Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function

Plant Journal

Volumn 50, Issue 6, 2007, Pages 1093-1106

  Nunes Nesi, Adriano ^a   Carrari, Fernando ^a,c   Gibon, Yves ^a   Sulpice, Ronan ^a   Lytovchenko, Anna ^a   Fisahn, Joachim ^a   Graham, James ^b   Ratcliffe, R George ^b   Sweetlove, Lee J ^b   Fernie, Alisdair R ^a  

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

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

Author keywords

Fumarase; Malate; Photosynthesis; Stomatal function; Transcript and metabolite profiles; Tricarboxylic acid cycle

Indexed keywords

OXIDATION; PHOTOSYNTHESIS; PLANTS (BOTANY);

FUMARASE; METABOLITE PROFILES; STOMATAL FUNCTION; TRICARBOXYLIC ACID CYCLE;

ENZYME ACTIVITY;

CARBON; COMPLEMENTARY DNA; FUMARATE HYDRATASE; MALIC ACID; MALIC ACID DERIVATIVE;

ARTICLE; BIOMASS; CHLOROPLAST; CITRIC ACID CYCLE; ELECTRON TRANSPORT; ENZYMOLOGY; FRUIT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOCHONDRION; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; PLANT ROOT; TOMATO; TRANSGENIC PLANT;

BIOMASS; CARBON; CHLOROPLASTS; CITRIC ACID CYCLE; DNA, COMPLEMENTARY; ELECTRON TRANSPORT; FRUIT; FUMARATE HYDRATASE; LYCOPERSICON ESCULENTUM; MALATES; MITOCHONDRIA; PHOTOSYNTHESIS; PLANT LEAVES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED;

ENZYMES; OXIDATION; PHOTOSYNTHESIS; PLANTS;

LYCOPERSICON ESCULENTUM; SOLANUM;

EID: 34250174823     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03115.x     Document Type: Article

References (44)

1. Baxter, C.J., Carrari, F., Bauke, A., Overy, S., Hill, S.A., Quick, P.W., Fernie, A.R. Sweetlove, L.J. (2005) Fruit carbohydrate metabolism in an introgression line of tomato with increased fruit soluble solids. Plant Cell Physiol. 46, 425 437.
2. Behal, R.H. Oliver, D.J. (1997) Biochemical and molecular characterization of fumarase from plants. Purification and characterization of the enzyme - cloning. sequencing and expression of the gene. Arch. Biochem. Biophys. 165, 397 406.
3. Bender-Machado, L., Bäuerlein, M., Carrari, F. 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.
4. Carrari, F., Nunes-Nesi, A., Gibon, Y., Lytovchenko, A., Ehlers-Loureiro, M. 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.
5. Catoni, E., Schwab, R., Hilpert, M., Desimone, M., Schwacke, R., Flugge, U.I., Schumacher, K. Frommer, W.B. (2003) Identification of an Arabidopsis mitochondrial succinate-fumarate translocator. FEBS Lett. 534, 87 92.
6. Chia, D.W., Yoder, T.J., Reiter, W.D. Gibson, S.I. (2000) Fumaric acid an overlooked form of fixed carbon in Arabidopsis and other plant species. Planta, 211, 743 751.
7. Falk, K.L., Behal, R.H., Xiang, C. Oliver, D.J. (1998) Metabolic bypass of the tricarboxylic acid cycle during lipid mobilization in germinating oilseeds. Regulation of NAD + -dependent isocitrate dehydrogenase versus fumarase. Plant Physiol. 117, 473 481.
8. Fernie, A.R., Roscher, A., Ratcliffe, R.G. 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.
9. Fernie, A.R., Trethewey, R.N., Krotzky, A. Willmitzer, L. (2004a) Metabolic profiling: from diagnostics to systems biology. Nat. Rev. Mol. Cell Biol. 5, 1 7.
10. Fernie, A.R., Carrari, F. Sweetlove, L.J. (2004b) Respiratory metabolism: glycolysis the TCA cycle and mitochondrial electron transport chain. Curr. Opin. Plant Biol. 7, 254 261.
11. Gibon, Y., Vigeolas, H., Tiessen, A., Geigenberger, P. Stitt, M. (2002) Sensitive and high throughput metabolite assays for inorganic pyrophosphate, ADPGlc, nucleotide phosphates and glycolytic intermediates based on a novel cycling system. Plant J. 30, 221 233.
12. Gibon, Y., Blaesing, O.E., Hannemann, J., Carillo, P., Hohne, M., Hendriks, J.H.M., Palacios, N., Cross, J., Selbig, J. Stitt, M. (2004) A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes in enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell, 16, 3304 3325.
13. Gout, E., Bligny, R., Pascal, N. Douce, R. (1993) C-13 nuclear-magnetic-resonance studies of malate and citrate synthesis and compartmentation in higher plant cells. J. Biol. Chem. 268, 3986 3992.
14. Holtzapffel, R.C., Finnegan, P.M., Millar, A.H., Badger, M.R. Day, D.A. (2002) Mitochondrial protein expression in tomato fruit during on-vine ripening and cold storage. Funct. Plant Biol. 29, 827 834.
15. Jenner, H., Winning, B., Millar, A.H., Tomlinson, K., Leaver, C.J. Hill, S.A. (2001) NAD malic enzyme and the control of carbohydrate metabolism in potato tubers. Plant Physiol. 126, 1139 1149.
16. Keeling, P.L., Wood, J.R., Tyson, R.W. Bridges, I.G. (1988) Starch biosynthesis in developing wheat grain. Plant Physiol. 52, 111 118.
17. Kim, S.H. Lee, W.S. (2002) Participation of extracellular fumarase in the utilization of malate in cultured carrot cells. Plant Cell Rep. 20, 1087 1092.
18. Liu, X.J., Prat, S., Willmitzer, L. Frommer, W.B. (1999) Cis-regulatory elements directing tuber specific and sucrose inducible expression of a chimeric class I patatin promoter-GUS gene fusion. Mol. Gen. Genet. 223, 101 106.
19. Liu, K., Fu, H.H., Bei, Q.X. Luan, S. (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol. 124, 1315 1325.
20. Lytovchenko, A., Sweetlove, L.J., Pauly, M. Fernie, A.R. (2002) The influence of cytosolic phosphoglucomutase on photosynthetic carbohydrate metabolism. Planta, 215, 1013 1021.
21. Martinoia, E. Rentsch, D. (1994) Malate compartmentation - responses to a complex metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 447 467.
22. Millar, A.H., Day, D.A. Whelan, J. (2004) Mitochondrial biogenesis and function in Arabidopsis. In The Arabidopsis Book Somerville, C.R. Meyerowitz, E.M., eds). Rockville, MD : American Society of Plant Biologists, doi: 10.1199/tab.0105 http://www.aspb.org/publications/arabidopsis/.
23. Nast, G. Müller-Röber, B. (1996) Molecular characterization of potato fumarate hydratase and functional expression in Escherichia coli. Plant Physiol. 112, 1219 1227.
24. Nunes-Nesi, A., Carrari, F., Lytovchenko, A., Smith, A.M., Loureiro, M.E., Ratcliffe, R.G., Sweetlove, L.J. 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.
25. Outlaw, W.H. (2003) Integration of cellular and physiological functions of guard cells. Crit. Rev. Plant Sci. 22, 503 529.
26. Plaxton, W.C. Podesta, F.E. (2006) The functional organization and control of plant respiration. Crit. Rev. Plant Sci. 25, 159 198.
27. Pracharoenwattana, I., Cornah, J.E. Smith, S.M. (2005) Arabidopsis peroxisomal citrate synthase is required for fatty acid respiration and seed germination. Plant Cell, 17, 2037 2048.
28. Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L. Fernie, A.R. (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell, 13, 11 29.
29. Roessner-Tunali, U., Hegemann, B., Lytovchenko, A., Carrari, F., Bruedigam, C., Granot, D. 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.
30. Sambrook, J., Fritsch, EF. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
31. Sass, E., Karniely, S. Pines, O. (2003) Folding of fumarase during mitochondrial import determines its dual targeting in yeast. J. Biol. Chem. 278, 45109 45116.
32. Schauer, N., Steinhauser, D., Strelkov, S. et al. (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett. 579, 1332 1337.
33. Scheibe, R. Stitt, M. (1988) Comparison of NADP-malate dehydrogenase activation QA reduction and O2 evolution in spinach leaves. Plant Physiol. Biochem. 26, 473 481.
34. Scheibe, R., Backhausen, J.E., Emmerlich, V. Holtgrefe, S. (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J. Exp. Bot. 56, 1481 1489.
35. Sharkey, T.D. Vanderveer, P.J. (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol. 91, 679 684.
36. Sharkey, T.D., Savitch, L.V. Butz, N.D. (1991) Photometric method for routine determination of kcat and carbamylation of rubisco. Photosynth. Res. 28, 41 48.
37. Shaw, C.R. Prasad, R. (1970) Starch gel electrophoresis of enzymes: a compilation of recipes. Biochem. Genet. 4, 297.
38. Shen, T.Y. Oden, P.C. (2002) Relationship between seed vigour and fumarase activity in Picea abies, Pinus contorta, Betula pendula and Fagus sylvatica. Seed Sci. Technol. 30, 177 186.
39. Stitt, M. (1997) The flux of carbon between the chloroplast and the cytoplasm. In Plant Metabolism (Dennis, D.T., Turpin, D.H., Lefebre, D.D. Layzell, D.B., eds). Harlow : Longman, pp. 382 400.
40. Studart-Guimarães, C., Gibon, Y., Frankel, N., Wood, C.C., Zanor, M.I., Fernie, A.R. Carrari, F. (2005) Identification and characterisation of the alpha and beta subunits of succinyl CoA ligase of tomato. Plant Mol. Biol. 59, 781 791.
41. Sweetlove, L.J., Heazelwood, J.L., Herald, V., Holtzapffel, R., Day, D.A., Leaver, C.J. Millar, A.H. (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J. 32, 891 904.
42. Tauberger, E., Fernie, A.R., Emmermann, M., Renz, A., Kossmann, J., Willmitzer, L. 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.
43. Urbanczyk-Wochniak, E., Usadel, B., Thimm, O. 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.
44. Van der Hoeven, R., Ronning, C., Giovannoni, J., Martin, G. 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.