Orchestration of thiamin biosynthesis and central metabolism by combined action of the thiamin pyrophosphate riboswitch and the circadian clock in Arabidopsis

Plant Cell

Volumn 25, Issue 1, 2013, Pages 288-307

  Bocobza, Samuel E ^a   Malitsky, Sergey ^a   Araújo, Wagner L ^b,d   Nunes Nesi, Adriano ^b   Meir, Sagit ^a   Shapira, Michal ^c   Fernie, Alisdair R ^b   Aharoni, Asaph ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^d FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84874548158     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.106385     Document Type: Article

References (73)

1. Ajjawi, I., Rodriguez Milla, M.A., Cushman, J., and Shintani, D.K. (2007b). Thiamin pyrophosphokinase is required for thiamin cofactor activation in Arabidopsis. Plant Mol. Biol. 65: 151-162.
2. Ajjawi, I., Tsegaye, Y., and Shintani, D. (2007a). Determination of the genetic, molecular, and biochemical basis of the Arabidopsis thaliana thiamin auxotroph th1. Arch. Biochem. Biophys. 459: 107-114.
3. Alabadí, D., Oyama, T., Yanovsky, M.J., Harmon, F.G., Más, P., and Kay, S.A. (2001). Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293: 880-883.
4. Araújo, W.L., Nunes-Nesi, A., Trenkamp, S., Bunik, V.I., and Fernie, A.R. (2008). Inhibition of 2-oxoglutarate dehydrogenase in potato tuber suggests the enzyme is limiting for respiration and confirms its importance in nitrogen assimilation. Plant Physiol. 148: 1782-1796.
5. Bass, J., and Takahashi, J.S. (2010). Circadian integration of metabolism and energetics. Science 330: 1349-1354.
6. Begley, T.P., Downs, D.M., Ealick, S.E., McLafferty, F.W., Van Loon, A.P., Taylor, S., Campobasso, N., Chiu, H.J., Kinsland, C., Reddick, J.J., and Xi, J. (1999). Thiamin biosynthesis in prokaryotes. Arch. Microbiol. 171: 293-300.
7. Belanger, F.C., Leustek, T., Chu, B., and Kriz, A.L. (1995). Evidence for the thiamine biosynthetic pathway in higher-plant plastids and its developmental regulation. Plant Mol. Biol. 29: 809-821.
8. Bernier, G., Havelange, A., Houssa, C., Petitjean, A., and Lejeune, P. (1993). Physiological signals that induce flowering. Plant Cell 5: 1147-1155.
9. Berthon, H.A., Kuchel, P.W., and Nixon, P.F. (1992). High control coefficient of transketolase in the nonoxidative pentose phosphate pathway of human erythrocytes: NMR, antibody, and computer simulation studies. Biochemistry 31: 12792-12798.
10. Biemelt, S., Hajirezaei, M.R., Melzer, M., Albrecht, G., and Sonnewald, U. (1999). Sucrose synthase activity does not restrict glycolysis in roots of transgenic potato plants under hypoxic conditions. Planta 210: 41-49.
11. Bocobza, S., Adato, A., Mandel, T., Shapira, M., Nudler, E., and Aharoni, A. (2007). Riboswitch-dependent gene regulation and its evolution in the plant kingdom. Genes Dev. 21: 2874-2879.
12. Bocobza, S.E., and Aharoni, A. (2008). Switching the light on plant riboswitches. Trends Plant Sci. 13: 526-533.
13. Bunik, V.I., and Fernie, A.R. (2009). Metabolic control exerted by the 2-oxoglutarate dehydrogenase reaction: a cross-kingdom comparison of the crossroad between energy production and nitrogen assimilation. Biochem. J. 422: 405-421.
14. Callis, J., Raasch, J.A., and Vierstra, R.D. (1990). Ubiquitin extension proteins of Arabidopsis thaliana. Structure, localization, and expression of their promoters in transgenic tobacco. J. Biol. Chem. 265: 12486-12493.
15. Caspar, T., Lin, T.P., Kakefuda, G., Benbow, L., Preiss, J., and Somerville, C. (1991). Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol. 95: 1181-1188.
16. Cheah, M.T., Wachter, A., Sudarsan, N., and Breaker, R.R. (2007). Control of alternative RNA splicing and gene expression by eukaryotic riboswitches. Nature 447: 497-500.
17. Chuartzman, S.G., Nevo, R., Shimoni, E., Charuvi, D., Kiss, V., Ohad, I., Brumfeld, V., and Reich, Z. (2008). Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20: 1029-1039.
18. 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.
19. Covington, M.F., Maloof, J.N., Straume, M., Kay, S.A., and Harmer, S.L. (2008). Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9: R130.
20. Croft, M.T., Moulin, M., Webb, M.E., and Smith, A.G. (2007). Thiamine biosynthesis in algae is regulated by riboswitches. Proc. Natl. Acad. Sci. USA 104: 20770-20775.
21. Doyle, J.A., and Doyle, J.L. (1987). A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochem. Bull. 19: 11-15.
22. Fernie, A.R., Carrari, F., and Sweetlove, L.J. (2004). Respiratory metabolism: Glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 7: 254-261.
23. Fernie, A.R., Roscher, A., Ratcliffe, R.G., and Kruger, N.J. (2001). Fructose 2,6-bisphosphate activates pyrophosphate: Fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta 212: 250-263.
24. Frank, R.A., Leeper, F.J., and Luisi, B.F. (2007). Structure, mechanism and catalytic duality of thiamine-dependent enzymes. Cell. Mol. Life Sci. 64: 892-905.
25. Fraser, P.D., Pinto, M.E., Holloway, D.E., and Bramley, P.M. (2000). Technical advance: Application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J. 24: 551-558.
26. Fukushima, A., Kusano, M., Nakamichi, N., Kobayashi, M., Hayashi, N., Sakakibara, H., Mizuno, T., and Saito, K. (2009). Impact of clockassociated Arabidopsis pseudo-response regulators in metabolic coordination. Proc. Natl. Acad. Sci. USA 106: 7251-7256.
27. Gibon, Y., Blaesing, O.E., Hannemann, J., Carillo, P., Höhne, M., Hendriks, J.H., Palacios, N., Cross, J., Selbig, J., and Stitt, M. (2004). A Robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: Comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16: 3304-3325.
28. Graf, A., Schlereth, A., Stitt, M., and Smith, A.M. (2010). Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc. Natl. Acad. Sci. USA 107: 9458-9463.
29. Haus, E., and Touitow, Y. (1992). NModel software is based on Best fit cosine analysis method. In Biological Rhythms in Clinical and Laboratory Medicine, E. Haus and Y. Touitow, eds (Berlin: Springer Verlag), pp. 6-33.
30. Heintzen, C., Nater, M., Apel, K., and Staiger, D. (1997). AtGRP7, a nuclear RNA-binding protein as a component of a circadianregulated negative feedback loop in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94: 8515-8520.
31. Henkes, S., Sonnewald, U., Badur, R., Flachmann, R., and Stitt, M. (2001). A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell 13: 535-551.
32. Imaizumi, T., and Kay, S.A. (2006). Photoperiodic control of flowering: Not only by coincidence. Trends Plant Sci. 11: 550-558.
33. Kammann, M., Laufs, J., Schell, J., and Gronenborn, B. (1989). Rapid insertional mutagenesis of DNA by polymerase chain reaction (PCR). Nucleic Acids Res. 17: 5404.
34. Komeda, Y., Tanaka, M., and Nishimune, T. (1988). A th-1 mutant of Arabidopsis thaliana is defective for a thiamin-phosphate-synthesizing enzyme: Thiamin phosphate pyrophosphorylase. Plant Physiol. 88: 248-250.
35. Kong, D., Zhu, Y., Wu, H., Cheng, X., Liang, H., and Ling, H.Q. (2008). AtTHIC, a gene involved in thiamine biosynthesis in Arabidopsis thaliana. Cell Res. 18: 566-576.
36. Levy, Y.Y., and Dean, C. (1998). The transition to flowering. Plant Cell 10: 1973-1990.
37. 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: 387-396.
38. Lu, Y., Gehan, J.P., and Sharkey, T.D. (2005). Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol. 138: 2280-2291.
39. Lytovchenko, A., Bieberich, K., Willmitzer, L., and Fernie, A.R. (2002). Carbon assimilation and metabolism in potato leaves deficient in plastidial phosphoglucomutase. Planta 215: 802-811.
40. Machado, C.R., de Oliveira, R.L., Boiteux, S., Praekelt, U.M., Meacock, P.A., and Menck, C.F. (1996). Thi1, a thiamine biosynthetic gene in Arabidopsis thaliana, complements bacterial defects in DNA repair. Plant Mol. Biol. 31: 585-593.
41. Malitsky, S., Blum, E., Less, H., Venger, I., Elbaz, M., Morin, S., Eshed, Y., and Aharoni, A. (2008). The transcript and metabolite networks affected by the two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol. 148: 2021-2049.
42. Mandal, M., Boese, B., Barrick, J.E., Winkler, W.C., and Breaker, R.R. (2003). Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113: 577-586.
43. Mandal, M., and Breaker, R.R. (2004). Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat. Struct. Mol. Biol. 11: 29-35.
44. Marillia, E.F., Micallef, B.J., Micallef, M., Weninger, A., Pedersen, K.K., Zou, J., and Taylor, D.C. (2003). Biochemical and physiological studies of Arabidopsis thaliana transgenic lines with repressed expression of the mitochondrial pyruvate dehydrogenase kinase. J. Exp. Bot. 54: 259-270.
45. Mintz-Oron, S., Mandel, T., Rogachev, I., Feldberg, L., Lotan, O., Yativ, M., Wang, Z., Jetter, R., Venger, I., Adato, A., and Aharoni, A. (2008). Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol. 147: 823-851.
46. Mironov, A.S., Gusarov, I., Rafikov, R., Lopez, L.E., Shatalin, K., Kreneva, R.A., Perumov, D.A., and Nudler, E. (2002). Sensing small molecules by nascent RNA: A mechanism to control transcription in bacteria. Cell 111: 747-756.
47. Mizoguchi, T., Wheatley, K., Hanzawa, Y., Wright, L., Mizoguchi, M., Song, H.R., Carré, I.A., and Coupland, G. (2002). LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev. Cell 2: 629-641.
48. Molin, W.T., Wilkerson, C.G., and Fites, R.C. (1980). Thiamin phosphorylation by thiamin pyrophosphotransferase during seed germination. Plant Physiol. 66: 313-315.
49. Nakamichi, N., Kusano, M., Fukushima, A., Kita, M., Ito, S., Yamashino, T., Saito, K., Sakakibara, H., and Mizuno, T. (2009). Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol. 50: 447-462.
50. Nunes-Nesi, A., Carrari, F., Gibon, Y., Sulpice, R., Lytovchenko, A., Fisahn, J., Graham, J., Ratcliffe, R.G., Sweetlove, L.J., and Fernie, A.R. (2007). Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J. 50: 1093-1106.
51. Nunes-Nesi, A., Carrari, F., Lytovchenko, A., Smith, A.M., Loureiro, M.E., Ratcliffe, R.G., Sweetlove, L.J., and Fernie, A.R. (2005). Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol. 137: 611-622.
52. Randall, D.D., Miernyk, J.A., Fang, T.K., Budde, R.J., and Schuller, K.A. (1989). Regulation of the pyruvate dehydrogenase complexes in plants. Ann. N. Y. Acad. Sci. 573: 192-205.
53. Raschke, M., Bürkle, L., Müller, N., Nunes-Nesi, A., Fernie, A.R., Arigoni, D., Amrhein, N., and Fitzpatrick, T.B. (2007). Vitamin B1 biosynthesis in plants requires the essential iron sulfur cluster protein, THIC. Proc. Natl. Acad. Sci. USA 104: 19637-19642.
54. Refinetti, R., Cornelissen, G., and Halberg, F. (2007). Procedures for numerical analysis of circadian rhythms. Biol. Rhythm Res. 38: 275-325.
55. Rindi, G., and De Giuseppel, L. (1961). A new chromatographic method for the determination of thiamine and its mono-, di-and triphosphates in animal tissues. Biochem. J. 78: 602-606.
56. Roessner-Tunali, U., Liu, J., Leisse, A., Balbo, I., Perez-Melis, A., Willmitzer, L., and Fernie, A.R. (2004). Kinetics of labelling of organic and amino acids in potato tubers by gas chromatographymass spectrometry following incubation in (13)C labelled isotopes. Plant J. 39: 668-679.
57. Sambrook, J., Fritsch, E., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
58. Schweingruber, A.M., Dlugonski, J., Edenharter, E., and Schweingruber, M.E. (1991). Thiamine in Schizosaccharomyces pombe: Dephosphorylation, intracellular pool, biosynthesis and transport. Curr. Genet. 19: 249-254.
59. Sharkey, T.D., Savitch, L.V., and Butz, N.D. (1991). Photometric method for routine determination of kcat and carbamylation of rubisco. Photosynth. Res. 28: 41-48.
60. Sienkiewicz-Porzucek, A., Sulpice, R., Osorio, S., Krahnert, I., Leisse, A., Urbanczyk-Wochniak, E., Hodges, M., Fernie, A.R., and Nunes-Nesi, A. (2010). Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Mol. Plant 3: 156-173.
61. Singleton, C.K., and Martin, P.R. (2001). Molecular mechanisms of thiamine utilization. Curr. Mol. Med. 1: 197-207.
62. Stitt, M., and Zeeman, S.C. (2012). Starch turnover: Pathways, regulation and role in growth. Curr. Opin. Plant Biol. 15: 282-292.
63. Studart-Guimarães, C., Fait, A., Nunes-Nesi, A., Carrari, F., Usadel, B., and Fernie, A.R. (2007). Reduced expression of succinyl-coenzyme A ligase can be compensated for by up-regulation of the gamma-aminobutyrate shunt in illuminated tomato leaves. Plant Physiol. 145: 626-639.
64. Sudarsan, N., Cohen-Chalamish, S., Nakamura, S., Emilsson, G.M., and Breaker, R.R. (2005). Thiamine pyrophosphate riboswitches are targets for the antimicrobial compound pyrithiamine. Chem. Biol. 12: 1325-1335.
65. Tcherkez, G., Cornic, G., Bligny, R., Gout, E., and Ghashghaie, J. (2005). In vivo respiratory metabolism of illuminated leaves. Plant Physiol. 138: 1596-1606.
66. Tovar-Méndez, A., Miernyk, J.A., and Randall, D.D. (2003). Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur. J. Biochem. 270: 1043-1049.
67. Tschoep, H., Gibon, Y., Carillo, P., Armengaud, P., Szecowka, M., Nunes-Nesi, A., Fernie, A.R., Koehl, K., and Stitt, M. (2009). Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis. Plant Cell Environ. 32: 300-318.
68. Wachter, A., Tunc-Ozdemir, M., Grove, B.C., Green, P.J., Shintani, D.K., and Breaker, R.R. (2007). Riboswitch control of gene expression in plants by splicing and alternative 39 end processing of mRNAs. Plant Cell 19: 3437-3450.
69. Wang, J.J., Martin, P.R., and Singleton, C.K. (1997a). Aspartate 155 of human transketolase is essential for thiamine diphosphatemagnesium binding, and cofactor binding is required for dimer formation. Biochim. Biophys. Acta 1341: 165-172.
70. Wang, J.J., Martin, P.R., and Singleton, C.K. (1997b). A transketolase assembly defect in a Wernicke-Korsakoff syndrome patient. Alcohol. Clin. Exp. Res. 21: 576-580.
71. Wang, Z.Y., and Tobin, E.M. (1998). Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93: 1207-1217.
72. Winkler, W., Nahvi, A., and Breaker, R.R. (2002). Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419: 952-956.
73. Yu, T.S., Lue, W.L., Wang, S.M., and Chen, J. (2000). Mutation of Arabidopsis plastid phosphoglucose isomerase affects leaf starch synthesis and floral initiation. Plant Physiol. 123: 319-326.