Identification of a mitochondrial transporter for basic amino acids in Arabidopsis thaliana by functional reconstitution into liposomes and complementation in yeast

Plant Journal

Volumn 33, Issue 6, 2003, Pages 1027-1035

  Hoyos, Mary Elizabeth ^a   Palmieri, Luigi ^b,c   Wertin, Timothy ^a   Arrigoni, Roberto ^b,c   Polacco, Joseph C ^a   Palmieri, Ferdinando ^b  

^a University of Missouri   (United States)

^b UNIVERSITY OF BARI   (Italy)

^c CNR   (Italy)

Author keywords

Arginase; Arginine; Basic amino acids; Mitochondria; Nitrogen mobilization; Transport

Indexed keywords

PHOSPHOLIPIDS; SEED; YEAST;

SEEDLING COTYLEDONS;

AMINO ACIDS;

AMINO ACID SEQUENCE; AMINO ACID TRANSPORT SYSTEMS; AMINO ACIDS, BASIC; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGININE; BIOLOGICAL TRANSPORT, ACTIVE; GENE EXPRESSION; GENES, PLANT; GENETIC COMPLEMENTATION TEST; KINETICS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PROTEOLIPIDS; SACCHAROMYCES;

AMINO ACIDS; LIPIDS; MITOCHONDRIA; SEEDLINGS; YEASTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; ESCHERICHIA COLI; EUKARYOTA; GLYCINE MAX; MAMMALIA;

EID: 0037356772     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01685.x     Document Type: Article

References (44)

1. Baker, A. and Leaver, C.J. (1985) Isolation and sequence analysis of a cDNA encoding the ATP/ADP translocator of Zea mays L. Nucl. Acids Res. 13, 5857-5867.
2. Borecky, J., Maia, I.G., Costa, A.D., Jezek, P., Chaimovich, H., de Andrade, P.B., Vercesi, A.E. and Arruda, P. (2001) Functional reconstitution of Arabidopsis thaliana plant uncoupling mitochondrial protein (AtPUMP1) expressed in Escherichia coli. FEBS Lett. 505, 240-244.
3. Camacho, J.A., Obie, C., Biery, B. et al. (1999) Hyperornithinaemiahyperammonaemia-homocitrullinuria syndrome is caused by mutations in a gene encoding a mitochondrial ornithine transporter. Nat. Genet. 22, 151-158.
4. Chou, K.H. and Splittstoesser, W.E. (1972) Changes in amino acid content and the metabolism of γ-aminobutyrate in Cucurbita moschata seedlings. Physiol. Plant. 26, 110-114.
5. Crabeel, M., Soetens, O., De Rijcke, M., Pratiwi, R. and Pankiewicz, R. (1996) The ARG11 gene of Saccharomyces cerevisiae encodes a mitochondrial integral membrane protein required for arginine biosynthesis. J. Biol. Chem. 271, 25011-25018.
6. Dolce, V., Fiermonte, G., Runswick, M.J., Palmieri, F. and Walker, J.E. (2001) The human mitochondrial deoxynucleotide carrier and its role in toxicity of nucleoside antivirals. Proc. Natl. Acad. Sci. USA, 98, 2284-2288.
7. Downum, K.R., Rosenthal, G.A. and Cohen, W.S. (1983) L-Arginine and L-canavanine metabolism in jack bean. Canavalia ensiformis (L.) DC. & soybean, Glycine max (L.) Merr. Plant Physiol. 73, 965-968.
8. Fiermonte, G., Dolce, V. and Palmieri, F. (1998b) Expression in Escherichia coli, functional characterization and tissue distribution of isoforms A and B of the phosphate carrier from bovine mitochondria. J. Biol. Chem. 273, 22782-22787.
9. Fiermonte, G., Palmieri, L., Dolce, V., Lasorsa, F.M., Palmieri, F., Runswick, M.J. and Walker, J.E. (1998a) The sequence, bacterial expression and functional reconstitution of the rat mitochondrial dicarboxylatetransporter cloned via distant homologs in yeast and Caenorhabditis elegans. J. Biol. Chem. 273, 24754-24759.
10. Fiermonte, G., Palmieri, L., Todisco, S., Agrimi, G., Palmieri, F. and Walker, J.E. (2002) Identification of the mitochondrial glutamate transporter: bacterial expression, reconstitution, function characterization and tissue distribution of two isoforms. J. Biol. Chem. 277, 19289-19294.
11. Fiermonte, G., Walker, J.E. and Palmieri, F. (1993) Abundant bacterial expression and reconstitution of an intrinsic membrane transport protein from bovine mitochondria. Biochem. J. 294, 293-299.
12. Gietz, D., St. Jean, A., Woods, R.A. and Schiestl, R.H. (1992) Improved method for high efficiency transformation of intact yeast cells. Nucl. Acids Res. 22, 1502-1503.
13. Goldraij, A. and Polacco, J.C. (1999) Arginase is inoperative in developing soybean seeds. Plant Physiol. 119, 297-304.
14. Goldraij, A. and Polacco, J.C. (2000) Arginine degradation by arginase in mitochondria of soybean seedling cotyledons. Planta, 210, 652-658.
15. Hofman, K. and Stoffel, W. (1993) TMbase - a database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler, 374, 166.
16. Indiveri, C., Tonazzi, A. and Palmieri, F. (1992) Identification and purification of the ornithine/citrulline carrier from rat liver mitochondria. Eur. J. Biochem. 207, 449-454.
17. Ito, H., Fukada, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
18. Kang, J.H. and Cho, Y.D. (1990) Purification and properties of arginase from soybean (Glycine max) axes. Plant Physiol. 93, 1230-1234.
19. Kaplan, R.S. (1996) High-level bacterial expression of mitochondrial transport proteins. J. Bioenerg. Biomembr. 28, z41-47.
20. Kiiskinen, M., Korhonen, M. and Kangasjarvi, J. (1997) Isolation and characterization of cDNA for a plant mitochondrial phosphate translocator (Mpt1): ozone stress induces Mpt1 mRNA accumulation in birch (Betula pendula Both). Plant Mol. Biol. 35, 271-279.
21. King, J.E. and Gifford, D.J. (1997) Amino acid utilization in seeds of loblolly pine during germination and early seedling growth. Plant Physiol. 113, 1125-1135.
22. Krämer, R. and Palmieri, F. (1989) Molecular aspects of isolated and reconstituted carrier proteins from animal mitochondria. Biochim. Biophys. Acta, 974, 1-23.
23. Laloi, M. (1999) Plant mitochondrial carriers: an overview. Cell. Mol. Life Sci. 56, 918-944.
24. Laloi, M., Klein, M., Riesmeier, J.W., Muller-Rober, B., Fleury, C., Bouillaud, F. and Ricquier, D. (1997) A plant cold-induced uncoupling protein. Nature, 389, 135-136.
25. Marobbio, C.M.T., Vozza, A., Harding, M., Bisaccia, F., Palmieri, F. and Walker, J.E. (2002) Identification and reconstitution of the yeast mitochondrial transporter for thiamine pyrophosphate. EMBO J. 21, 5653-5661.
26. Micallef, B.J. and Shelp, B.J. (1989) Arginine metabolism in developing soybean cotyledons. Part I. Relationship to nitrogen nutrition. Plant Physiol. 90, 624-630.
27. Minet, M., Dufour, M.E. and Lacroute, F. (1992) Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 2, 417-422.
28. Murfett, J., Atherton, T.L., Mou, B., Gasser, C.S. and McClure, B.A. (1994) S-Rnase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature, 367, 563-566.
29. Palmieri, F. (1994) Mitochondrial carrier proteins. FEBS Lett. 346, 48-54.
30. Palmieri, L, De Marco, V., Iacobazzi, V., Palmieri, F., Runswick, M. and Walker, J. (1997) Identification of the yeast ARG- 11 gene as a mitochondrial ornithine carrier involved in arginine biosynthesis. FEBS Lett. 410, 447-451.
31. Palmieri, F., Indiveri, C., Bisaccia, F. and Iacobazzi, V. (1995) Mitochondrial metabolite carrier proteins: purification, reconstitution, and transport studies. Meth. Enzymol. 260, 349-369.
32. 2+-stimulated aspartate/glutamate transporters in mitochondria. EMBO J. 20, 5060-5069.
33. Picault, N., Palmieri, L., Pisano, I., Hodges, M. and Palmieri, F. (2002) Identification of a novel transporter for dicarboxylates and tricarboxylates in plant mitochondria: bacterial expression, reconstitution, functional characterization and tissue distribution. J. Biol. Chem. 277, 24204-24211.
34. Polacco, J.C. and Holland, M.A. (1993) Roles of urease in plant cells. In International Rev. Cytology, Vol. 145 (Jeon, K.W. and Friedlander, M., eds). San Diego: Academic Press, pp. 65-103.
35. de Ruiter, H. and Kollöffel, C. (1983) Arginine catabolism in the cotyledons of developing and germinating pea seeds. Plant Physiol. 73, 525-528.
36. Shargool, P.D., Jain, J.C. and McKay, G. (1988) Ornithine biosynthesis, and arginine biosynthesis and degradation in plant cells. Phytochemistry, 27, 1571-1574.
37. Stebbins, N.E., Holland, M.A., Cianzio, S.R. and Polacco, J.C. (1991) Genetic tests of the roles of the embryonic ureases of soybean. Plant Physiol. 97, 1004-1010.
38. Stebbins, N.E. and Polacco, J.C. (1995) Urease is not essential for ureide degradation in soybean. Plant Physiol. 109, 169-175.
39. Takabatake, R., Hata, S., Taniguchi, M., Kouchi, H., Sugiyama, T. and Izui, K. (1999) Isolation and characterization of cDNAs encoding mitochondrial phosphate transporters in soybean, maize, rice, and Arabidopsis. Plant Mol. Biol. 40, 479-486.
40. Thompson, J.F. (1980) Arg synthesis, proline synthesis and related processes. In The Biochemistry of Plants, Vol. 5 (Miflin, B.J. ed.). New York: Academic Press, pp. 375-402.
41. Todd, C.D., Cooke, J.E.K., Mullen, R.T. and Gifford, D.J. (2001) Regulation of loblolly pine (Pinus taeda L.) arginase in developing seedling tissue during germination and post-germinative growth. Plant Mol. Biol. 45, 555-565.
42. VanEtten, C.H., Kwolek, W.F., Peters, I.E. and Barclay, A.S. (1967) Plant seeds as protein sources for food or feed. Evaluation based on amino acid composition of 379 species. J. Agric. Food Chem. 15, 1077-1085.
43. Winkler, R.G., Blevins, D.G., Polacco, J.C. and Randall, D.D. (1987) Ureide catabolism of soybeans. Part II. Path of catabolism in intact leaf tissue. Plant Physiol. 83, 585-591.
44. Zonia, L.E., Stebbins, N.E. and Polacco, J.C. (1995) Essential role of urease in germination of nitrogen-limited Arabidopsis thaliana seeds. Plant Physiol. 107, 1097-1103.