AAP1 regulates import of amino acids into developing Arabidopsis embryos

Plant Journal

Volumn 59, Issue 4, 2009, Pages 540-552

  Sanders, Ann ^a   Collier, Ray ^a   Trethewy, Alexander ^a   Gould, Grant ^a   Sieker, Renate ^a   Tegeder, Mechthild ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Amino acid transport; Embryo; Endosperm; Nitrogen partitioning; Seed uptake; Storage protein

Indexed keywords

AAP1 PROTEIN, ARABIDOPSIS; AMINO ACID; AMINO ACID TRANSPORTER; ARABIDOPSIS PROTEIN; CARBON; MESSENGER RNA; NITROGEN; PLANT RNA;

ARABIDOPSIS; ARTICLE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT SEED; PRENATAL DEVELOPMENT;

AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; AMINO ACIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBON; NITROGEN; RNA, MESSENGER; RNA, PLANT; SEEDS;

ARABIDOPSIS;

EID: 68849103549     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03890.x     Document Type: Article

References (59)

1. Baud, S., Boutin, J.P., Miquel, M., Lepiniec, L. Rochat, C. (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol. Biochem. 40, 151 160.
2. Beeckman, T., De Rycke, R., Viane, R. Inzé, D. (2000) Histological study of seed coat development in Arabidopsis thaliana. J. Plant Res., 113, 139 148.
3. + co-transport in developing soybean embryos. Plant Physiol. 72, 781 786.
4. +/amino acid transporter from Arabidopsis thaliana. J. Biol. Chem. 271, 2213 2220.
5. +-dependent l-asparaginase. Planta, 224, 668 679.
6. Cakmak, I. Engels, C. (1999) Role of mineral nutrients in photosynthesis and yield formation. In Crop Nutrition (Rengel, Z. ed). New York : Haworth Press, pp. 141 168.
7. Coschigano, K.T., Melo-Oliveira, R., Lim, J. Coruzzi, G.M. (1998) Arabidopsis gls mutants and distinct Fd-GOGAT genes. Implications for photorespiration and primary nitrogen assimilation. Plant Cell, 10, 741 752.
8. DeJong, A., Koerselman-Kooij, J.W., Schuurmans, J.A.M.J. Borstlap, A.C. (1996) Characterization of the uptake of sucrose and glucose by isolated seed coat halves of developing pea seeds. Evidence that a sugar facilitator with diffusional kinetics is involved in seed coat unloading. Planta, 199, 486 492.
9. Dietrich, D., Hammes, U., Thor, K., Suter-Grotemeyer, M., Flückiger, R., Slusarenko, A., Ward, J.M. Rentsch, D. (2004) AtPTR1, a plasma membrane peptide transporter expressed during seed germination and in vascular tissue of Arabidopsis. Plant J. 40, 488 499.
10. Fait, A., Angelovici, R., Less, H., Ohad, I., Urbanczyk-Wochniak, E., Fernie, A.R. Galili, G. (2006) Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiol. 142, 839 854.
11. 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.
12. +-cotransporters for cellular import of neutral and charged amino acids. Plant J. 29, 717 731.
13. Fisher, D.B. (1968) Protein staining of ribboned epon sections for light microscopy. Histochem. Cell Biol. 16, 92 96.
14. Forde, B.G. Lea, P.J. (2007) Glutamate in plants: metabolism, regulation and signaling. J. Exp. Bot. 58, 2339 2358.
15. Frommer, W.B., Hummel, S. 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.
16. Grant, M. Bevan, M.W. (1994) Asparaginase gene expression is regulated in a complex spatial and temporal pattern in nitrogen-sink tissues. Plant J. 5, 695 704.
17. Guerche, P., Tire, C., de Sa, F.G., De Clercq, A., van Montagu, M. Krebbers, E. (1990) Differential expression of the Arabidopsis 2S albumin genes and the effect of increasing gene family size. Plant Cell, 2, 469 478.
18. Gutierrez, L., Mauriat, M., Guénin, S. et al. (2008) The lack of a systematic validation of reference genes: a serious pitfall undervalued in reverse transcription-polymerase chain reaction (RT-PCR) analysis in plants. Plant Biotech. J. 6, 609 618.
19. Hammes, U.Z., Nielsen, E., Honaas, L.A., Taylor, C.G. Schachtman, D.P. (2006) AtCAT6, a sink-tissue-localized transporter for essential amino acids in Arabidopsis. Plant J. 48, 414 426.
20. +/amino acid permease gene expression during seed development of Arabidopsis. Plant J. 14, 535 544.
21. Hirner, A., Ladwig, F., Stransky, H., Okumoto, S., Keinath, M., Harms, A., Frommer, W.B. Koch, W. (2006) Arabidopsis LHT1 is a high affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell, 18, 1931 1946.
22. Hou, A., Liu, K. Catawatcharakul, N. (2005) Two naturally occurring deletion mutants of 12S seed storage proteins in Arabidopsis thaliana. Planta, 222, 512 520.
23. Hsu, L.C., Chiou, T.J., 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.
24. Hunt, E.J., Pritchard, J., Bennett, M.J., Zhu, X., Barrett, D.A., Allen, T., Bale, J.S. Newbury, H.J. (2006) The Arabidopsis thaliana Myzus persicae model system demonstrates that a single gene can influence the interaction between a plant and a sap-feeding insect. Mol. Ecol. 15, 4203 4213.
25. Komarova, N.Y., Thor, K., Gubler, A., Meier, S., Dietrich, D., Weichert, A., Suter Grotemeyer, M., Tegeder, M. Rentsch, D. (2008) AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiol. 148, 856 869.
26. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680 685.
27. Lalonde, S., Tegeder, M., Throne-Holst, M., Frommer, W.B. Patrick, J.W. (2003) Phloem loading and unloading of sugars and amino acids. Plant Cell Environ. 25, 1 20.
28. Lam, H.-M., Peng, S.S. Coruzzi, G.M. (1994) Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol. 106, 1347 1357.
29. Lam, H.-M., Coschiagano, K., Schultz, C., Melo-Oliveira, R., Tjaden, G., Oliveira, I., Ngai, N., Hsieh, M.-H. Coruzzi, G. (1995) Use of Arabidopsis mutants and genes to study amino acid biosynthesis. Plant Cell, 7, 887 898.
30. Lanfermeijer, F.C., Koerselman Kooij, J.W. Borstlap, A.C. (1990) Changing kinetics of l-valine uptake by immature pea cotyledons during development - an unsaturable pathway is supplemented by a saturable system. Planta, 181, 576 582.
31. Lee, Y.-H., Foster, J., Chen, J., Voll, L.M., Weber, A.P.M. Tegeder, M. (2007) AAP1 transports uncharged amino acids into roots of Arabidopsis. Plant J. 50, 305 319.
32. Liu, X. Bush, D.R. (2006) Expression and transcriptional regulation of amino acid transporters in plants. Amino Acids, 30, 113 120.
33. -ΔΔCT method. Methods, 25, 402 408.
34. Lohaus, G. Moellers, C. (2000) Phloem transport of amino acids in two Brassica napus L. genotypes and one B. carinata genotype in relation to their seed protein content. Planta, 211, 833 840.
35. Lott, J.N.A., Greenwood, J.S. Batten, G.D. (1995) Mechanisms and regulation of mineral nutrient storage during seed development. In Seed Development and Germination (Kigel, J. Galili, G. eds). New York : Marcel Dekker, pp. 215 235.
36. Miquel, M. Browse, J. (1992) Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis. Biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase. J. Biol. Chem. 267, 1502 1509.
37. Miranda, M., Borisjuk, L., Tewes, A., Heim, U., Sauer, N., Wobus, U. Weber, H. (2001) Amino acid permeases in developing seeds of Vicia faba L.: expression precedes storage protein synthesis and is regulated by amino acid supply. Plant J. 28, 61 71.
38. Miranda, M., Borisjuk, L., Tewes, A., Dietrich, D., Rentsch, D., Weber, H. Wobus, U. (2003) Peptide and amino acid transporters are differentially regulated during seed development and germination in faba bean. Plant Physiol. 132, 1950 1960.
39. Murashige, T. Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15, 473 497.
40. Okumoto, S., Schmidt, R., Tegeder, M., Fischer, W.N., Rentsch, D., Frommer, W.B. Koch, W. (2002) High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. J. Biol. Chem. 277, 45338 45346.
41. Okumoto, S., Koch, W., Tegeder, M., Fischer, W.N., Biehl, A., Leister, D., Stierhof, Y.D. Frommer, W.B. (2004) Root phloem-specific expression of the plasma membrane amino acid proton co-transporter AAP3. J. Exp. Bot. 55, 2155 2168.
42. Otegui, M.S., Capp, R. Staehelin, L.A. (2002) Developing seeds of Arabidopsis store different minerals in two types of vacuoles and in the endoplasmic reticulum. Plant Cell, 14, 1311 1327.
43. Pélissier, H.C. Tegeder, M. (2007) PvUPS1 plays a role in source-sink transport of allantoin in French bean (Phaseolus vulgaris) Funct. Plant Biol. 34, 282 291.
44. Pélissier, H.C., Frerich, A., Desimone, M., Schumacher, K. Tegeder, M. (2004) PvUPS1, an allantoin transporter in nodulated roots of French bean. Plant Physiol. 134, 664 675.
45. Rentsch, D., Schmidt, S. Tegeder, M. (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett. 581, 2281 2289.
46. Riens, B., Lohaus, G., Heinike, D. 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.
47. Rochat, C. (2001) Transport of amino acids in plants. In Nitrogen Assimilation by Plants (Morot-Gaudry, J.F. ed). Enfield, NH, USA : Science Publishers, pp. 253 267.
48. Schmidt, R., Stransky, H. Koch, W. (2007) The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta, 226, 805 813.
49. Stadler, R., Lauterbach, C. Sauer, N. (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol. 139, 701 712.
50. Svennerstam, H., Ganeteg, U., Bellini, C. Näsholm, T. (2007) Comprehensive screening of Arabidopsis mutants suggests the Lysine Histidine Transporter 1 to be involved in plant uptake of amino acids. Plant Physiol. 143, 1853 1860.
51. Tan, Q., Grennan, A.K., Pélissier, H.C., Rentsch, D. Tegeder, M. (2008) Characterization and expression of French bean amino acid transporter PvAAP1. Plant Sci. 174, 348 356.
52. Tegeder, M. Weber, A.P.M. (2006) Metabolite transporters in the control of plant primary metabolism. In Control of Primary Metabolism in Plants (Plaxton, W.C. McManus, M.T. eds). USA : Blackwell Publishing, pp. 85 120.
53. Tegeder, M., Offler, C.E., Frommer, W.B. Patrick, J.W. (2000) Amino acid transporters are localized to transfer cells of developing pea seeds. Plant Physiol. 122, 319 326.
54. Tegeder, M., Tan, Q., Grennan, A.K. Patrick, J.W. (2007) Amino acid transporter expression and localization studies in pea (Pisum sativum) Funct. Plant Biol. 34, 1019 1028.
55. Tsay, Y.F., Chiu, C.C., Tsai, C.B., Ho, C.H. Hsu, P.K. (2007) Nitrate transporters and peptide transporters. FEBS Lett. 581, 2290 2300.
56. Weigelt, K., Küster, H., Radchuk, R., Müller, M., Weichert, H., Fait, A., Fernie, A.R., Saalbach, I. Weber, H. (2008) Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism and highlights the importance of mitochondrial metabolism. Plant J. 55, 909 926.
57. Wilkinson, T.L. Douglas, A.E. (2003) Phloem amino acids and the host plant range of the polyphagous aphid, Aphis fabae. Entomol. Exp. Appl. 106, 103 113.
58. Winter, D., Vinegar, B., Hardeep, N., Ammar, R., Wilson, G.V. Provart, N.J. (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2, e718.
59. Zhao, S. Fernald, R.D. (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol., 12, 1047 1064.