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

Volumn 24, Issue 6, 2012, Pages 2328-2351

  Araújo, Wagner L ^a,b   Tohge, Takayuki ^a   Osorio, Sonia ^a   Lohse, Marc ^a   Balbo, Ilse ^a   Krahnert, Ina ^a   Sienkiewicz Porzucek, Agata ^a   Usadel, Björn ^a,c   Nunes Nesi, Adriano ^b   Fernie, Alisdair R ^a  

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

^b FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LYCOPERSICON ESCULENTUM;

EID: 84864478052     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.099002     Document Type: Article

References (136)

1. Aharoni, N., and Richmond, A.E. (1978). Endogenous gibberellin and abscisic acid content as related to senescence of detached lettuce leaves. Plant Physiol. 62: 224-228.
2. ap Rees, T.A., and Beevers, H. (1960). Pathways of glucose dissimilation in carrot slices. Plant Physiol. 35: 830-838.
3. Araújo, W.L., Ishizaki, K., Nunes-Nesi, A., Larson, T.R., Tohge, T., Krahnert, I., Witt, S., Obata, T., Schauer, N., Graham, I.A., Leaver, C.J., and Fernie, A.R. (2010). Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22: 1549-1563.
4. Araújo, W.L., Ishizaki, K., Nunes-Nesi, A., Tohge, T., Larson, T.R., Krahnert, I., Balbo, I., Witt, S., Dörmann, P., Graham, I.A., Leaver, C.J., and Fernie, A.R. (2011b). Analysis of a range of catabolic mutants provides evidence that phytanoyl-coenzyme A does not act as a substrate of the electron-transfer flavoprotein/ electron-transfer flavoprotein:ubiquinone oxidoreductase complex in Arabidopsis during dark-induced senescence. Plant Physiol. 157: 55-69.
5. Araújo, W.L., Nunes-Nesi, A., Nikoloski, Z., Sweetlove, L.J., and Fernie, A.R. (2012). Metabolic control and regulation of the tri-carboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant Cell Environ. 35: 1-21.
6. Araújo, W.L. et al. (2011a). Antisense inhibition of the iron-sulfur subunit of succinate dehydrogenase enhances photosynthesis and growth in tomato via an organic acid-mediated effect on stomatal aperture. Plant Cell 23: 600-627.
7. 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.
8. Back, A., and Richmond, A.E. (1971). Interrelations between gibberellic acid, cytokinins and abscisic acid in retarding leaf senescence. Physiol. Plant. 24: 76-79.
9. Bapat, V.A., Trivedi, P.K., Ghosh, A., Sane, V.A., Ganapathi, T.R., and Nath, P. (2010). Ripening of fleshy fruit: Molecular insight and the role of ethylene. Biotechnol. Adv. 28: 94-107.
10. Barth, C., De Tullio, M., and Conklin, P.L. (2006). The role of ascorbic acid in the control of flowering time and the onset of senescence. J. Exp. Bot. 57: 1657-1665.
11. Bender-Machado, L., Bäuerlein, M., Carrari, F., Schauer, N., Lytovchenko, A., Gibon, Y., Kelly, A.A., Loureiro, M., Müller-Röber, B., Willmitzer, L., and Fernie, A.R. (2004). Expression of a yeast acetyl CoA hydrolase in the mitochondrion of tobacco plants inhibits growth and restricts photosynthesis. Plant Mol. Biol. 55: 645-662.
12. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289-300.
13. Bleecker, A.B., and Patterson, S.E. (1997). Last exit: Senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9: 1169-1179.
14. Brangeon, J., Sabar, M., Gutierres, S., Combettes, B., Bove, J., Gendy, C., Chétrit, P., Des Francs-Small, C.C., Pla, M., Vedel, F.,and De Paepe, R. (2000). Defective splicing of the first nad4 intron is associated with lack of several complex I subunits in the Nicotiana sylvestris NMS1 nuclear mutant. Plant J. 21: 269-280.
15. Bugos, R.C., Chiang, V.L., Zhang, X.H., Campbell, E.R., Podila, G.K., and Campbell, W.H. (1995). RNA isolation from plant tissues recalcitrant to extraction in guanidine. Biotechniques 19: 734-737.
16. 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.
17. Caldana, C., Scheible, W.R., Mueller-Roeber, B., and Ruzicic, S. (2007). A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 3: 7.
18. Carlsson, J., Leino, M., Sohlberg, J., Sundström, J.F., and Glimelius, K. (2008). Mitochondrial regulation of flower development. Mitochondrion 8: 74-86.
19. Carrari, F., Baxter, C., Usadel, B., Urbanczyk-Wochniak, E., Zanor, M.I., Nunesnesi, A., Nikiforova, V., Ratzka, A., Pauly, M., Sweetlove, L.J., and Fernie, A.R. (2006). Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol. 142: 1380-1396.
20. Carrari, F., Fernie, A.R., and Iusem, N.D. (2004). Heard it through the grapevine? ABA and sugar cross-talk: The ASR story. Trends Plant Sci. 9: 57-59.
21. Carrari, F., Nunes-Nesi, A., Gibon, Y., Lytovchenko, A., Loureiro, M.E., and Fernie, A.R. (2003). Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of wild species tomato. Plant Physiol. 133: 1322-1335.
22. Chin, T.Y., and Beevers, L. (1970). Changes in endogenous growth regulators in nasturtium leaves during senescence. Planta 92: 178-188.
23. Cornu, S., Pireaux, J.C., Gerard, J., and Dizengremel, P. (1996). NAD(P)-dependent isocitrate dehydrogenases in mitochondria purified from Picea abies seedlings. Physiol. Plant. 96: 312-318.
24. Coruzzi, G., and Last, R. (2000). Amino acids. In Biochemistry and Molecular Biology of Plants, B.B. Buchanan, W. Gruissem, and R.L. Jones, eds (Rockville, MD: American Society of Plant Biologists), pp. 358-410.
25. Csukasi, F., Osorio, S., Gutierrez, J.R., Kitamura, J., Giavalisco, P., Nakajima, M., Fernie, A.R., Rathjen, J.P., Botella, M.A., Valpuesta, V., and Medina-Escobar, N. (2011). Gibberellin biosynthesis and signalling during development of the strawberry receptacle. New Phytol. 191: 376-390.
26. Czechowski, T., Bari, R.P., Stitt, M., Scheible, W.R., and Udvardi, M.K. (2004). Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: Unprecedented sensitivity reveals novel root-and shoot-specific genes. Plant J. 38: 366-379.
27. de Oliveira Dal'Molin, C.G., Quek, L.E., Palfreyman, R.W., Brumbley, S.M., and Nielsen, L.K. (2010). AraGEM, a genomescale reconstruction of the primary metabolic network in Arabidopsis. Plant Physiol. 152: 579-589.
28. Dry, I.B., and Wiskich, J.T. (1985). Inhibition of 2-oxoglutarate oxidation in plant mitochondria by pyruvate. Biochem. Biophys. Res. Commun. 133: 397-403.
29. Dubois, F., Brugière, N., Sangwan, R.S., and Hirel, B. (1996). Localization of tobacco cytosolic glutamine synthetase enzymes and the corresponding transcripts shows organ-and cell-specific patterns of protein synthesis and gene expression. Plant Mol. Biol. 31: 803-817.
30. Dutilleul, C., Lelarge, C., Prioul, J.L., De Paepe, R., Foyer, C.H., and Noctor, G. (2005). Mitochondria-driven changes in leaf NAD status exert a crucial influence on the control of nitrate assimilation and the integration of carbon and nitrogen metabolism. Plant Physiol. 139: 64-78.
31. 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.
32. Fernie, A.R., Aharoni, A., Willmitzer, L., Stitt, M., Tohge, T., Kopka, J., Carroll, A.J., Saito, K., Fraser, P.D., and DeLuca, V. (2011). Recommendations for reporting metabolite data. Plant Cell 23: 2477-2482.
33. Fernie, A.R., Carrari, F., and Sweetlove, L.J. (2004b). Respiratory metabolism: Glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 7: 254-261.
34. 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.
35. Fernie, A.R., Trethewey, R.N., Krotzky, A., and Willmitzer, L. (2004a). Metabolic profiling: From diagnostics to systems biology. Nat. Rev. Mol. Cell Biol. 5: 1-7.
36. 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.
37. Gálvez, S., Lancien, M., and Hodges, M. (1999). Are isocitrate dehydrogenases and 2-oxoglutarate involved in the regulation of glutamate synthesis? Trends Plant Sci. 4: 484-490.
38. Gan, S., and Amasino, R.M. (1997). Making sense of senescence: Molecular genetic regulation and manipulation of leaf senescence. Plant Physiol. 113: 313-319.
39. Garmier, M., Carroll, A.J., Delannoy, E., Vallet, C., Day, D.A., Small, I.D., and Millar, A.H. (2008). Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis. Plant Physiol. 148: 1324-1341.
40. Gaude, N., Bréhélin, C., Tischendorf, G., Kessler, F., and Dörmann, P. (2007). Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters. Plant J. 49: 729-739.
41. Gauthier, P.P.G., Bligny, R., Gout, E., Mahé, A., Nogués, S., Hodges, M., and Tcherkez, G.G.B. (2010). In folio isotopic tracing demonstrates that nitrogen assimilation into glutamate is mostly independent from current CO2 assimilation in illuminated leaves of Brassica napus. New Phytol. 185: 988-999.
42. Gibon, Y., Blaesing, O.E., Hannemann, J., Carillo, P., Höhne, M., Hendriks, J.H.M., 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.
43. Goldwaithe, J.J. (1972). Further studies of hormone regulated senescence in Rumex leaf tissue. In Plant Growth Substances, D.J. Carr, ed (Berlin: Springer), pp. 581-588.
44. Goldthwaite, J.J., and Laetsch, W.M. (1968). Control of senescence in Rumex leaf discs by gibberellic acid. Plant Physiol. 43: 1855-1858.
45. Grbic, V., and Bleecker, A.B. (1995). Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J. 8: 595-602.
46. Greenboim-Wainberg, Y., Maymon, I., Borochov, R., Alvarez, J., Olszewski, N., Ori, N., Eshed, Y., and Weiss, D. (2005). Cross talk between gibberellin and cytokinin: The Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 17: 92-102.
47. Gu, L., Jones, A.D., and Last, R.L. (2010). Broad connections in the Arabidopsis seed metabolic network revealed by metabolite profiling of an amino acid catabolism mutant. Plant J. 61: 579-590.
48. Gutierres, S., Sabar, M., Lelandais, C., Chetrit, P., Diolez, P., Degand, H., Boutry, M., Vedel, F., de Kouchkovsky, Y., and De Paepe, R. (1997). Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc. Natl. Acad. Sci. USA 94: 3436-3441.
49. Hedden, P., and Kamiya, Y. (1997). Gibberellin biosynthesis: Enzymes, genes and their regulation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 431-460.
50. Higgins, D.G., and Sharp, P.M. (1988). CLUSTAL: A package for performing multiple sequence alignment on a microcomputer. Gene 73: 237-244.
51. Hodges, M. (2002). Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J. Exp. Bot. 53: 905-916.
52. Hörtensteiner, S. (2006). Chlorophyll degradation during senescence. Annu. Rev. Plant Biol. 57: 55-77.
53. Hung, K.T., and Kao, C.H. (2004). Hydrogen peroxide is necessary for abscisic acid-induced senescence of rice leaves. J. Plant Physiol. 161: 1347-1357.
54. Hurry, V., Igamberdiev, A.U., Keerberg, O., Pärnik, T., Atkin, O.K., Zaragoza-Castells, J., and Gardeström, P. (2005). Respiration in photosynthetic cells: Gas exchange components, interactions with photorespiration and the operation of mitochondria in the light. In Plant Respiration: From Cell to Ecosystem, Vol. 18, Advances in Photosynthesis and Respiration Series, H. Lambers and M. RibasCarbo, eds (Dordrecht, The Netherlands: Springer), pp. 43-61.
55. Igamberdiev, A.U., and Gardeström, P. (2003). Regulation of NAD-and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochim. Biophys. Acta 1606: 117-125.
56. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., and Speed, T.P. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
57. Ishizaki, K., Larson, T.R., Schauer, N., Fernie, A.R., Graham, I.A.,and Leaver, C.J. (2005). The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17: 2587-2600.
58. Ishizaki, K., Schauer, N., Larson, T.R., Graham, I.A., Fernie, A.R., and Leaver, C.J. (2006). The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J. 47: 751-760.
59. Jing, H.C., Sturre, M.J., Hille, J., and Dijkwel, P.P. (2002). Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. Plant J. 32: 51-63.
60. Kappers, I.F., Jordi, W., Maas, F.M., Stoopen, G.M., and van der Plas, L.H.W. (1998). Gibberellin and phytochrome control senescence in Alstromeria leaves independently. Physiol. Plant. 103: 91-98.
61. Karpova, O.V., Kuzmin, E.V., Elthon, T.E., and Newton, K.J. (2002). Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell 14: 3271-3284.
62. Keeling, P.L., Wood, J.R., Tyson, R.H., and Bridges, I.G. (1988). Starch biosynthesis in developing wheat grain: Evidence against the direct involvement of triose phosphates in the metabolic pathway. Plant Physiol. 87: 311-319.
63. Lange, T., Schweimer, A., Ward, D.A., Hedden, P., and Graebe, J.E. (1994). Separation and characterization of three 2-oxoglutarate-dependent dioxygenases from Cucurbita maxima L. endosperm involved in gibberellin biosynthesis. Planta 195: 98-107.
64. León, G., Holuigue, L., and Jordana, X. (2007). Mitochondrial complex II is essential for gametophyte development in Arabidopsis. Plant Physiol. 143: 1534-1546.
65. León, P., and Sheen, J. (2003). Sugar and hormone connections. Trends Plant Sci. 8: 110-116.
66. Less, H., and Galili, G. (2008). Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol. 147: 316-330.
67. Lim, P.O., Kim, H.J., and Nam, H.G. (2007). Leaf senescence. Annu. Rev. Plant Biol. 58: 115-136.
68. Lim, P.O., Woo, H.R., and Nam, H.G. (2003). Molecular genetics of leaf senescence in Arabidopsis. Trends Plant Sci. 8: 272-278.
69. Lin, Z., Zhong, S., and Grierson, D. (2009). Recent advances in ethylene research. J. Exp. Bot. 60: 3311-3336.
70. Linke, B., and Börner, T. (2005). Mitochondrial effects on flower and pollen development. Mitochondrion 5: 389-402.
71. 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.
72. Liu, X.J., Prat, S., Willmitzer, L., and Frommer, W.B. (1990) Cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I patatin promoter/GUS-gene fusion. Mol. Gen. Genet. 223: 401-406.
73. Liu, Y.J., Nunes-Nesi, A., Wallström, S.V., Lager, I., Michalecka, A.M., Norberg, F.E., Widell, S., Fredlund, K.M., Fernie, A.R., and Rasmusson, A.G. (2009). A redox-mediated modulation of stem bolting in transgenic Nicotiana sylvestris differentially expressing the external mitochondrial NADPH dehydrogenase. Plant Physiol. 150: 1248-1259.
74. Lohse, M. et al. (2010). Robin: An intuitive wizard application for R-based expression microarray quality assessment and analysis. Plant Physiol. 153: 642-651.
75. Loreti, E., Povero, G., Novi, G., Solfanelli, C., Alpi, A., and Perata, P. (2008). Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol. 179: 1004-1016.
76. Lytovchenko, A., Sweetlove, L.J., Pauly, M., and Fernie, A.R. (2002). The influence of cytosolic phosphoglucomutase on photo-synthetic carbohydrate metabolism. Planta 215: 1013-1021.
77. Manos, P.J., and Goldwaithe, J.J. (1975). A kinetic analysis of the effects of gibberellic acid, zeatin, and abscisic acid on leaf tissue senescence in Rumex. Plant Physiol. 55: 192-198.
78. Marienfeld, J.R., and Newton, K.J. (1994). The maize NCS2 abnormal growth mutant has a chimeric nad4-nad7 mitochondrial gene and is associated with reduced complex I function. Genetics 138: 855-863.
79. Masclaux, C., Valadier, M.H., Brugière, N., Morot-Gaudry, J.F., and Hirel, B. (2000). Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211: 510-518.
80. Masclaux-Daubresse, C., Valadier, M.-H., Carrayol, E., Reisdorf-Cren, M., and Hirel, B. (2002). Diurnal changes in the expression of glutamate dehydrogenase and nitrate reductase are involved in the C/N balance of tobacco source leaves. Plant Cell Environ. 25: 1451-1462.
81. Millar, A.H., Eubel, H., Jänsch, L., Kruft, V., Heazlewood, J.L., and Braun, H.-P. (2004). Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol. Biol. 56: 77-90.
82. Moore, B., Zhou, L., Rolland, F., Hall, Q., Cheng, W.H., Liu, Y.X., Hwang, I., Jones, T., and Sheen, J. (2003). Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300: 332-336.
83. 2+, adenine nucleotides and pH on the kinetic properties of mitochondrial NAD(+)-isocitrate dehydrogenase and oxoglutarate dehydrogenase from the yeast Saccharomyces cerevisiae and rat heart. Biochem. J. 303: 461-465.
84. Noctor, G., Dutilleul, C., De Paepe, R., and Foyer, C.H. (2004). Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. J. Exp. Bot. 55: 49-57.
85. Noguchi, K., and Yoshida, K. (2008). Interaction between photo-synthesis and respiration in illuminated leaves. Mitochondrion 8: 87-99.
86. Nunes-Nesi, A., Araújo, W.L., and Fernie, A.R. (2011). Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis. Plant Physiol. 155: 101-107.
87. 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. (2007a). Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J. 50: 1093-1106.
88. 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.
89. Nunes-Nesi, A., Sweetlove, L.J., and Fernie, A.R. (2007b). Operation and function of the tricarboxlic acid cycle in the illuminated leaf. Physiol. Plant. 129: 45-56.
90. Oh, S.A., Lee, S.Y., Chung, I.K., Lee, C.H., and Nam, H.G. (1996). A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol. Biol. 30: 739-754.
91. 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.
92. Pineau, B., Mathieu, C., Gérard-Hirne, C., De Paepe, R., and Chétrit, P. (2005). Targeting the NAD7 subunit to mitochondria restores a functional complex I and a wild type phenotype in the Nicotiana sylvestris CMS II mutant lacking nad7. J. Biol. Chem. 280: 25994-26001.
93. Poolman, M.G., Miguet, L., Sweetlove, L.J., and Fell, D.A. (2009). A genome-scale metabolic model of Arabidopsis and some of its properties. Plant Physiol. 151: 1570-1581.
94. Pruzinská, A., Tanner, G., Aubry, S., Anders, I., Moser, S., Müller, T., Ongania, K.-H., Kräutler, B., Youn, J.-Y., Liljegren, S.J., and Hörtensteiner, S. (2005). Chlorophyll breakdown in senescent Arabidopsis leaves: Characterization of chlorophyll catabolites and chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol. 139: 52-63.
95. Raghavendra, A.S., and Padmasree, K. (2003). Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 8: 546-553.
96. Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L., and Fernie, A.R. (2001). Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13: 11-29.
97. Roessner-Tunali, U., Hegemann, B., Lytovchenko, A., Carrari, F., Bruedigam, C., Granot, D., and Fernie, A.R. (2003). Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol. 133: 84-99.
98. 13)C labelled isotopes. Plant J. 39: 668-679.
99. Roschzttardtz, H., Fuentes, I., Vásquez, M., Corvalán, C., León, G., Gómez, I., Araya, A., Holuigue, L., Vicente-Carbajosa, J., and Jordana, X. (2009). A nuclear gene encoding the iron-sulfur subunit of mitochondrial complex II is regulated by B3 domain transcription factors during seed development in Arabidopsis. Plant Physiol. 150: 84-95.
100. Rosenvasser, S., Mayak, S., and Friedman, H. (2006). Increase in reactive oxygen species (ROS) and in senescence-associated gene transcript (SAG) levels during dark-induced senescence of Pelargonium cuttings, and the effect of gibberellic acid. Plant Sci. 170: 873-879.
101. Rossel, J.B., Wilson, P.B., Hussain, D., Woo, N.S., Gordon, M.J., Mewett, O.P., Howell, K.A., Whelan, J., Kazan, K., and Pogson, B.J. (2007). Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 19: 4091-4110.
102. Sabar, M., De Paepe, R., and de Kouchkovsky, Y. (2000). Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol. 124: 1239-1250.
103. Saitou, N., and Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
104. Schauer, N., Steinhauser, D., Strelkov, S., Schomburg, D., Allison, G., Moritz, T., Lundgren, K., Roessner-Tunali, U., Forbes, M.G., Willmitzer, L., Fernie, A.R., and Kopka, J. (2005). GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett. 579: 1332-1337.
105. Scheibe, R., Backhausen, J.E., Emmerlich, V., and Holtgrefe, S. (2005). Strategies to maintain redox homeostasis during photo-synthesis under changing conditions. J. Exp. Bot. 56: 1481-1489.
106. Schippers, J.H.M., Nunes-Nesi, A., Apetrei, R., Hille, J., Fernie, A.R., and Dijkwel, P.P. (2008). The Arabidopsis onset of leaf death5 mutation of quinolinate synthase affects nicotinamide adenine dinucleotide biosynthesis and causes early ageing. Plant Cell 20: 2909-2925.
107. Schnable, P.S., and Wise, R.P. (1998). The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci. 3: 175-180.
108. Serrani, J.C., Carrera, E., Ruiz-Rivero, O., Gallego-Giraldo, L., Peres, L.E.P., and García-Martínez, J.L. (2010). Inhibition of auxin transport from the ovary or from the apical shoot induces parthenocarpic fruit-set in tomato mediated by gibberellins. Plant Physiol. 153: 851-862.
109. Sienkiewicz-Porzucek, A., Nunes-Nesi, A., Sulpice, R., Lisec, J., Centeno, D.C., Carillo, P., Leisse, A., Urbanczyk-Wochniak, E.,and Fernie, A.R. (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.
110. 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.
111. Smyth, G.K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol 3
112. 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.
113. Sweetlove, L.J., Beard, K.F.M., Nunes-Nesi, A., Fernie, A.R., and Ratcliffe, R.G. (2010). Not just a circle: Flux modes in the plant TCA cycle. Trends Plant Sci. 15: 462-470.
114. Sweetlove, L.J., Fait, A., Nunes-Nesi, A., Williams, T., and Fernie, A.R. (2007). The mitochondrion: An integration point in cellular metabolism and signalling. Crit. Rev. Plant Sci. 26: 17-43.
115. Sweetlove, L.J., and Fernie, A.R. (2005). Regulation of metabolic networks: Understanding metabolic complexity in the systems biology era. New Phytol. 168: 9-24.
116. Sweetlove, L.J., Lytovchenko, A., Morgan, M., Nunes-Nesi, A., Taylor, N.L., Baxter, C.J., Eickmeier, I., and Fernie, A.R. (2006). Mitochondrial uncoupling protein is required for efficient photo-synthesis. Proc. Natl. Acad. Sci. USA 103: 19587-19592.
117. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
118. Tauberger, E., Fernie, A.R., Emmermann, M., Renz, A., Kossmann, J., Willmitzer, L., and Trethewey, R.N. (2000). Antisense inhibition of plastidial phosphoglucomutase provides compelling evidence that potato tuber amyloplasts import carbon from the cytosol in the form of glucose-6-phosphate. Plant J. 23: 43-53.
119. Taylor, L., Nunes-Nesi, A., Parsley, K., Leiss, A., Leach, G., Coates, S., Wingler, A., Fernie, A.R., and Hibberd, J.M. (2010). Cytosolic pyruvate,orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content. Plant J. 62: 641-652.
120. Tieman, D., Taylor, M., Schauer, N., Fernie, A.R., Hanson, A.D., and Klee, H.J. (2006). Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proc. Natl. Acad. Sci. USA 103: 8287-8292.
121. 13C isotopic labeling and H/D isotope effects highlight the noncyclic nature of the tricarboxylic acid "cycle" in illuminated leaves. Plant Physiol. 151: 620-630.
122. Usadel, B., Nagel, A., Steinhauser, D., Gibon, Y., Bläsing, O.E., Redestig, H., Sreenivasulu, N., Krall, L., Hannah, M.A., Poree, F., Fernie, A.R., and Stitt, M. (2006). PageMan: An interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics 7: 535.
123. van der Hoeven, R., Ronning, C., Giovannoni, J., Martin, G., and Tanksley, S. (2002). Deductions about the number, organization, and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencing. Plant Cell 14: 1441-1456.
124. van der Merwe, M.J., Osorio, S., Araújo, W.L., Balbo, I., Nunes-Nesi, A., Maximova, E., Carrari, F., Bunik, V.I., Persson, S., and Fernie, A.R. (2010). Tricarboxylic acid cycle activity regulates tomato root growth via effects on secondary cell wall production. Plant Physiol. 153: 611-621.
125. 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.
126. van Doorn, W.G. (2004). Is petal senescence due to sugar starvation? Plant Physiol. 134: 35-42.
127. van Doorn, W.G. (2008). Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels? J. Exp. Bot. 59: 1963-1972.
128. Wang, S., Liu, J., Feng, Y., Niu, X., Giovannoni, J., and Liu, Y. (2008). Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant J. 55: 89-103.
129. Watson, J.M., Fusaro, A.F., Wang, M.B., and Waterhouse, P.M. (2005). RNA silencing platforms in plants. FEBS Lett. 579: 5982-5987.
130. Whyte, P., and Luckwill, L.C. (1966). A sensitive bioassay for gibberellins based on retardation of leaf senescence in Rumex obtusifolious. Nature 210: 1360.
131. Wingler, A., Purdy, S., MacLean, J.A., and Pourtau, N. (2006). The role of sugars in integrating environmental signals during the regulation of leaf senescence. J. Exp. Bot. 57: 391-399.
132. Wingler, A., and Roitsch, T. (2008). Metabolic regulation of leaf senescence: Interactions of sugar signalling with biotic and abiotic stress responses. Plant Biol (Stuttg) 10 (suppl. 1): 50-62.
133. Xu, P., Zhang, Y.J., Kang, L., Roossinck, M.J., and Mysore, K.S. (2006). Computational estimation and experimental verification of off-target silencing during posttranscriptional gene silencing in plants. Plant Physiol. 142: 429-440.
134. Yang, S.F. (1987). The role of ethylene and ethylene biosynthesis in fruit ripening. In Plant Senescence: Its Biochemistry and Physiology, W.W. Thomson, E.A. Nothnagel, and R.C. Huffaker, eds (Rockville, MD: American Society of Plant Physiologists), pp. 156-165.
135. Zanor, M.I. et al. (2009). RNA interference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiol. 150: 1204-1218.
136. Zhu, X., and Galili, G. (2003). Increased lysine synthesis coupled with a knockout of its catabolism synergistically boosts lysine content and also transregulates the metabolism of other amino acids in Arabidopsis seeds. Plant Cell 15: 845-853.