2-oxoglutarate: Linking TCA cycle function with amino acid, glucosinolate, flavonoid, alkaloid, and gibberellin biosynthesis

Frontiers in Plant Science

Volumn 5, Issue OCT, 2014, Pages

  Araújo, Wagner L ^a   Martins, Auxiliadora O ^a   Fernie, Alisdair R ^b   Tohge, Takayuki ^b  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

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

Author keywords

2 Oxoglutarate dependent dioxygenases; Alkaloid; Dioxygenases; Flavonoid; Gibberellin; TCA cycle

Indexed keywords

EID: 84907993199     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00552     Document Type: Article

References (53)

1. Araújo, W. L., Nunes-Nesi, A., Nikoloski, Z., Sweetlove, L. J., and Fernie, A. R. (2012a). Metabolic control and regulation of the tricarboxylic acid cycle in pho-tosynthetic and heterotrophic plant tissues. Plant Cell Environ. 35, 1–21. doi: 10.1111/j.1365-3040.2011.02332.x
2. Araújo, W. L., Tohge, T., Osorio, S., Lohse, M., Balbo, I., Krahnert, I., et al. (2012b). Antisense inhibition of the 2-oxoglutarate dehydrogenase complex in tomato demonstrates its importance for plant respiration and during leaf senescence and fruit maturation. Plant Cell 24, 2328–2351. doi: 10.1105/tpc.112.099002
3. 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. doi: 10.1104/pp.108.126219
4. Araujo, W. L., Tohge, T., Nunes-Nesi, A., Daloso, D. M., Nimick, M., Krahnert, I., et al. (2012). Phosphonate analogs of 2-oxoglutarate perturb metabolism and gene expression in illuminated Arabidopsis leaves. Front. Plant Sci. 3:114. doi: 10.3389/fpls.2012.00114
5. Biemelt, S., Tschiersch, H., and Sonnewald, U. (2004). Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol. 135, 254–265. doi: 10.1104/pp.103.036988
6. Dayan, J., Schwarzkopf, M., Avni, A., and Aloni, R. (2010). Enhancing plant growth and fiber production by silencing GA 2-oxidase. Plant Biotechnol. J. 8, 425–435. doi: 10.1111/j.1467-7652.2009.00480.x
7. 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. doi: 10.1016/j.tplants.2007.10.005
8. Feria Bourrellier, A. B., Ferrario-Méry, S., Vidal, J., and Hodges, M. (2009). Metabolite regulation of the interaction between Arabidopsis thaliana PII and N-acetyl-l-glutamate kinase. Biochem. Biophys. Res. Commun. 387, 700–704. doi: 10.1016/j.bbrc.2009.07.088
9. Feria Bourrellier, A. B., Valot, B., Guillot, A., Ambard-Bretteville, F., Vidal, J., and Hodges, M. (2010). Chloroplast acetyl-CoA carboxylase activity is 2-oxoglutarate–regulated by interaction of PII with the biotin carboxyl carrier subunit. Proc. Natl. Acad. Sci. U.S.A. 107, 502–507. doi: 10.1073/pnas.0910097107
10. Ferrario-Mery, S., Besin, E., Pichon, O., Meyer, C., and Hodges, M. (2006). The regulatory PII protein controls arginine biosynthesis in Arabidopsis. FEBS Lett. 580, 2015–2020. doi: 10.1016/j.febslet.2006.02.075
11. Ferrario-Mery, S., Masclaux, C., Suzuki, A., Valadier, M. H., Hirel, B., and Foyer, C. H. (2001). Glutamine and alpha-ketoglutarate are metabolite signals involved in nitrate reductase gene transcription in untransformed and transformed tobacco plants deficient in ferredoxin-glutamine-alpha-ketoglutarate aminotransferase. Planta 213, 265–271. doi: 10.1007/s004250000504
12. Foyer, C. H., Parry, M., and Noctor, G. (2003). Markers and signals associated with nitrogen assimilation in higher plants. J. Exp. Bot. 54, 585–593. doi: 10.1093/jxb/erg053
13. Frey, M., Huber, K., Park, W. J., Sicker, D., Lindberg, P., Meeley, R. B., et al. (2003). A 2-oxoglutarate-dependent dioxygenase is integrated in DIMBOA-biosynthesis. Phytochemistry 62, 371–376. doi: 10.1016/S0031-9422(02)00556-3
14. Gauthier, P. P. G., Bligny, R., Gout, E., Mahé, A., Nogués, S., Hodges, M., et al. (2010). In folio isotopic tracing demonstrates that nitrogen assimilation into glu-tamate is mostly independent from current CO2 assimilation in illuminated leaves of Brassica napus. New Phytol. 185, 988–999. doi: 10.1111/j.1469-8137.2009. 03130.x
15. Graebe, J. E. (1987). Gibberellin biosynthesis and control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 38, 419–465. doi: 10.1146/annurev.pp.38.060187.002223
16. Griggs, D. L., Hedden, P., and Lazarus, C. M. (1991). Partial-purification of 2 gibberellin 2-beta-hydroxylases from cotyledons of Phaseolus vulgaris. Phytochemistry 30, 2507–2512. doi: 10.1016/0031-9422(91)85090-M
17. Hagel, J. M., and Facchini, P. J. (2010). Dioxygenases catalyze the O-demethylation steps of morphine biosynthesis in opium poppy. Nat. Chem. Biol. 6, 273–275. doi: 10.1038/nchembio.317
18. Hansen, B. G., Kerwin, R. E., Ober, J. A., Lambrix, V. M., Mitchell-Olds, T., Ger-shenzon, J., et al. (2008). A novel 2-oxoacid-dependent dioxygenase involved in the formation of the goiterogenic 2-hydroxybut-3-enyl glucosinolate and generalist insect resistance in Arabidopsis. Plant Physiol. 148, 2096–2108. doi: 10.1104/pp.108.129981
19. Hedden, P., Phinney, B. O., Heupel, R., Fujii, D., Cohen, H., Gaskin, P., et al. (1982). Hormones of young tassels of Zea mays. Phytochemistry 21, 391–393. doi: 10.1016/S0031-9422(00)95273-7
20. Hodges, M. (2002). Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J. Exp. Bot. 53, 905–916. doi: 10.1093/jexbot/53.370.905
21. Jan, A., Nakamura, H., Handa, H., Ichikawa, H., Matsumoto, H., and Komatsu, S. (2006). Gibberellin regulates mitochondrial pyruvate dehydrogenase activity in rice. Plant Cell Physiol. 47, 244–253. doi: 10.1093/pcp/pci241
22. Kai, K., Mizutani, M., Kawamura, N., Yamamoto, R., Tamai, M., Yamaguchi, H., et al. (2008). Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana. Plant J. 55, 989–999. doi: 10.1111/j.1365-313X.2008.03568.x
23. Kawai, Y., Ono, E., and Mizutani, M. (2014). Evolution and diversity of the 2-oxoglutarate-dependent dioxygenase superfamily in plants. Plant J. 78, 328–343. doi: 10.1111/tpj.12479
24. Kliebenstein, D. J., Lambrix, V. M., Reichelt, M., Gershenzon, J., and Mitchell-Olds, T. (2001). Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosi-nolate biosynthesis in Arabidopsis. Plant Cell 13, 681–693. doi: 10.1105/tpc.13.3.681
25. Lancien, M., Gadal, P., and Hodges, M. (2000). Enzyme redundancy and the importance of 2-oxoglutarate in higher plant ammonium assimilation. Plant Physiol. 123, 817–824. doi: 10.1104/pp.123.3.817
26. Lange, T., and Graebe, J. E. (1989). The partial purification and characterization of a gibberellin C-20 hydroxylase from immature Pisum sativum L. seeds. Planta 179, 211–221. doi: 10.1007/BF00393691
27. Liu, T., Zhu, P., Cheng, K. D., Meng, C., and Zhu, H. X. (2005). Molecular cloning and expression of putrescine N-methyltransferase from the hairy roots of Anisodus tanguticus. Planta Med. 71, 987–989. doi: 10.1055/s-2005-871260
28. Loenarz, C., and Schofield, C. J. (2008). Expanding chemical biology of 2-oxoglutarate oxygenases. Nat. Chem. Biol. 4, 152–156. doi: 10.1038/nchembio0308-152
29. Martens, S., Forkmann, G., Matern, U., and Lukacin, R. (2001). Cloning of parsley flavone synthase I. Phytochemistry 58, 43–46. doi: 10.1016/S0031-9422(01) 00191-1
30. Martens, S., Preuß, A., and Matern, U. (2010). Multifunctional flavonoid dioxygenases: flavonol and anthocyanin biosynthesis in Arabidopsis thaliana L. Phytochemistry 71, 1040–1049. doi: 10.1016/j.phytochem.2010.04.016
31. Matsuda, J., Okabe, S., Hashimoto, T., and Yamada, Y. (1991). Molecular cloning of hyoscyamine 6-beta-hydroxylase, a 2-oxoglutarate dependent dioxygenase from cultured roots of Hyoscyamus niger. J. Biol. Chem. 266, 9460–9464.
32. Nakanishi, H., Yamaguchi, H., Sasakuma, T., Nishizawa, N. K., and Mori, S. (2000). Two dioxygenase genes, Ids3 and Ids2, from Hordeum vulgare are involved in the biosynthesis of mugineic acid family phytosiderophores. Plant Mol. Biol. 44, 199–207. doi: 10.1023/A:1006491521586
33. Ozer, A., and Bruick, R. K. (2007). Non-heme dioxygenases: cellular sensors and regulators jelly rolled into one? Nat. Chem. Biol. 3, 144–153. doi: 10.1038/nchembio863
34. Prescott, A. G. (1993). A dilemma of dioxygenases (or where biochemistry and molecular biology fail to meet). J. Exp. Bot. 44, 849–861. doi: 10.1093/jxb/44.5.849
35. Prescott, A. G., and John, P. (1996). Dioxygenases: molecular structure and role in plant metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 245–271. doi: 10.1146/annurev.arplant.47.1.245
36. Sá Santos, S., Gibson, G. E., Cooper, A. J. L., Denton, T. T., Thompson, C. M., Bunik, V. I., et al. (2006). Inhibitors of the α-ketoglutarate dehydrogenase complex alter [1-13C]glucose and [U-13C]glutamate metabolism in cerebellar granule neurons. J. Neurosci. Res. 83, 450–458. doi: 10.1002/jnr.20749
37. Scheible, W. R., Krapp, A., and Stitt, M. (2000). Reciprocal diurnal changes of phosphoenolpyruvate carboxylase expression and cytosolic pyru-vate kinase, citrate synthase and NADP-isocitrate dehydrogenase expression regulate organic acid metabolism during nitrate assimilation in tobacco leaves. Plant Cell Environ. 23, 1155–1167. doi: 10.1046/j.1365-3040.2000.00634.x
38. Shi, Q., Risa, Ø., Sonnewald, U., and Gibson, G. E. (2009). Mild reduction in the activity of the alpha-ketoglutarate dehydrogenase complex elevates GABA shunt and glycolysis. J. Neurochem. 109, 214–221. doi: 10.1111/j.1471-4159.2009.05955.x
39. Sienkiewicz-Porzucek, A., Nunes-Nesi, A., Sulpice, R., Lisec, J., Centeno, D. C., Carillo, P., et al. (2008). Mild reductions in mitochondrial citrate synthase activity result in a compromised nitrate assimilation and reduced leaf pigmentation but have no effect on photosynthetic performance or growth. Plant Physiol. 147, 115–127. doi: 10.1104/pp.108.117978
40. Sienkiewicz-Porzucek, A., Sulpice, R., Osorio, S., Krahnert, I., Leisse, A., Urbanczyk-Wochniak, E., et al. (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. doi: 10.1093/mp/ssp101
41. Smith, V. A., Gaskin, P., and Macmillan, J. (1990). Partial purification and characterization of the gibberellin A20 3-beta-hydroxylase from seeds of Phaseolus vulgaris. Plant Physiol. 94, 1390–1401. doi: 10.1104/pp.94.3.1390
42. Smith, V. A., and Macmillan, J. (1986). The partial purification and characterisation of gibberellin 2 beta -hydroxylases from seeds of Pisum sativum. Planta 167, 9–18. doi: 10.1007/BF00446362
43. Stafford, H. A. (1991). Flavonoid evolution – an enzymatic approach. Plant Physiol. 96, 680–685. doi: 10.1104/pp.96.3.680
44. Suzuki, K., Yun, D. J., Chen, X. Y., Yamada, Y., and Hashimoto, T. (1999). An Atropa belladonna hyoscyamine 6 beta-hydroxylase gene is differentially expressed in the root pericycle and anthers. Plant Mol. Biol. 40, 141–152. doi: 10.1023/A:1026465518112
45. Tohge, T., Watanabe, M., Hoefgen, R., and Fernie, A. R. (2013). The evolution of phenylpropanoid metabolism in the green lineage. Crit. Rev. Biochem. Mol. Biol. 48, 123–152. doi: 10.3109/10409238.2012.758083
46. Turnbull, J. J., Nakajima, J.-I., Welford, R. W. D., Yamazaki, M., Saito, K., and Schofield, C. J. (2004). Mechanistic studies on three 2-oxoglutarate-dependent oxygenases of flavonoid biosynthesis: anthocyanidin synthase, flavonol synthase, and flavanone 3|3-hydroxylase. J. Biol. Chem. 279, 1206-1216. doi: 10.1074/jbc.M309228200
47. Uhrig, R. G., Ng, K. K. S., and Moorhead, G. B. G. (2009). PII in higher plants: a modern role for an ancient protein. Trends Plant Sci. 14, 505-511. doi: 10.1016/j.tplants.2009.07.003
48. Vaillancourt, F. H., Bolin, J. T., and Eltis, L. D. (2006). The ins and outs of ring-cleaving dioxygenases. Crit. Rev. Biochem. Mol. Biol. 41, 241-267. doi: 10.1080/10409230600817422
49. van der Merwe, M. J., Osorio, S., Moritz, T., Nunes-Nesi, A., and Fernie, A. R. (2009). Decreased mitochondrial activities of malate dehydrogenase and fumarase in tomato lead to altered root growth and architecture via diverse mechanisms. Plant Physiol. 149, 653-669. doi: 10.1104/pp.108.130518
50. ;H): a missing step in the synthesis of umbelliferone in plants. Plant J. 70, 460-470. doi: 10.1080/10409230600817422
51. Weber, A., and Flügge, U. I. (2002). Interaction of cytosolic and plastidic nitrogen metabolism in plants. J. Exp. Bot. 53, 865-874. doi: 10.1093/jexbot/53.370.865
52. Yamaguchi, S. (2008). Gibberellin metabolism and its regulation. Annu. Rev. Plant Biol. 59,225-251. doi: 10.1146/annurev.arplant.59.032607.092804
53. Yazaki, J., Kishimoto, N., Nagata, Y., Ishikawa, M., Fujii, F., Hashimoto, A., et al. (2003). Genomics approach to abscisic acid- and gibberellin-responsive genes in rice. DNA Res. 10, 249–261. doi: 10.1093/dnares/10.6.249