Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth

Molecular Plant

Volumn 3, Issue 1, 2010, Pages 156-173

  Sienkiewicz Porzucek, Agata ^a   Sulpice, Ronan ^a   Osorio, Sonia ^a   Krahnert, Ina ^a   Leisse, Andrea ^a   Urbanczyk Wochniak, Ewa ^a   Hodges, Michael ^b   Fernie, Alisdair R ^a   Nunes Nesi, Adriano ^a  

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

^b INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

Carbon metabolism; Mitochondria; Nitrogen metabolism; Photorespiration; Photosynthesis; Tomato

Indexed keywords

LYCOPERSICON ESCULENTUM; SOLANUM;

EID: 76549093444     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssp101     Document Type: Article

References (91)

1. Abiko, T., Obara, M., Ushioda, A., Hayakawa, T., Hodges, M., and Yamaya, T. (2005). Localization of NAD-isocitrate dehydrogenase and glutamate dehydrogenase in rice roots: candidates for providing carbon skeletons to NADH-glutamate synthase. Plant Cell Physiol. 46, 1724-1734.
2. Alba, R., et al. (2004). ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant J. 39, 697-714.
3. ap Rees, T., and Beevers, H. (1960). Pathways of glucose dissimilation in carrot slices. Plant Physiol. 35, 830-838.
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. Aubert, S., Bligny, R., Douce, R., Gout, E., Ratcliffe, R.G., and Roberts, J.K.M. (2001). Contribution of glutamate dehydrogenase to mitochondrial glutamate metabolism studied by 13C and 31P nuclear magnetic resonance. J. Exp. Bot. 52, 37-45.
6. Bartoli, C.G., Gomez, F., Gergoff, G., Guiamet, J.J., and Puntarulo, S. (2005). Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. J. Exp. Bot. 56, 1269-1276.
7. Bender-Machado, L., et al. (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.
8. Bläsing, O., Gibon, Y., Günther, M., Höhne, M., Osuna, D., Thimm, T., Scheible, W.-R., Morcuende, R., and Stitt, M. (2005). Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell. 17, 3257-3281.
9. Boldt, R., Edner, C., Kolukisaoglu,Ü,Hagemann, M.,Weckwerth,W., Wienkoop, S., Morgenthal, K., and Bauwe, H. (2005). D-glycerate 3-kinase, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. Plant Cell. 17, 2413-2420.
10. Carrari, F., Nunes-Nesi, A., Gibon, Y., Lytovchenko, A., Ehlers-Loureiro, M., 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.
11. Chen, R. (1998). Plant NADP-dependent isocitrate dehydrogenases are predominantly localized in the cytosol. Planta. 207, 280-285.
12. Chen, R.D., and Gadal, P. (1990). Do the mitochondria provide the 2-oxoglutarate needed for glutamate synthesis in higher plant chloroplasts? Plant Physiol. Biochem. 28, 141-145.
13. Corpas, F.J., Barroso, J.B., Sandalio, L.M., Palma, J.M., Lupianez, J.A., and del Rio, L.A. (1999). Peroxisomal NADP-dependent isocitrate dehydrogenase: characterization and activity regulation during natural senescence. Plant Physiol. 121, 921-928.
14. Czechowski, T., Bari, R.P., Stitt, M., Scheible, W.R., and Udvardi, M.K. (2004). Real-time RT-sensitivity reveals novel rootand shoot-specific genes. Plant J. 38, 366-379.
15. Dutilleul, C., Driscoll, S., Cornic, G., De Paepe, R., Foyer, C.H., and Noctor, G. (2003). Functional mitochondrial complex I is required for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol. 131, 264-275.
16. 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.
17. Fernie, A.R., Carrari, F., and Sweetlove, L.J. (2004). Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport chain. Curr. Opin. Plant Biol. 7, 254-261.
18. 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.
19. Ferrario-Mery, S., Hodges, M., Hirel, B., and Foyer, C.H. (2002). Photorespiration-dependent increases in phosphoenolpyruvate carboxylase, isocitrate dehydrogenase and glutamate dehydrogenase in transformed tobacco plants deficient in ferredoxindependent glutamine-a-ketoglutarate aminotransferase. Planta. 214, 877-886. (Pubitemid 36059253)
20. Fieuw, S., Müller-Röber, B., Gálvez, S., and Willmitzer, L. (1995). Cloning and expression analysis of the cytosolic NADP+-dependent isocitrate dehydrogenase from potato. Plant Physiol. 107, 905-913.
21. Fritz, C., Palacios-Rojas, N., Feil, R., and Stitt, M. (2006). Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J. 46, 533-548.
22. Gallardo, F., Gálvez, S., Gadal, P., and Canovas, F.M. (1995). Changes in NADP+-linked isocitrate dehydrogenase during tomato fruit ripening. Planta. 196, 148-154.
23. Gálvez, S., Bismuth, E., Sarda, C., and Gadal, P. (1994). Purification and characterization of chloroplast NADP-isocitrate dehydrogenase from mixotrophic tobacco cells: comparison with the cytosolic isoenzyme. Plant Physiol. 105, 593-600.
24. Gálvez, S., Hodges, M., Decottignies, P., Bismuth, E., Lancien, M., Sangwan, R.S., Dubois, F., LeMaréchal, P., Cretin, C., and Gadal, P. (1996). Identification of a tobacco cDNA encoding a cytosolic NADP-isocitrate dehydrogenase. Plant Mol. Biol. 30, 307-320.
25. 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.
26. Gálvez, S., Roche, O., Bismuth, E., Brown, S., Gadal, P., and Hodges, M. (1998). Mitochondrial localization of a NADP-dependent isocitrate dehydrogenase isoenzyme by using the green fluorescent protein as a marker. Proc. Natl Acad. Sci. U S A. 95, 7813-7818.
27. 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.
28. Gaude, N., Brehelin, C., Tischendorf, G., Kessler, F., and Dormann, 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.
29. Gibon, Y., and Larher, F. (1997). Cycling assay for nicotinamide adenine dinucleotides: NaCl precipitation and ethanol solubilization of the reduced tetrazolium. Anal. Biochem. 251, 153-157.
30. Gibon, Y., Blaesing, O.E., Hannemann, J., Carrillo, P., Hohne, 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.
31. Gray, G.R., Villarimo, A.R., Whitehead, C.L., and McIntosh, L. (2004). Transgenic tobacco (Nicotiana tabacum L.) plants with increased expression levels of mitochondrial NADP+-dependent isocitrate dehydrogenase: evidence implicating this enzyme in the redox activation of the alternative oxidase. Plant Cell Physiol. 45, 1413-1425.
32. Herbers, K., and Sonnewald, U. (1998). Molecular determinants of sink strength. Curr. Opin. Plant Biol. 1, 207-216.
33. Higgins, D.G., and Sharp, P.M. (1988). CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 73, 237-244.
34. Hodges, M. (2002). Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J. Exp. Bot. 53, 905-916.
35. Hodges, M., Fleish, V., Gálvez, S., and Bismuth, E. (2003). Higher plant NADP dependent isocitrate dehydrogenases, ammonium assimilation and NADPH production. Plant Physiol. Biochem. 41, 577-585.
36. Hong, F., Breitling, R., McEntee, C.W., Wittner, B.S., Nemhauser, J.L., and Chory, J. (2006). RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics. 22, 2825-2827.
37. Huege, J., Sulpice, R., Gibon, Y., Lisec, J., Koehl, K., and Kopka, J. (2007). GC-EI-TOF-MS analysis of in vivo carbon-partitioning into soluble metabolite pools of higher plants by monitoring isotope dilution after (CO2)-C-13 labelling. Phytochemistry. 68, 2258-2272.
38. Igamberdiev, A.U., and Gardeström, P. (2003). Regulation of NADand NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochim. Biophys. Acta. 1606, 117-125.
39. Igamberdiev, A.U., Romanowska, E., and Gardeström, P. (2001). Photorespiratory flux and mitochondrial contribution to energy and redox balance of barley leaf protoplasts in the light and during light-dark transitions. J. Plant Physiol. 158, 1325-1332.
40. Jo, S.H., et al. (2001). Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J. Biol. Chem. 276, 16168-16176.
41. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195.
42. Kasimova, M.A., Grigiene, J., Krab, K., Hagedorn, P.H., Flyvbjerg, H., Andersen, P.E., and Møller, I.M. (2006). The free NADH concentration is kept constant in plant mitochondria under different metabolic conditions. Plant Cell. 18, 688-698.
43. Kopka, J., et al. (2005). GMD@CSB.DB: the Golm Metabolome Database. Bioinformatics. 21, 1635-1638.
44. Kruse, A., Fieuw, S., Heineke, D., and Müller-Röber, B. (1998). Antisense inhibition of cytosolic NADP-dependent isocitrate dehydrogenase in transgenic potato plants. Planta. 205, 82-91.
45. Lancien, M., Ferrario-Mery, S., Roux, V., Bismuth, E., Masclaux, C., Hirel, B., Gadal, P., and Hodges, M. (1999). Simultaneous expression of NAD-dependent isocitrate dehydrogenase and other Krebs cycle genes after nitrate resupply to short-term nitrogenstarved tobacco. Plant Physiol. 120, 717-725.
46. Lancien, M., Gadal, P., and Hodges, M. (1998). Molecular characterization of higher plant NAD-dependent isocitrate dehydrogenase: evidence for a heteromeric structure by the complementation of yeast mutants. Plant J. 16, 325-333.
47. 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.
48. Landschütze, V., Willmitzer, L., and Müller-Röber, B. (1995). Inhibition of flower formation by antisense repression of mitochondrial citrate synthase in transgenic potato plants leads to specific disintegration of the ovary tissues of flowers. EMBO J. 14, 660-666.
49. Lemaitre, T., and Hodges, M. (2006). Expression analysis of Arabidopsis thaliana NAD-dependent isocitrate dehydrogenase genes shows the presence of a functional subunit that is mainly expressed in the pollen and absent from vegetative organs. Plant Cell Physiol. 47, 634-643.
50. Lemaitre, T., Urbanczyk-Wochniak, E., Flesch, V., Bismuth, E., Fernie, A.R., and Hodges, M. (2007). NAD-dependent isocitrate dehydrogenase mutants of Arabidopsis suggest the enzyme is not limiting for nitrogen assimilation. Plant Physiol. 144, 1546-1558.
51. Liu, X.J., Prat, S., Willmitzer, L., and Frommer, W.B. (1999). Cisregulatory elements directing tuber specific and sucrose inducible expression of a chimeric class I patatin promoter-GUS gene fusion. Mol. Gen. Genet. 223, 101-106.
52. Møller, I.M., and Rasmusson, A.G. (1998). The role of NADP in the mitochondrial matrix. Trends Plant Sci. 3, 21-27.
53. Noctor, G., De Paepe, R., and Foyer, C.H. (2007).Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 12, 125-134.
54. 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.
55. Nunes-Nesi, A., Carrari, F., Lytovchenko, A., Smith, A.M.O., Ehlers-Loureiro, M., 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.
56. Nunes-Nesi, A., Sulpice, R., Gibon, Y., and Fernie, A.R. (2008). The enigmatic contribution of mitochondrial function in photosynthesis. J. Exp. Bot. 59, 1675-1684.
57. Obiadalla-Ali, H., Fernie, A.R., Lytovchenko, A., Kossmann, J., and Lloyd, J.R. (2004). Inhibition of chloroplastic fructose 1,6-bisphosphatase in tomato fruits leads to surprisingly small changes in carbohydrate metabolism and decreases fruit size. Planta. 219, 533-540.
58. Palomo, J., Gallardo, F., Suarez, M.F., and Canovas, F.M. (1998). Purification and characterization of NADP+-linked isocitrate dehydrogenase from Scots pine. Plant Physiol. 118, 617-626.
59. Pellny, T.K., et al. (2008). Mitochondrial respiratory pathways modulate nitrate sensing and nitrogen-dependent regulation of plant architecture in Nicotiana sylvestris. Plant J. 54, 976-992.
60. Raghavendra, A.S., and Padmasree, K. (2003). Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 8, 546-553.
61. Robinson, S.A., Slade, A.P., Fox, G.G., Phillips, R., Ratcliffe, R.G., and Stewart, G.R. (1991). The role of glutamate dehydrogenase in plant nitrogen metabolism. Plant Physiol. 95, 509-516.
62. 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.
63. 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.
64. 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 C-14 labelled isotopes. Plant J. 39, 668-679.
65. Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
66. Schaarschmidt, S., Roitsch, T., and Hause, B. (2006). Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. J. Exp. Bot. 57, 4015-4023.
67. Schauer, N., et al. (2005). GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett. 579, 1332-1337.
68. Scheibe, R. (2004). Malate valves to balance cellular energy balance. Physiol. Plant. 120, 21-26.
69. 2 evolution in spinach leaves. Plant Physiol. Biochem. 26, 473-481.
70. Scheible, W.R., Gonzalez-Fontes, A., Lauerer, M., Müller-Röber, B., Caboche, M., and Stitt, M. (1997). Nitrate acts as a signal to induce organic acid metabolism and represses starch metabolism in tobacco. Plant Cell. 9, 783-798.
71. Scheible, W.R., Krapp, A., and Stitt, M. (2000). Reciprocal diurnal changes of phosphoenolpyruvate and NADP-isocitrate dehydrogenase expression regulate organic acid metabolism during nitrate assimilation in tobacco leaves. Plant Cell Environ. 23, 1155-1167.
72. Schneidereit, J., Häusler, R.E., Fiene, G., Kaiser, W.M., and Weber, A.P.M. (2006). Antisense repression reveals a crucial role of the plastidic 2-oxoglutarate/malate translocator DiT1 at the interface between carbon and nitrogen metabolism. Plant J. 45, 206-224.
73. Siedow, J.N., and Day, D.A. (2000). Respiration and photorespiration. In Biochemistry and Molecular Biology of Plants, Buchanan B. Gruissem W. and Jones R., eds (Rockville, MD: American Society of Plant Physiologists), pp. 676-728.
74. 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.
75. Smyth, G.K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, 1-29.
76. Stitt, M., and Fernie, A.R. (2003). From measurement of metabolites to metabolomics. An 'on the fly' perspective illustrated by recent studies of carbon-nitrogen interactions. Curr. Opin. Biotechnol. 14, 136-144.
77. Strodtkötter, I., et al. (2009). Induction of the AOX1D isoform of alternative oxidase in A-thaliana T-DNA insertion lines lacking isoform AOX1A is insufficient to optimize photosynthesis when treated with antimycin A. Mol. Plant. 2, 284-297.
78. Studart-Guimaraes, C., Fait, A., Nunes-Nesi, A., Carrari, F., Usadel, B., and Fernie, A.R. (2007). Reduced expression of succinyl CoA ligase can be compensated for by an upregulation of the c-amino-butyrate (GABA) shunt in illuminated tomato leaves. Plant Physiol. 145, 626-639.
79. 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.
80. 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 photosynthesis. Proc. Natl Acad. Sci. U S A. 103, 19587-19592.
81. 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.
82. 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.
83. Tercé-Laforgue, T., Dubois, F., Ferrario-Mery, S., Pou de Crecenzo, M.A., Sangwan, R., and Hirel, B. (2004). Glutamate dehydrogenase of tobacco is mainly induced in the cytosol of phloem companion cells when ammonia is provided either externally or released during photorespiration. Plant Physiol. 136, 4308-4317.
84. 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. U S A. 103, 8287-8292.
85. Urbanczyk-Wochniak, E., Baxter, C., Kolbe, A., Kopka, J., Sweetlove, L.J., and Fernie, A.R. (2005). Profiling of diurnal patterns of metabolite and transcript abundance in potato (Solanum tuberosum) leaves. Planta. 221, 891-903.
86. Urbanczyk-Wochniak, E., et al. (2006). Conversion of MapMan to allow the analysis of transcript data from Solanaceous species: effects of genetic and environmental alterations in energy metabolism in the leaf. Plant Mol. Biol. 60, 773-792.
87. Usadel, B., Nagel, A., Thimm, O., Redestig, H., Blaesing, O.E., Palacios-Rojas, N., Selbig, J., Hannemann, J., Piques, M.C., and Steinhauser, D. (2005). Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol. 138, 1195-1204.
88. Van der Hoeven, R., Ronning, C., Giovannoni, J., Martin, G., and Tanksley, S. (2003). 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.
89. 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.
90. 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.
91. Zanor, M.I., et al. (2009). RNA interference of LIN5 in Solanum lycopersicum 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.