Selective expression of a novel high-affinity transport system for acidic and neutral amino acids in the tapetum cells of Arabidopsis flowers

Plant Journal

Volumn 40, Issue 1, 2004, Pages 60-74

  Lee, Yong Hwa ^a   Tegeder, Mechthild ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Amino acid transport; Arabidopsis; Flower bud; in situ RT PCR; Microspore development; Tapetum

Indexed keywords

ACIDITY; AMINO ACIDS; CELLS; NITROGEN; SYNTHESIS (CHEMICAL);

CELLULAR EXPRESSION; FLOWER BUDS; HIGH-AFFINITY TRANSPORT SYSTEM; MICROSPOROGENESIS;

PLANTS (BOTANY);

AMINO ACID; AMINO ACID TRANSPORTER; ARABIDOPSIS PROTEIN; DICARBOXYLIC AMINO ACID; MESSENGER RNA; PLANT RNA;

ARABIDOPSIS; ARTICLE; FLOWER; GENETICS; KINETICS; METABOLISM;

AMINO ACID TRANSPORT SYSTEMS; AMINO ACIDS, DICARBOXYLIC; AMINO ACIDS, NEUTRAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; KINETICS; RNA, MESSENGER; RNA, PLANT;

AMINO ACIDS; CELLS; FLOWERS; NITROGEN; PLANTS;

ARABIDOPSIS; EMBRYOPHYTA; EUKARYOTA;

EID: 5144227859     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02186.x     Document Type: Article

References (77)

1. An, Y.-Q., McDowell, J.M., Huang, S.R., McKinney, E.C., Chambliss, S. and Meagher, R.B. (1996) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J. 10, 107-121.
2. Banga, S.S., Labana, K.S. and Banga, S.K. (1984) Mail sterility in Indian mustard (Brassica juncea (L) Coss.). A biochemical characterization. Theor. Appl. Genet, 67, 515-518.
3. Bennett, M.J., Marchant A., Green, H.G., May, S.T., Ward, S.P., Millner, P.A., Walker, A.R., Schultz, B. and Feldmann, K.A. (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science, 273, 948-950.
4. +/amino acid transporter AAP5. J. Biol. Chem. 272, 13040-13046.
5. + amino acid transporter from Arabidopsis thaliana. J. Biol. Chem. 271, 2213-2220.
6. Bowman, J.L., Drews, G.N. and Meyerowitz, E.M. (1991) Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell, 3, 749-758.
7. Chen, L.S. and Bush, D.R. (1997) LHT1, a lysine- and histidine-specific amino acid transporter in Arabidopsis. Plant Physiol. 115, 1127-1134.
8. Chen, L.S., Ortiz-Lopez, A., Jung, A. and Bush, D.R. (2001) ANT1, an aromatic and neutral amino acid transporter in Arabidopsis. Plant Physiol. 125, 1813-1820.
9. Clément, C. and Audran, J.C. (1995) Anther wall layers control pollen sugar nutrition in Lilium. Protoplasma, 187, 172-181.
10. Clément, C., Burrus, M. and Audran, J.C. (1996) Floral organ growth and carbohydrate content during pollen development in Lilium. Am. J. Bot. 83, 459-469.
11. Cserzö, M., Wallin, E., Simon, I., von Heijne, G. and Elofsson, A. (1997) Prediction of transmembrane α-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng. 10, 673-676.
12. De Block, M. and Debrouwer, D. (1993) Engineered fertility control in transgenic Brassica napus L.: histochemical analysis of anther development. Planta, 189, 218-225.
13. Deeken, R. and Kaldenhoff, R. (1997) Light-repressible receptor protein kinase: a novel photo-regulated gene from Arabidopsis thaliana. Planta, 202, 479-486.
14. Delrot, S., Atanassova, R. and Maurousset, L. (2000) Regulation of sugar, amino acid and peptide plant membrane transporters. BBA-Biomembranes, 1465, 281-306.
15. Dohmen, R.J., Strasser, A.W.M., Höner, C.B. and Hollenberg, C. (1991) An efficient transformation procedure enabling long-term storage of competent cells of various yeast genera. Yeast, 7, 691-692.
16. Echlin, P. (1971) The role of the tapetum during microsporogenesis of angiosperme. In Pollen: Development and Physiology (Heslop-Harrison, J., ed.). London: Butterworhs, pp. 41-61.
17. Fischer, W.N. (1997) Substratspezifität und Transportmechanismus pflanzlicher Aminosäuren in Relation zu ihrer physiologischen Funktion. Ph.D. Thesis. Eberhard-Karls-Universtity, Tübingen, pp. 1-135.
18. Fischer, W.N., Kwart, M., Hummel, S. and Frommer, W.B. (1995) Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J. Biol. Chem. 270, 16315-16320.
19. Fischer, W.N., André, B., Rentsch, D., Krolkiewicz, S., Tegeder, M., Breitkreuz, K. and Frommer, W.B. (1998) Amino acid transport in plants. Trends Plant Sci. 3, 188-195.
20. +-cotransporters for cellular import of neutral and charged amino acids. Plant J. 29, 717-731.
21. Frommer, W.B., Hummel, S. and Riesmeier, J.W. (1993) Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 90, 5944-5948.
22. Frommer, W.B., Hummel, S. and Rentsch, D. (1994) Cloning of an Arabidopsis histidine transporting protein related to nitrate and peptide transporters. FEBS Lett. 347, 185-189.
23. Frommer, W.B., Hummel, S., Unseld, M. and 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.
24. Gifford, R.M., Thorne, J.H., Hitz, W.D. and Giaquinta, R.T. (1984) Crop productivity and photo assimilate partitioning. Science, 225, 801-808.
25. Goldberg, R.B., Beals, T.P. and Sanders, P.M. (1993) Anther development: basic principles and practical applications. Plant Cell, 5, 1217-1229.
26. Harrington, G.N., Franceschi, V.R., Offler, C.E., Patrick, J.W., Tegeder, M., Frommer, W.B., Harper, J.F. and 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.
27. Hesse, M. and Hess, M.W. (1993) Recent trends in tapetum research. A cytological and methodological review. In The Tapetum: Cytology, Function, Biochemistry and Evolution (Hesse, M., Pacini, E. and Willemse, M.T.M., eds). Plant Syst. Evol. (Suppl. 7), 127-145.
28. Hofmann, K. and Stoffel, W. (1993) A database of membrane spanning protein segments. Biol. Chem. 374, 166.
29. Horner, M. and Pratt, M.L. (1979) Amino acid analysis of in vivo and androgenic anthers of Nicotiana tabacum. Protoplasma, 98, 279-282.
30. Hsu, L.C., Chiou, T.J., Chen, L. and 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.
31. Jauniaux, J.C., Vandenbol, M., Vissers, S., Broman, K. and 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.
32. Keijzer, C.J., Hoek, I.H. and Willemse, M.T.M. (1987) The development of staminal filament of Gasteria verrucosa. Acta Bot. Neerl. 36, 271-282.
33. Koltai, H. and Bird, D.M. (2000) High throughput cellular localization of specific plant mRNAs by liquid-phase in situ reverse transcription-polymerase chain reaction of tissue sections. Plant Physiol. 123, 1203-1212.
34. Krogaard, H. and Anderson, A.S. (1983) Free amino acids of Nicotiana alata anthers during development in vivo. Physiol. Plant. 57, 527-531.
35. Kühn, C., Franceschi, V.R., Schulz, A., Lemoine, R. and Frommer, W.B. (1997) Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science, 275, 1298-1300.
36. Kwart, M., Hirner, B., Hummel, S. and Frommer, W.E. (1993) Differential expression of two related amino acid transporters with differing substrate specificity in Arabidopsis thaliana. Plant J. 4, 993-1002.
37. Lalanne, E., Mathieu, C., Roche, O., Vedel, F. and DePape, R. (1997) Structure and specific expression of a Nicotiana sylvestris putative amino-acid transporter gene in mature and in vitro germinating pollen. Plant Mol. Biol. 35, 855-864.
38. Lalonde, S., Tegeder, M., Throne-Holst, M., Frommer, W.B. and Patrick, J.W. (2003) Phloem loading and unloading of sugars and amino acids. Plant Cell Environ. 26, 37-56.
39. Lam, H.-M., Coschigano, K., Schultz, C., Melo-Oliveira, R., Tjaden, G., Oliveira, I., Ngai, N., Hsieh, M.-H. and Coruzzi, G. (1995) Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis. Plant Cell, 7, 887-898.
40. Lee, Y.-H., Chung, K.-H., Kim, H.-U., Jin, Y.-M., Kim, H.-I. and Park, B.-S. (2003) Induction of male sterile cabbage using a tapetum-specific promoter from Brassica campestris L. ssp. pekinensis. Plant Cell Rep. 22, 268-273.
41. Lemoine, R., Burkle, L., Barker, L., Sakr, S., Kuhn, C., Regnacq, M., Gaillard, C., Delrot, S. and Frommer, W.B. (1999) Identification of a pollen-specific sucrose transporter-like protein NtSUT3 from tobacco. FEBS Lett. 454, 325-330.
42. Lohaus, G., Burba, M. and Heldt, H.W. (1994) Comparison of the contents of sucrose and amino acids in the leaves, phloem sap and taproots of high and low sugar-producing hybrids of sugar beet (Beta vulgaris L.). J. Exp. Bot. 45, 1097-1101.
43. Minet, M., Dufour, M.E. and Lacroute, F. (1992) Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 2, 417-422.
44. Müller, A.J. (1961) Zur Charakterisierung der Blüten und Infloreszenzen von Arabidopsis thaliana (L.) Heynh. Kulturpflanze, 9, 364-393.
45. Okumoto, S., Schmidt, R., Tegeder, M., Fischer, W.N., Rentsch, D., Frommer, W.B. and Koch, W. (2002) High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. J. Biol. Chem. 277, 45338-45346.
46. Ortiz-Lopez, A., Chang, H.-C. and Bush, D.R. (2000) Amino acid transporters in plants. Biochem. Biophys. Acta, 1465, 275-280.
47. Pacini, E. (1997) Tapetum character states: analytical keys for tapeturn types and activities. Can. J. Bot. 75, 1448-1459.
48. Pacini, E. and Franchi, G.G. (1993) Role of tapetum in pollen and spore dispersal. In The Tapetum: Cytology, Function, Biochemistry and Evolution (Hesse, M., Pacini, E. and Willemse, M.T.M., eds). Plant Syst. Evol. (Suppl. 7), 127-145.
49. Pacini, E., Franchi, G.G. and Hesse, M. (1985) The tapetum: Its form, function, and possible phylogeny in Embryophyta. Plant Syst. Evol. 149, 155-185.
50. Pacini, E., Taylor, P.E., Singh, M.B. and Knox, R.B. (1992) Development of plastids in pollen and tapetum of rye-grass, Lolium perenne L. Ann. Bot. 70, 179-188.
51. Pate, J.S. (1980) Transport and partitioning of nitrogenous solutes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 31, 3133-3140.
52. Patrick, J.W. (1990) Sieve element unloading: cellular pathway, mechanism and control. Physiol. Plant. 78, 298-308.
53. Przybecki, Z., Kowalczyk, M.E., Siedlecka, E., Urabanczyk-Wochniak, E. and Malepszy, S. (2003) The isolation of cDNA clones from cucumber (Cucumis sativus L.) floral buds coming from plants differing in sex. Cell. Mol. Biol. Lett. 8, 421-438.
54. Rentsch, D., Laloi, M., Rouhara, I., Schmelzer, E., Delrot, S. and Frommer, W.B. (1995) NTR1 encodes a high affinity oligopeptide transporter in Arabidopsis. FEBS Lett. 370, 264-268.
55. Rentsch, D., Hirner, B., Schmelzer, E. and Frommer, W.B. (1996) Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell, 8, 1437-1446.
56. Reznickova, S.A. and Dickinson, H.G. (1982) Ultrastructural aspects of storage lipid mobilization in the tapetum of Lilium hybrida var. enchantment. Planta, 155, 400-408.
57. Riens, B., Lohaus, G., Heinike, D. and Heldt, H.W. (1991) Amino acid and sucrose content determined in the cytosolic, chloroplastic, and vacuolar compartments and in the phloem sap of spinach leaves. Plant Physiol. 97, 227-233.
58. Ruiz-Medrano, R., Xoconostle-Cazares, B. and Lucas, W.J. (1999) Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development, 126, 4405-4419.
59. Sawhney, V.K. and Bhadula, S.K. (1988) Histochemical and biochemical analyses of microsporogenesis in normal and male sterile, Stamenless-2 mutant of tomato. In Sexual Reproduction in Higher Plants (Cresti, M., Gori, P. and Pacini, E., eds). Berlin: Springer Verlag, pp. 187-192.
60. Schneidereit, A., Scholz-Starke, J. and Büttner, M. (2003) Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis. Plant Physiol. 133, 182-190.
61. +-monosaccharide symporter from Arabidopsis. Plant Physiol. 131, 70-77.
62. Schrauwen, J.A.M., Mettenmeyer, T., Croes, A.F. and Wullems, G.J. (1996) Tapetum-specific genes: what role do they play in male gametophyte development? Acta Bot. Neerl. 45, 1-15.
63. Schwacke, R., Grallath, S., Breitkreuz, K.E., Stransky, E., Stransky, H., Frommer, W.B. and Rentsch, D. (1999) LeProT1, a transporter for praline, glycine betaine, and gamma-amino butyric acid in tomato pollen. Plant Cell, 11, 377-391.
64. Scott, R. (1993) Anther development: a molecular perspective. In The Molecular Biology of Flowering (Jordan, B.R., ed.). Wallingford: CAB International, pp. 141-184.
65. Smyth, D.R., Bowman, J.L. and Meyerowitz, E.M. (1990) Early flower development in Arabidopsis. Plant Cell, 2, 755-767.
66. Sonnhammer, E.L.L., von Heijne, G. and Krogh, A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. In Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology (Glasgow, J., Littlejohn, T., Major, F., Lathrop, R., Sankoff, D. and Sensen, C., eds), Menlo Park, CA: American Association for Artificial Intelligence Press, pp. 175-182.
67. Stacey, M.G., Koh, S., Becker, J. and Stacey, G. (2002) AtOPT3, a member of the oligopeptide transporter family, is essential for embryo development in Arabidopsis. Plant Cell, 14, 2799-2811.
68. Stadler, R. and Sauer, N. (1996) The Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells. Bot. Acta, 109, 299-306.
69. Stadler, R., Brandner, J., Schulz, A., Gahrtz, M. and Sauer, N. (1996) Phloem loading by the PmSUC2 sucrose carrier from Plantago major occurs into companion cells. Plant Cell, 7, 1545-1554.
70. Stadler, R., Truernit, E., Gahrtz, M. and Sauer, N. (1999) The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis. Plant J. 19, 269-278.
71. Swofford, D.L. (2001) PAUP* 4.0b10. Phylogenetic Analysis using Parsimony (and Other Methods). Sunderland, MA: Sinauer.
72. Taylor, L.P. and Hepler, P.K. (1997) Pollen germination and tube growth. Annu. Rev. Plant Phys. 48, 461-491.
73. Tegeder, M., Offler, C.E., Frommer, W.B. and Patrick, J.W. (2000) Amino acid transporters are localized to transfer cells of developing pea seeds. Plant Physiol. 122, 319-325.
74. Truernit, E., Stadler, R., Baier, K. and Sauer, M. (1999) A male gametophyte-specific monosaccharide transporter in Arabidopsis. Plant J. 17, 191-201.
75. Wipf, D., Ludewig, U., Tegeder, M., Rentsch, D., Koch, W. and Frommer, W. (2002) Conservation of amino acid transporters in fungi, plants and animals. Trends Biochem. Sci. 27, 139-147.
76. Zhang, H-Q., Croes, A.F. and Linskens, H.F. (1982) Protein synthesis in germinating pollen of Petunia: role of proline. Planta, 154, 199-203.
77. Zheng, Z.F., Xia, Q., Dauk, M., Shen, W.Y., Selvaraj, G. and Zou, J.T. (2003) Arabidopsis AtGPAT1, a member of the membrane-bound glycerol-3-phosphate acyltransferase gene family, is essential for tapetum differentiation and male fertility. Plant Cell, 15, 1872-1887.