A tonoplast Glu/Asp/GABA exchanger that affects tomato fruit amino acid composition

Plant Journal

Volumn 81, Issue 5, 2015, Pages 651-660

  Snowden, Christopher J ^a   Thomas, Benjamin ^b   Baxter, Charles J ^c   Smith, J Andrew C ^a   Sweetlove, Lee J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c JEALOTT S HILL INTERNATIONAL RESEARCH CENTRE   (United Kingdom)

Author keywords

amino acid; ripening; tomato; transport; vacuole

Indexed keywords

AMINO ACIDS; METABOLITES; PLANTS (BOTANY); PROTEINS; PROTEOMICS;

AMINO ACID COMPOSITIONS; NUTRITIONAL QUALITIES; QUANTITATIVE PROTEOMICS; RIPENING; TOMATO; TRANSGENIC TOMATO PLANTS; TRANSPORT; VACUOLE;

FRUITS;

LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM;

4 AMINOBUTYRIC ACID; AMINO ACID; ASPARTIC ACID; DIPEPTIDE; GAMMA-GLUTAMYLASPARTIC ACID; GLUTAMIC ACID; PROTEOME; VEGETABLE PROTEIN;

CELL VACUOLE; CYTOLOGY; FRUIT; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; REPORTER GENE; TOBACCO; TOMATO; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACIDS; ASPARTIC ACID; BIOLOGICAL TRANSPORT; DIPEPTIDES; FRUIT; GAMMA-AMINOBUTYRIC ACID; GENES, REPORTER; GLUTAMIC ACID; INTRACELLULAR MEMBRANES; LYCOPERSICON ESCULENTUM; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEOME; TOBACCO; VACUOLES;

EID: 84923412557     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12766     Document Type: Article

References (51)

1. Akihiro, T., Koike, S., Tani, R., et al. (2008) Biochemical mechanism on GABA accumulation during fruit development in tomato. Plant Cell Physiol. 49, 1378-1389.
2. Bettey, M., and, Smith, J.A., (1993) Dicarboxylate transport at the vacuolar membrane of the CAM plant Kalanchoe daigremontiana: sensitivity to protein-modifying and sulphydryl reagents. Biochim. Biophys. Acta, 1152, 270-279.
3. Carrari, F., Baxter, C., Usadel, B., et al. (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol. 142, 1380-1396.
4. Carter, C., Pan, S., Zouhar, J., Avila, E.L., Girke, T., and, Raikhel, N.V., (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell, 16, 3285-3303.
5. Chang, S., Puryear, J., and, Cairney, J., (1993) A simple and effcient method for isolating RNA from pine trees. Plan Mol Biol Rep., 11, 113-116.
6. Deikman, J., and, Fischer, R.L., (1988) Interaction of a DNA binding factor with the 5′-flanking region of an ethylene-responsive fruit ripening gene from tomato. EMBO J. 7, 3315-3320.
7. Denecke, J., Ek, B., Caspers, M., Sinjorgo, K.M.C., and, Palva, E.T., (1993) Analysis of sorting signals responsible for the accumulation of soluble reticuloplasmins in the plant endoplasmic reticulum. J Exp Bot., 44, 213-221.
8. Endler, A., Meyer, S., Schelbert, S., Schneider, T., Weschke, W., Peters, S.W., Keller, F., Baginsky, S., Martinoia, E., and, Schmidt, U.G., (2006) Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol. 141, 196-207.
9. Eshed, Y., and, Zamir, D., (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics, 141, 1147-1162.
10. Fait, A., Fromm, H., Walter, D., Galili, G., and, Fernie, A.R., (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci. 13, 14-19.
11. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., and, Bourguignon, J., (2007) A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell Proteomics, 6, 394-412.
12. Johnson, C., Hall, J.L., and, Ho, L.C., (1988) Pathways of uptake and accumulation of sugars in tomato fruit. Ann. Bot. 61, 593-603.
13. Kessner, D., Chambers, M., Burke, R., Agus, D., and, Mallick, P., (2008) ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics, 24, 2534-2536.
14. Kisaka, H., and, Kida, T., (2003) Transgenic tomato plant carrying a gene for NADP-dependent glutamate dehydrogenase (gdhA) from Aspergillus nidulans. Plant Sci. 164, 35-42.
15. Klee, H.J., and, Giovannoni, J.J., (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu. Rev. Genet. 45, 41-59.
16. Koike, S., Matsukura, C., Takayama, M., Asamizu, E., and, Ezura, H., (2013) Suppression of gamma-aminobutyric acid (GABA) transaminases induces prominent GABA accumulation, dwarfism and infertility in the tomato (Solanum lycopersicum L.). Plant Cell Physiol. 54, 793-807.
17. Linka, N., and, Weber, A.P., (2010) Intracellular metabolite transporters in plants. Mol. Plant, 3, 21-53.
18. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and, Fernie, A.R., (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1, 387-395.
19. Ma, D., Lu, P., Yan, C., Fan, C., Yin, P., Wang, J., and, Shi, Y., (2012) Structure and mechanism of a glutamate-GABA antiporter. Nature, 483, 632-636.
20. Ma, D., Lu, P., and, Shi, Y., (2013) Substrate selectivity of the acid-activated glutamate/gamma-aminobutyric acid (GABA) antiporter GadC from Escherichia coli. J. Biol. Chem. 288, 15148-15153.
21. Martinoia, E., Maeshima, M., and, Neuhaus, H.E., (2007) Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 58, 83-102.
22. Martinoia, E., Meyer, S., De Angeli, A., and, Nagy, R., (2012) Vacuolar transporters in their physiological context. Annu. Rev. Plant Biol. 63, 183-213.
23. Meyer, A., Eskandari, S., Grallath, S., and, Rentsch, D., (2006) AtGAT1, a high affinity transporter for gamma-aminobutyric acid in Arabidopsis thaliana. J. Biol. Chem. 281, 7197-7204.
24. Michaeli, S., Fait, A., Lagor, K., et al. (2011) A mitochondrial GABA permease connects the GABA shunt and the TCA cycle, and is essential for normal carbon metabolism. Plant J. 67, 485-498.
25. Mondal, K., Sharma, N.S., Malhotra, S.P., Dhawan, K., and, Singh, R., (2004) Antioxidant systems in ripening tomato fruits. Biol. Plant, 48, 49-53.
26. Morgan, M.J., Osorio, S., Gehl, B., Baxter, C.J., Kruger, N.J., Ratcliffe, R.G., Fernie, A.R., and, Sweetlove, L.J., (2013) Metabolic engineering of tomato fruit organic acid content guided by biochemical analysis of an introgression line. Plant Physiol. 161, 397-407.
27. Neuhaus, J.M., and, Boevink, P., (2001) The green fluorescent protein (GFP) as a reporter in plant cells. In Plant Cell Biology: A Practical Approach (, Hawes, C., and, Satiat-Jenunemaitre, B., eds). Oxford, UK: Oxford University Press, pp. 127-142.
28. Okumoto, S., and, Pilot, G., (2011) Amino acid export in plants: a missing link in nitrogen cycling. Mol. Plant, 4, 453-463.
29. Oleski, N., Mahdavi, P., Peiser, G., and, Bennett, A.B., (1987) Transport properties of the tomato fruit tonoplast: I. Identification and characterization of an anion-sensitive H-ATPase. Plant Physiol. 84, 993-996.
30. Overy, S.A., Walker, H.J., Malone, S., Howard, T.P., Baxter, C.J., Sweetlove, L.J., Hill, S.A., and, Quick, W.P., (2005) Application of metabolite profiling to the identification of traits in a population of tomato introgression lines. J. Exp. Bot. 56, 287-296.
31. Palmieri, F., Pierri, C.L., De Grassi, A., Nunes-Nesi, A., and, Fernie, A.R., (2011) Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant J. 66, 161-181.
32. Pimpl, P., Hanton, S.L., Taylor, J.P., Pinto-daSilva, L.L., and, Denecke, J., (2003) The GTPase ARF1p controls the sequence-specific vacuolar sorting route to the lytic vacuole. Plant Cell, 15, 1242-1256.
33. Rolin, D., Baldet, P., Just, D., Chevalier, C., Biran, M., and, Raymond, P., (2000) NMR study of low subcellular pH during the development of cherry tomato fruit. Aust. J. Plant Physiol. 27, 61-69.
34. Saier, M.H. Jr, Yen, M.R., Noto, K., Tamang, D.G., and, Elkan, C., (2009) The transporter classification database: recent advances. Nucleic Acids Res. 37, D274-D278.
35. Schauer, N., Semel, Y., Roessner, U., et al. (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat. Biotechnol. 24, 447-454.
36. Schmidt, U.G., Endler, A., Schelbert, S., Brunner, A., Schnell, M., Neuhaus, H.E., Marty-Mazars, D., Marty, F., Baginsky, S., and, Martinoia, E., (2007) Novel tonoplast transporters identified using a proteomic approach with vacuoles isolated from cauliflower buds. Plant Physiol. 145, 216-229.
37. Shelp, B.J., Mullen, R.T., and, Waller, J.C., (2012) Compartmentation of GABA metabolism raises intriguing questions. Trends Plant Sci. 17, 57-59.
38. Shiratake, K., and, Martinoia, E., (2007) Transporters in fruit vacuoles. Plant Biotechnol. 24, 127-133.
39. Sorrequieta, A., Ferraro, G., Boggio, S.B., and, Valle, E.M., (2010) Free amino acid production during tomato fruit ripening: a focus on L-glutamate. Amino Acids, 38, 1523-1532.
40. Stein, W.D., (1990) Channels, Carriers, and Pumps: An Introduction to Membrane transport. San Diego, CA: Academic Press.
41. Su, Y.H., Frommer, W.B., and, Ludewig, U., (2004) Molecular and functional characterization of a family of amino acid transporters from Arabidopsis. Plant Physiol. 136, 3104-3113.
42. Sweetlove, L.J., and, Fernie, A.R., (2013) The spatial organization of metabolism within the plant cell. Annu. Rev. Plant Biol. 64, 723-746.
43. Tegeder, M., (2014) Transporters involved in source to sink partitioning of amino acids and ureides: opportunities for crop improvement. J. Exp. Bot. 65, 1865-1878.
44. The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635-641.
45. Tsai, M.F., McCarthy, P., and, Miller, C., (2013) Substrate selectivity in glutamate-dependent acid resistance in enteric bacteria. Proc. Natl Acad. Sci. USA, 110, 5898-5902.
46. Tusnady, G.E., and, Simon, I., (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics, 17, 849-850.
47. Van Eck, J., Kirk, D.D., and, Walmsley, A.M., (2006) Tomato (Lycopersicum esculentum). In Agrobacterium Protocols (, Wang, K., ed.). New York, NY: Humana Press, pp. 459-474.
48. Whiteman, S.A., Serazetdinova, L., Jones, A.M., Sanders, D., Rathjen, J., Peck, S.C., and, Maathuis, F.J., (2008) Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Arabidopsis thaliana. Proteomics, 8, 3536-3547.
49. Wong, F.H., Chen, J.S., Reddy, V., Day, J.L., Shlykov, M.A., Wakabayashi, S.T., and, Saier, M.H. Jr, (2012) The amino acid-polyamine-organocation superfamily. J. Mol. Microbiol. Biotechnol. 22, 105-113.
50. Yang, H., Bogner, M., Stierhof, Y.D., and, Ludewig, U., (2010) H-independent glutamine transport in plant root tips. PLoS ONE, 5, e8917.
51. Yin, Y.G., Tominaga, T., Iijima, Y., Aoki, K., Shibata, D., Ashihara, H., Nishimura, S., Ezura, H., and, Matsukura, C., (2010) Metabolic alterations in organic acids and gamma-aminobutyric acid in developing tomato (Solanum lycopersicum L.) fruits. Plant Cell Physiol. 51, 1300-1314.