Biochemical characterization, mitochondrial localization, expression, and potential functions for an Arabidopsis γ-aminobutyrate transaminase that utilizes both pyruvate and glyoxylate

Journal of Experimental Botany

Volumn 60, Issue 6, 2009, Pages 1743-1757

  Clark, Shawn M ^a   Di Leo, Rosa ^a   Dhanoa, Preetinder K ^a   Van Cauwenberghe, Owen R ^a   Mullen, Robert T ^a   Shelp, Barry J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Enzyme kinetics; GABA transaminase; Gene expression; Glyoxylate; Photorespiration; Recombinant protein; Subcellular localization

Indexed keywords

AMINOTRANSFERASE; ARABIDOPSIS PROTEIN; GLYOXYLIC ACID DERIVATIVE; POP2 PROTEIN, ARABIDOPSIS; PYRUVIC ACID; RECOMBINANT PROTEIN;

ARABIDOPSIS; ARTICLE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; MITOCHONDRION; PROTEIN TRANSPORT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION; GLYOXYLATES; KINETICS; MITOCHONDRIA; PROTEIN TRANSPORT; PYRUVIC ACID; RECOMBINANT PROTEINS; TRANSAMINASES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ESCHERICHIA COLI;

EID: 65349113784     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erp044     Document Type: Article

References (80)

1. Akihiro T, Koike S, Tani R, et al. 2008. Biochemical mechanism on GABA accumulation during fruit development in tomato. Plant and Cell Physiology 49, 1378-1389.
2. Allan WL, Peiris C, Bown AW, Shelp BJ. 2003. Gamma-hyroxybutyrate accumulates in green tea and soybean sprouts in response to oxygen deficiency. Canadian Journal of Plant Science 83, 951-953.
3. Allan WL, Shelp BJ. 2006. Fluctuations of γ-aminobutyrate, γ-hydroxybutyrate and related amino acids in Arabidopsis leaves as a function of the light-dark cycle, leaf age and N stress. Canadian Journal of Botany 84, 1339-1346.
4. Allan WL, Simpson JP, Clark SM, Shelp BJ. 2008. γ-Hydroxybutyrate accumulation in Arabidopsis and tobacco plants is a general response to abiotic stress: putative regulation by redox balance and glyoxylate reductase isoforms. Journal of Experimental Botany 59, 2555-2564.
5. André B, Jauniaux J-C. 1990. Nucleotide sequence of the yeast UGA1 gene encoding GABA transaminase. Nucleic Acids Research 18, 3046.
6. Ansari IM, Lee R, Chen SG. 2005. A novel senescence-associated gene encoding γ-aminobutyric acid (GABA):pyruvate transaminase is unregulated during rice leaf senescence. Physiologia Plantarum 123, 1-8.
7. Banjoko A, Trelease RN. 1995. Development and application of an in vivo plant peroxisome import system. Plant Physiology 107, 1201-1208.
8. Barbosa JMF. 2002. Physiological, biochemical and molecular aspects of γ-aminobutyric acid (GABA): a stress-responsive non-protein amino acid. PhD thesis. Auburn: Auburn University.
9. Bari R, Kebeish R, Kalamajka R, Rademacher T, Peterhansel C. 2004. A glycolate dehydrogenase in the mitochondria of Arabidopsis thaliana. Journal of Experimental Botany 55, 623-630.
10. Bartsch K, von Johnn-Marteville A, Schulz A. 1990. Molecular analysis of two genes of the Escherichia coli gab cluster: nucleotide sequence of the glutamate:succinic semialdehyde transaminase (gabT) and characterization of the succinic semialdehyde dehydrogenase (gabD). Journal of Bacteriology 172, 7035-7042.
11. Baum G, Chen Y, Arazi T, Takatsuji H, Fromm H. 1993. A plant glutamate decarboxylase containing a calmodulin binding domain. Journal of Biological Chemistry 268, 19610-19617.
12. Bouché N, Lacombe B, Fromm H. 2003. GABA signaling: a conserved and ubiquitous mechanism. Trends in Cell Biology 13, 607-610.
13. Bouché N, Fromm H. 2004. GABA in plants: just a metabolite? Trends in Plant Science 9, 110-115.
14. Bown AW, Shelp BJ. 1989. The metabolism and physiological roles of 4-aminobutyric acid. Biochemistry (Life Science Advances) 8, 21-25.
15. Bown AW, Shelp BJ. 1997. The metabolism and functions of γ-aminobutyric acid. Plant Physiology 115, 1-5.
16. Bradford M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
17. Breitkreuz KE, Allan WA, Van Cauwenberghe OR, Jakobs C, Talibi D, André B, Shelp BJ. 2003. A novel γ-hyrdoxybutyrate dehydrogenase. Identification and expression of an Arabidopsis cDNA and potential role under oxygen deficiency. Journal of Biological Chemistry 278, 41552-41556.
18. Breitkreuz KE, Shelp BJ. 1995. Subcellular compartmentation of the 4-aminobutyrate shunt in protoplasts from developing soybean cotyledons. Plant Physiology 108, 99-103.
19. Busch KB, Fromm H. 1999. Plant succinic semialdehyde dehydrogenase. Cloning, purification, localization in mitochondria, and regulation by adenine nucleotides. Plant Physiology 121, 589-597.
20. Buzenet AM, Fages C, Bloch-Tardy M, Gonnard P. 1978. Purification and properties of 4-aminobutyrate 2-ketoglutarate aminotransferase from pig liver. Biochimica et Biophysica Acta 522, 400-411.
21. Campbell WJ, Ogren WL. 1990. Glyoxylate inhibition of ribulosebisphosphate carboxylase/oxygenase activation in intact, lysed, and reconstituted chloroplasts. Photosynthesis Research 23, 257-268.
22. 1-ATPase β subunit from Nicotiana plumbaginifolia CAT and GUS proteins into mitochondria of transgenic tobacco. Plant Molecular Biology 24, 631-641.
23. Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J. 1996. Engineered GFP as a vital reporter in plants. Current Biology 6, 325-330.
24. Crawford LA, Bown AW, Breitkreuz KE, Guinel FC. 1994. The synthesis of γ-aminobutyric acid in response to treatments reducing cytosolic pH. Plant Physiology 104, 865-871.
25. Dale GE, Schonfield H-J, Langen H, Stieger M. 1994. Increased solubility of trimethoprim-resistant type S1 DHFR from Staphylococcus aureus in Escherichia coli cells overproducing the chaperonins GroEL and GroES. Protein Engineering 7, 925-931.
26. De Biase D, Barre D, Bossa F, Pucci P, John RA. 1991. Chemistry of the inactivation of 4-aminobutyrate aminotransferase by the antiepileptic drug vigabatrin. Journal of Biological Chemistry 266, 20056-20061.
27. De Biase D, Barra D, Simmaco M, John RA, Bossa F. 1995. Primary structure and tissue distribution of human 4-aminobutyrate aminotransferase. European Journal of Biochemistry 227, 476-480.
28. Der Garabedian PA, Lotti AM, Vermeersch J. 1986. 4-Amino-butyrate:2-oxoglutarate aminotransferase from Candida: purification and properties. European Journal of Biochemistry 156, 589-596.
29. Fait A, Fromm H, Walter D, Galili G, Fernie AR. 2008. Highway or byway: the metabolic role of the GABA shunt in plants. Trends in Plant Science 13, 14-19.
30. Fait A, Yellin A, Fromm H. 2005. GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Letters 579, 415-420.
31. Fritze CE, Anderson TR. 2000. Epitope tagging: general method for tracking recombinant proteins. Methods in Enzymology 327, 3-16.
32. Glaser E, Sjö ling S, Tanudji M, Whelan J. 1998. Mitochondrial protein import in plants. Signals, sorting, targeting and regulation. Plant Molecular Biology 38, 311-338.
33. Hausler RE, Bailey KJ, Lea PJ, Leegood RC. 1996. Control of photosynthesis in barley mutants with reduced activities of glutamine synthetase and glutamate synthase. III. Aspects of glyoxylate metabolism and effects of glyoxylate on the activation state of ribulose-1,5-bisphosphate carboxylase-oxygenase. Planta 200, 388-396.
34. Hoover GJ, Van Cauwenberghe OR, Breitkreuz KE, Clark SM, Merrill AR, Shelp BJ. 2007. Characteristics of an Arabidopsis glyoxylate reductase: general biochemical properties and substrate specificity for the recombinant protein, and developmental expression and implications for glyoxylate and succinic semialdehyde metabolism in planta. Canadian Journal of Botany 85, 883-895.
35. Kinnersley AM, Turano FJ. 2000. Gamma aminobutyric acid (GABA) and plant responses to stress. Critical Reviews of Plant Science 19, 479-509.
36. Köhler RH, Zipfel WR, Webb WW, Hanson MR. 1997. The green fluorescent protein as a marker to visualize plant mitochondria in vivo. The Plant Journal 11, 613-621.
37. Kozaki A, Takebo G. 1996. Photorespiration protects C3 plants from photooxidation. Nature 384, 557-560.
38. Kumar S, Punekar NS. 1997. The metabolism of 4-aminobutyrate (GABA) in fungi. Mycological Research 4, 403-409.
39. Lee MS, Mullen RT, Trelease RN. 1997. Oilseed isocitrate lyases lacking their essential type 1 peroxisomal targeting signal are piggybacked to glyoxysomes. The Plant Cell 9, 185-197.
40. Liepman AH, Olsen LJ. 2001. Peroxisomal alanine:glyoxylate aminotransferase (AGT1) is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. The Plant Journal 25, 487-498.
41. Liepman AH, Olsen LJ. 2003. Alanine aminotransferase homologs catalyze the glutamate:glyoxylate aminotransferase reaction in peroxisomes of Arabidopsis. Plant Physiology 131, 215-237.
42. Lindahl R. 1992. Aldehyde dehydrogenases and their roles in carcinogenesis. Critical Reviews in Biochemistry and Molecular Biology 27, 283-335.
43. Ling V, Snedden WA, Shelp BJ, Assman SM. 1994. Analysis of a soluble calmodulin binding protein from fava bean roots: identification of glutamate decarboxylase as a calmodulin activated enzyme. The Plant Cell 6, 1135-1143.
44. Liu W, Peterson PE, Carter RJ, Zhou X, Langston JA, Fisher AJ, Toney MD. 2004. Crystal structure of unbound and aminooxyacetate-bound Escherichia coli γ-aminobutyrate aminotransferase. Biochemistry 34, 10896-10905.
45. Ludewig F, Hü ser A, Fromm H, Beauclair L, Bouché N. 2008. Mutants of GABA transaminase (POP2) suppress the severe pheno-type of succinic semialdehyde dehydrogenase (ssadh) mutants in Arabidopsis. PLoS ONE 3, e3383. doi:10.1371/journal.pone.0003383.
46. Luethy MH, David NR, Elthon TE, Miernyk JA, Randall DD. 1995. Characterization of a monoclonal antibody directed against the E1α subunit of plant mitochondrial pyruvate dehydrogenase. Journal of Plant Physiology 145, 443-449.
47. Luethy MH, Gemel J, Johnston ML, Mooney BP, Miernyk JA, Randall DD. 2001. Developmental expression of the mitochondrial pyruvate dehydrogenase complex in pea (Pisum sativum) seedlings. Physiologia Plantarum 112, 559-566.
48. Maitre M, Ciesielski L, Cash C, Mandel P. 1978. Comparison of the structural characteristics of the 4-aminobutyrate:2-oxoglutarate transaminase from rat and humna brain, and of their affinites for certain inhibitors. Biochimica et Biophysica Acta 522, 385-399.
49. Miao YS, Jiang L. 2007. Transient expression of fluorescent fusion proteins in protoplasts of suspension cultured cells. Nature Protocols 2, 2348-2353.
50. Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylides C, Haring MA, Schurrink RC. 2008. The Arabidopsis her1 mutant implicates GABA in E-2hexenal responsivness. The Plant Journal 52, 197-213.
51. Mitsuda M, Iwasaki M. 2006. Improvement in the expression of CYP2B6 by co-expression with molecular chaperones GroES/EL in Escherichia coli. Protein Expression and Purification 46, 401-405.
52. Miyashita Y, Good AG. 2008. Contribution of the GABA shunt in hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant and Cell Physiology 49, 92-102.
53. Mullineaux PM, Rausch T. 2005. Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynthesis Research 86, 459-474.
54. Murphy MA, Phillipson BA, Baker A, Mullen RT. 2003. Characterization of the targeting signal of the Arabidopsis 22-kD integral peroxisomal membrane protein. Plant Physiology 133, 813-828.
55. Nakai K, Kanehisa M. 1992. A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14, 897-911.
56. Nicot N, Hausman JF, Hoffmann L, le Evers D. 2005. Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. Journal of Experimental Botany 56, 2907-2914.
57. Niessen M, Thiruveedhi K, Rosenkranz R, Kebeish R, Hirsch HJ, Kreuzaler F, Peterhansel C. 2007. Mitochondrial glycolate oxidation contributes to photorespiration in higher plants. Journal of Experimental Botany 58, 2709-2715.
58. Palanivelu R, Brass L, Edlund AF, Preuss D. 2003. Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114, 47-59.
59. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
60. Satya Narayan V, Nair PM. 1990. Metabolism, enzymology and possible roles of 4-aminobutyrate in higher plants. Phytochemistry 29, 367-375.
61. Sharkey TD. 1988. Estimating the rate of photorespiration in leaves. Physiologia Plantarum 73, 147-152.
62. Shelp BJ, Bown AW, Faure D. 2006. Extracellular gamma-aminobutyrate mediates communication between plants and other organisms. Plant Physiology 142, 1350-1352.
63. Shelp BJ, Bown AW, McLean MD. 1999. Metabolism and functions of gamma-aminobutyric acid. Trends in Plant Science 4, 446-452.
64. Shelp BJ, Penner R, Zhu Z. 1992. Broccoli (Brassica oleracea var. italica) cultivar response to boron deficiency. Canadian Journal of Plant Science 72, 883-888.
65. Shelp BJ, Walton CS, Snedden WA, Tuin LG, Oresnik IJ, Layzell DB. 1995. GABA shunt in developing soybean seeds is associated with hypoxia. Physiologia Plantarum 94, 219-228.
66. Simpson JP, Di Leo R, Dhanoa PK, Allan WL, Makhmoudova A, Clark SM, Hoover GJ, Mullen RT, Shelp BJ. 2008. Identification and characterization of a plastid-localized Arabidopsis glyoxylate reductase isoform: comparison with a cytosolic isoform and implications for cellular redox homeostasis and aldehyde detoxification. Journal of Experimental Botany 59, 2545-2554.
67. Sjö ling S, Glaser E. 1998. Mitochondrial targeting peptides in plants. Trends in Plant Science 3, 136-140.
68. Smith IK. 1985. Aminotransferases utilizing glyoxylate. In: Christen P, Metzler DE, eds. Transaminases. New York: Wiley, 390-396.
69. Snedden WA, Arazi T, Fromm H, Shelp BJ. 1995. Calcium/calmodulin activation of soybean glutamate decarboxylase. Plant Physiology 108, 543-549.
70. Snedden WA, Koutsia N, Baum G, Fromm H. 1996. Activation of petunia glutamate decarboxylase by calcium/calmodulin or a monoclonal antibody which recognizes the calmodulin binding domain. Journal of Biological Chemistry 271, 4148-4153.
71. Stabenau H, Winkler U. 2005. Glycolate metabolism in green algae. Physiologia Plantarum 123, 235-245.
72. Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH. 2003. The impact of oxidative stress on Arabidopsis mitochondria. The Plant Journal 32, 891-904.
73. Tibbetts AS, Applings DR. 2000. Characterization of two 5-amino-imidazole-4-carboxaminde ribonucleotide transformylase/inosine monophosphate cyclohydrolase isozymes from Saccharomyces cerevisiae. Journal of Biological Chemistry 275, 20920-20927.
74. Trelease RN, Xie W, Lee MS, Mullen RT. 1996. Rat liver catalase is sorted to peroxisomes by its C-terminal tripeptide Ala-Asn-Leu, not by the internal Ser-Lys-Leu motif. European Journal of Cell Biology 71, 248-258.
75. Van Bemmelen FJ, Schouten MJ, Fekkes D, Bruinvels J. 1985. Succinic semialdehyde as a substrate for the formation of c-amino-butyric acid. Journal of Neurochemistry 45, 1471-1474.
76. Van Cauwenberghe OR, Makhmoudova A, McLean MD, Clark S, Shelp BJ. 2002. Plant pyruvate-dependent gamma-aminobutyrate transaminase: identification of an Arabidopsis cDNA and its expression in Escherichia coli. Canadian Journal of Botany 80, 933-941.
77. Van Cauwenberghe OR, Shelp BJ. 1999. Biochemical characterization of partially purified GABA:pyruvate transaminase from Nicotiana tabacum. Phytochemistry 52, 575-581.
78. Wingler A, Lea PJ, Quick WP, Leegood RC. 2000. Photorespiration: metabolic pathways and their role in stress protection. Philosophical Transactions of the Royal Society B: Biological Sciences 355, 1517-1529.
79. Yonaha K, Suziki K, Minei H, Toyama S. 1983. Distribution of ω-amino-acid:pyruvate transaminase and aminobutyrate:α-ketoglutarate transaminase in microorganisms. Agricultural and Biological Chemistry 47, 2257-2265.
80. Yu G, Liang J, He Z, Sun M. 2006. Quantum dot-mediated detection of γ-aminobutyric acid binding sites on the surface of living protoplasts in tobacco. Chemistry and Biology 13, 723-731.