oocytes. Biophys. J. 61:78-82
114. Tanaka, J., Fink, G.R. 1985. The histidine permease gene (HIP1) of Saccharomyces cerevisiae. Gene 38:205-214
115. Tanner, W., Caspari, T. 1996. Membrane transport carriers. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:595-626
116. Thorens, B. 1996. Glucose transporters in the regulation of intestinal, renal, and liver glucose fluxes. Am. J. Physiol. 270:541-553
117. + symporter gene directs expression of β-glucuronidase to the phloem: Evidence for phloem loading and unloading by SUC2. Planta 196:564-570
118. Tsay, Y., Schroeder, J.I., Feldmann, K.A., Crawford, N.M. 1993. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705-713
119. Vandenbol, M., Jauniaux, J.C., Grenson, M. 1990. The Saccharomyces cerevisiae NPR1 gene required for the activity of ammonia-sensitive amino acid permeases encodes a protein kinase homologue. Mol. Gen. Genet. 222:393-399
120. Ward, J.M. 1997. Patch-clamping and other molecular approaches for the study of plasma membrane transporters demystified. Plant Physiol. 114:1151-1159
121. Ward, J.M., Kühn, C., Tegeder, M., Frommer, W.B. 1997. Sucrose transport in plants. Int. Rev. Cytol. (in press)
122. Warmbrodt, R.D., Buckhout, T.J., Hitz, W.D. 1989. Localization of a protein, immunologically similar to a sucrose binding protein from developing soybean cotyledons, on the plasma membrane of sieve tube members of spinach leaves. Planta 180:105-115
123. Weig, A., Komor, E. 1996. An active sucrose carrier (Scr 1) that is predominantly expressed in the seedling of Ricinus communis L. J. Plant Physiol. 147:685-690
124. Wright, E.M., Loo, D.D.F., Panayotova-Heiermann, M., Lostao, M.P., Hirayama, B.H. 1994. 'Active' sugar transport in eukaryotes. J. Exp. Biol. 196:197-212