An Arabidopsis GluTR binding protein mediates spatial separation of 5-Aminolevulinic acid synthesis in chloroplasts

Plant Cell

Volumn 23, Issue 12, 2011, Pages 4476-4491

  Czarnecki, Olaf ^a   Hedtke, Boris ^a   Melzer, Michael ^b   Rothbart, Maxi ^a   Richter, Andreas ^a   Schröter, Yvonne ^c   Pfannschmidt, Thomas ^c   Grimm, Bernhard ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84856441772     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.086421     Document Type: Article

References (80)

1. Andersson, J., Wentworth, M., Walters, R.G., Howard, C.A., Ruban, A. V., Horton, P., and Jansson, S. (2003). Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness. Plant J. 35: 350-361.
2. Annweiler, A., Hipskind, R.A., and Wirth, T. (1991). A strategy for efficient in vitro translation of cDNAs using the rabbit beta-globin leader sequence. Nucleic Acids Res. 19: 3750.
3. Archakov, A.I., Govorun, V.M., Dubanov, A.V., Ivanov, Y.D., Veselovsky, A.V., Lewi, P., and Janssen, P. (2003). Protein-protein interactions as a target for drugs in proteomics. Proteomics 3: 380-391.
4. Bartel, P.L., Chien, C.T., Sternglanz, R., and Fields, S. (1993). Using the two-hybrid system to detect protein protein interactions. In Cellular Interactions in Development: A Practical Approach., D.A. Hartley, ed (Oxford, UK: Oxford University Press), pp. 153-179.
5. Beale, S.I. (1999). Enzymes of chlorophyll biosynthesis. Photosynth. Res. 60: 43-73.
6. Beale, S.I. (2006). Biosynthesis of 5-aminolevulinic acid. In Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications, B. Grimm, R.J. Porra, W. Rudiger, and H. Scheer, eds (Dordrecht, The Netherlands: Springer), pp. 147-158.
7. Becker, D., Kemper, E., Schell, J., and Masterson, R. (1992). New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol. Biol. 20: 1195-1197.
8. Bendahmane, A., Querci, M., Kanyuka, K., and Baulcombe, D.C. (2000). Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: application to the Rx2 locus in potato. Plant J. 21: 73-81.
9. Birnboim, H.C., and Doly, J. (1979). A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7: 1513-1523.
10. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal. Biochem. 72: 248-254.
11. Brock, I.W., Hazell, L., Michl, D., Nielsen, V.S., Møller, B.L., Herrmann, R.G., Klösgen, R.B., and Robinson, C. (1993). Precursors of one integral and five lumenal thylakoid proteins are imported by isolated pea and barley thylakoids: Optimisation of in vitro assays. Plant Mol. Biol. 23: 717-725.
12. Bürkle, L., Meyer, S., Dortay, H., Lehrach, H., and Heyl, A. (2005). In vitro recombination cloning of entire cDNA libraries in Arabidopsis thaliana and its application to the yeast two-hybrid system. Funct. Integr. Genomics 5: 175-183.
13. Chen, S., Hofius, D., Sonnewald, U., and Börnke, F. (2003). Temporal and spatial control of gene silencing in transgenic plants by inducible expression of double-stranded RNA. Plant J. 36: 731-740.
14. Church, G.M., and Gilbert, W. (1984). Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991-1995.
15. Clausmeyer, S., Klösgen, R.B., and Herrmann, R.G. (1993). Protein import into chloroplasts. The hydrophilic lumenal proteins exhibit unexpected import and sorting specificities in spite of structurally conserved transit peptides. J. Biol. Chem. 268: 13869-13876.
16. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
17. Cornah, J.E., Terry, M.J., and Smith, A.G. (2003). Green or red: What stops the traffic in the tetrapyrrole pathway? Trends Plant Sci. 8: 224-230.
18. Czarnecki, O. (2010). Die Synthese der 5-Aminolävulinsäure in Pflanzen: Charakterisierung eines neuen GluTR-bindenden Proteins und dessen Rolle bei der Mikrokompartimentierung der Tetrapyrrolbiosynthese. (Berlin: Mensch & Buch Verlag).
19. Dawson, R.C.M., Elliott, D.C., Elliot, W.H., and Jones, K.M. (1986). Data for Biochemical Research. (Oxford, UK: Oxford University Press).
20. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2: 953-971.
21. Friso, G., Giacomelli, L., Ytterberg, A.J., Peltier, J.B., Rudella, A., Sun, Q., and Wijk, K.J. (2004). In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: New proteins, new functions, and a plastid proteome database. Plant Cell 16: 478-499.
22. Goehler, H., et al. (2004). A protein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington's disease. Mol. Cell 15: 853-865. Erratum. Mol. Cell 22: 287.
23. Goslings, D., Meskauskiene, R., Kim, C., Lee, K.P., Nater, M., and Apel, K. (2004). Concurrent interactions of heme and FLU with Glu tRNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis plants. Plant J. 40: 957-967.
24. Gough, S.P., and Kannangara, C.G. (1977). Synthesis of delta-aminolevulinate by a chloroplast stroma preparation from greening barley leaves. Carlsberg Res. Commun. 42: 459-464.
25. Grimm, B. (2010). Control of the metabolic flow in tetrapyrrole.biosynthesis: Regulation of expression and activity of enzymes in the Mg branch of tetrapyrrole biosynthesis. In The Chloroplast, Basics and Applications., C.A. Rebeiz, C. Benning, H.J. Bohnert, H. Daniell, J.K. Hoober, H.K. Lichtenthaler, A.R. Portis, and B.C. Tripathy, eds (Dordrecht, The Netherlands: Springer), pp. 39-53.
26. Hackenberg, D. (2010). Untersuchung der Funktion von Mitgliedern der NF-Y-Genfamilie während der Antwort auf abiotischen Stress in Arabidopsis thaliana. (Berlin: Mensch & Buch Verlag).
27. Han, L., and Colicelli, J. (1995). A human protein selected for interference with Ras function interacts directly with Ras and competes with Raf1. Mol. Cell. Biol. 15: 1318-1323.
28. Harel, E., and Ne'eman, E. (1983). Alternative routes for the synthesis of 5-aminolevulinic acid in maize leaves. II. Formation from glutamate. Plant Physiol. 72: 1062-1067.
29. Harlow, E., and Lane, D. (1988). Antibodies: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
30. Hellens, R., Mullineaux, P., and Klee, H. (2000). Technical Focus: A guide to Agrobacterium binary Ti vectors. Trends Plant Sci. 5: 446-451.
31. Hilson, P., et al. (2004). Versatile gene-specific sequence tags for Arabidopsis functional genomics: Transcript profiling and reverse genetics applications. Genome Res. 14: 2176-2189.
32. Huang, L., and Castelfranco, P.A. (1990). Regulation of 5-aminolevulinic acid (ALA) synthesis in developing chloroplasts: III. Evidence for functional heterogeneity of the ALA pool. Plant Physiol. 92: 172-178.
33. Joshi, C.P., Zhou, H., Huang, X., and Chiang, V.L. (1997). Context sequences of translation initiation codon in plants. Plant Mol. Biol. 35: 993-1001.
34. Joyard, J., Ferro, M., Masselon, C., Seigneurin-Berny, D., Salvi, D., Garin, J., and Rolland, N. (2009). Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol. Plant 2: 1154-1180.
35. Jung, H.S., Okegawa, Y., Shih, P.M., Kellogg, E., Abdel-Ghany, S.E., Pilon, M., Sjölander, K., Shikanai, T., and Niyogi, K.K. (2010). Arabidopsis thaliana PGR7 encodes a conserved chloroplast protein that is necessary for efficient photosynthetic electron transport. PLoS ONE 5: e11688.
36. Kannangara, C.G., Gough, S.P., Hansen, B., Rasmussen, J.N., and Simpson, D.J. (1977). Homogenizer with replaceable razor blades for bulk isolation of active barley plastids. Carlsberg Res. Commun. 42: 431-439.
37. Kitamura, M., Kojima, S., Ogasawara, K., Nakaya, T., Sagara, T., Niki, K., Miura, K., Akutsu, H., and Kumagai, I. (1994). Novel FMNbinding protein from Desulfovibrio vulgaris (Miyazaki F). Cloning and expression of its gene in Escherichia coli. J. Biol. Chem. 269: 5566-5573.
38. Koski, V.M., and Smith, J.H. (1948). The isolation and spectral absorption properties of protochlorophyll from etiolated barley seedlings. J. Am. Chem. Soc. 70: 3558-3562.
39. Krieger-Liszkay, A., Fufezan, C., and Trebst, A. (2008). Singlet oxygen production in photosystem II and related protection mechanism. Photosynth. Res. 98: 551-564.
40. Kunst, L. (1998). Preparation of physiologically active chloroplasts from Arabidopsis. In Arabidopsis Protocols. Methods in Molecular Biology, J. Martinez-Zapater and J. Salinas, eds (Totowa, NJ: Humana Press), pp. 43-48.
41. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
42. Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic membranes. Methods Enzymol. 148: 350-382.
43. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
44. Lüer, C., Schauer, S., Möbius, K., Schulze, J., Schubert, W.D., Heinz, D.W., Jahn, D., and Moser, J. (2005). Complex formation between glutamyl-tRNA reductase and glutamate-1-semialdehyde 2,1-aminomutase in Escherichia coli during the initial reactions of porphyrin biosynthesis. J. Biol. Chem. 280: 18568-18572.
45. Lunn, J.E. (2007). Compartmentation in plant metabolism. J. Exp. Bot. 58: 35-47.
46. MacDonald, P.N. (2001). Two-Hybrid Systems. Methods and Protocols. (Totowa, NJ: Humana Press).
47. Masuda, T., and Fujita, Y. (2008). Regulation and evolution of chlorophyll metabolism. Photochem. Photobiol. Sci. 7: 1131-1149.
48. Masuda, T., and Takahashi, S. (2006). Chemiluminescent-based method for heme determination by reconstitution with horseradish peroxidase apo-enzyme. Anal. Biochem. 355: 307-309.
49. Matsumoto, F., Obayashi, T., Sasaki-Sekimoto, Y., Ohta, H., Takamiya, K., and Masuda, T. (2004). Gene expression profiling of the tetrapyrrole metabolic pathway in Arabidopsis with a mini-array system. Plant Physiol. 135: 2379-2391.
50. Merchant, S.S., et al. (2007). The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250.
51. Meskauskiene, R., Nater, M., Goslings, D., Kessler, F., op den Camp, R., and Apel, K. (2001). FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 98: 12826-12831.
52. Mochizuki, N., Tanaka, R., Grimm, B., Masuda, T., Moulin, M., Smith, A.G., Tanaka, A., and Terry, M.J. (2010). The cell biology of tetrapyrroles: A life and death struggle. Trends Plant Sci. 15: 488-498.
53. Moser, J., Schubert, W.D., Beier, V., Bringemeier, I., Jahn, D., and Heinz, D.W. (2001). V-shaped structure of glutamyl-tRNA reductase, the first enzyme of tRNA-dependent tetrapyrrole biosynthesis. EMBO J. 20: 6583-6590.
54. Moulin, M., McCormac, A.C., Terry, M.J., and Smith, A.G. (2008). Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc. Natl. Acad. Sci. USA 105: 15178-15183.
55. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15: 473-497.
56. Murray, D.L., and Kohorn, B.D. (1991). Chloroplasts of Arabidopsis thaliana homozygous for the ch-1 locus lack chlorophyll b, lack stable LHCPII and have stacked thylakoids. Plant Mol. Biol. 16: 71-79.
57. Nogaj, L.A., and Beale, S.I. (2005). Physical and kinetic interactions between glutamyl-tRNA reductase and glutamate-1-semialdehyde aminotransferase of Chlamydomonas reinhardtii. J. Biol. Chem. 280: 24301-24307.
58. Papenbrock, J., Mock, H.P., Kruse, E., and Grimm, B. (1999). Expression studies in tetrapyrrole biosynthesis: Inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods. Planta 208: 264-273.
59. Papenbrock, J., Mock, H.P., Tanaka, R., Kruse, E., and Grimm, B. (2000b). Role of magnesium chelatase activity in the early steps of the tetrapyrrole biosynthetic pathway. Plant Physiol. 122: 1161-1169.
60. Papenbrock, J., Pfündel, E., Mock, H.P., and Grimm, B. (2000a). Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants. Plant J. 22: 155-164.
61. Peltier, J.B., Cai, Y., Sun, Q., Zabrouskov, V., Giacomelli, L., Rudella, A., Ytterberg, A.J., Rutschow, H., and van Wijk, K.J. (2006). The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol. Cell. Proteomics 5: 114-133.
62. Pontoppidan, B., and Kannangara, C.G. (1994). Purification and partial characterisation of barley glutamyl-tRNA(Glu) reductase, the enzyme that directs glutamate to chlorophyll biosynthesis. Eur. J. Biochem. 225: 529-537.
63. Richter, A., Peter, E., Pörs, Y., Lorenzen, S., Grimm, B., and Czarnecki, O. (2010). Rapid dark repression of 5-aminolevulinic acid synthesis in green barley leaves. Plant Cell Physiol. 51: 670-681.
64. Rolland, N., Ferro, M., Seigneurin-Berny, D., Garin, J., Douce, R., and Joyard, J. (2003). Proteomics of chloroplast envelope membranes. Photosynth. Res. 78: 205-230.
65. Rossel, J.B., Wilson, I.W., and Pogson, B.J. (2002). Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 130: 1109-1120.
66. Sambrook, J., and Russell, D.W. (2001). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory).
67. Schiffmann, E., and Shemin, D. (1957). Further studies on the utilization of aminolevulinic acid for porphyrin synthesis. J. Biol. Chem. 225: 623-628.
68. Schmittgen, T.D., and Livak, K.J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3: 1101-1108.
69. Srivastava, A., Lake, V., Nogaj, L.A., Mayer, S.M., Willows, R.D., and Beale, S.I. (2005). The Chlamydomonas reinhardtii gtr gene encoding the tetrapyrrole biosynthetic enzyme glutamyl-trna reductase: structure of the gene and properties of the expressed enzyme. Plant Mol. Biol. 58: 643-658.
70. Takahashi, S., and Masuda, T. (2009). High throughput heme assay by detection of chemiluminescence of reconstituted horseradish peroxidase. Comb. Chem. High Throughput Screen. 12: 532-535.
71. Tanaka, R., and Tanaka, A. (2007). Tetrapyrrole biosynthesis in higher plants. Annu. Rev. Plant Biol. 58: 321-346.
72. Tanaka, R., Yoshida, K., Nakayashiki, T., Masuda, T., Tsuji, H., Inokuchi, H., and Tanaka, A. (1996). Differential expression of two hemA mRNAs encoding glutamyl-tRNA reductase proteins in greening cucumber seedlings. Plant Physiol. 110: 1223-1230.
73. Tognetti, V.B., Palatnik, J.F., Fillat, M.F., Melzer, M., Hajirezaei, M. R., Valle, E.M., and Carrillo, N. (2006). Functional replacement of ferredoxin by a cyanobacterial flavodoxin in tobacco confers broadrange stress tolerance. Plant Cell 18: 2035-2050.
74. Ujwal, M.L., McCormac, A.C., Goulding, A., Kumar, A.M., Söll, D., and Terry, M.J. (2002). Divergent regulation of the HEMA gene family encoding glutamyl-tRNA reductase in Arabidopsis thaliana: Expression of HEMA2 is regulated by sugars, but is independent of light and plastid signalling. Plant Mol. Biol. 50: 83-91.
75. Vothknecht, U.C., Kannangara, C.G., and von Wettstein, D. (1998). Barley glutamyl tRNAGlu reductase: mutations affecting haem inhibition and enzyme activity. Phytochemistry 47: 513-519.
76. Walter, M., Chaban, C., Schütze, K., Batistic, O., Weckermann, K., Näke, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., Harter, K., and Kudla, J. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40: 428-438.
77. Wanker, E.E., Rovira, C., Scherzinger, E., Hasenbank, R., Wälter, S., Tait, D., Colicelli, J., and Lehrach, H. (1997). HIP-I: A huntingtin interacting protein isolated by the yeast two-hybrid system. Hum. Mol. Genet. 6: 487-495.
78. Weigel, D., and Glazebrook, J. (2002). Arabidopsis. A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
79. Woods, R.A., and Gietz, R.D. (2001). High-efficiency transformation of plasmid DNA into yeast. Methods Mol. Biol. 177: 85-97.
80. Ytterberg, A.J., Peltier, J.B., and van Wijk, K.J. (2006). Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol. 140: 984-997.