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Abstract:

Arabidopsis thaliana possesses two fumarase genes (FUM), AtFUM1 (At2g47510) encoding for the mitochondrial Krebs cycle-associated enzyme and AtFUM2 (At5g50950) for the cytosolic isoform required for fumarate massive accumulation. Here, the comprehensive biochemical studies of AtFUM1 and AtFUM2 shows that they are active enzymes with similar kinetic parameters but differential regulation. For both enzymes, fumarate hydratase (FH) activity is favored over the malate dehydratase (MD) activity; however, MD is the most regulated activity with several allosteric activators. Oxalacetate, glutamine, and/or asparagine are modulators causing the MD reaction to become preferred over the FH reaction. Activity profiles as a function of pH suggest a suboptimal FUM activity in Arabidopsis cells; moreover, the direction of the FUM reaction is sensitive to pH changes. Under mild oxidation conditions, AtFUMs form high mass molecular aggregates, which present both FUM activities decreased to a different extent. The biochemical properties of oxidized AtFUMs (oxAtFUMs) were completely reversed by NADPH-supplied Arabidopsis leaf extracts, suggesting that the AtFUMs redox regulation can be accomplished in vivo. Mass spectrometry analyses indicate the presence of an active site-associated intermolecular disulfide bridge in oxAtFUMs. Finally, a phylogenetic approach points out that other plant species may also possess cytosolic FUM2 enzymes mainly encoded by paralogous genes, indicating that the evolutionary history of this trait has been drawn through a process of parallel evolution. Overall, according to our results, a multilevel regulatory pattern of FUM activities emerges, supporting the role of this enzyme as a carbon flow monitoring point through the organic acid metabolism in plants. © 2018 Federation of European Biochemical Societies

Registro:

Documento: Artículo
Título:The complex allosteric and redox regulation of the fumarate hydratase and malate dehydratase reactions of Arabidopsis thaliana Fumarase 1 and 2 gives clues for understanding the massive accumulation of fumarate
Autor:Zubimendi, J.P.; Martinatto, A.; Valacco, M.P.; Moreno, S.; Andreo, C.S.; Drincovich, M.F.; Tronconi, M.A.
Filiación:Centro de Estudios Fotosintéticos y Bioquímicos (CEFOBI), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario (UNR)Santa Fe, Argentina
Departamento de Química Biológica, Facultad de Ciencias exactas y Naturales, Universidad de Buenos Aires (UBA), Argentina
Facultad de Ciencias Agrarias, Universidad Nacinal de Rosario (UNR), Campo Experimental Villarino, CC No 14, Zavalla, Santa Fe 2123, Argentina
Palabras clave:allosteric and redox regulation; Arabidopsis; enzyme kinetics; fumarase; paralogous genes; asparagine; fumarate hydratase; glutamine; hydrolyase; malic acid derivative; oxaloacetic acid; protein aggregate; allosterism; Arabidopsis thaliana; bioaccumulation; controlled study; Editorial; enzyme activity; enzyme analysis; enzyme kinetics; mass spectrometry; nonhuman; oxidation reduction reaction; pH; phylogeny; phytochemistry; plant cell; priority journal; protein function
Año:2018
Volumen:285
Número:12
Página de inicio:2205
Página de fin:2224
DOI: http://dx.doi.org/10.1111/febs.14483
Título revista:FEBS Journal
Título revista abreviado:FEBS J.
ISSN:1742464X
CODEN:FJEOA
CAS:asparagine, 70-47-3, 7006-34-0; fumarate hydratase, 9032-88-6; glutamine, 56-85-9, 6899-04-3; hydrolyase, 9044-86-4; oxaloacetic acid, 149-63-3, 328-42-7
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_1742464X_v285_n12_p2205_Zubimendi

Referencias:

  • Tseng, C.P., Yu, C.C., Lin, H.H., Chang, C.Y., Kuo, J.T., Oxygen- and growth rate-dependent regulation of Escherichia coli fumarase (FumA, FumB, and FumC) activity (2001) J Bacteriol, 183, pp. 461-467
  • Woods, S.A., Miles, J.S., Roberts, R.E., Guest, J.R., Structural and functional relationships between fumarase and aspartase. Nucleotide sequences of the fumarase (fumC) and aspartase (aspA) genes of Escherichia coli K12 (1986) Biochem J, 237, pp. 547-557
  • Weaver, T.M., Levitt, D.G., Donnelly, M.I., Stevens, P.P., Banaszak, L.J., The multisubunit active site of fumarase C from Escherichia coli (1995) Nat Struct Biol, 2, pp. 654-662
  • Weaver, T., Lees, M., Zaitsev, V., Zaitseva, I., Duke, E., Lindley, P., McSweeny, S., Keruchenko, I., Crystal structures of native and recombinant yeast fumarase (1998) J Mol Biol, 280, pp. 431-442
  • Picaud, S., Kavanagh, K.L., Yue, W.W., Lee, W.H., Muller-Knapp, S., Gileadi, O., Sacchettini, J., Oppermann, U., Structural basis of fumarate hydratase deficiency (2011) J Inherit Metab Dis, 34, pp. 671-676
  • Puthan Veetil, V., Fibriansah, G., Raj, H., Thunnissen, A.M.W.H., Poelarends, G.J., Aspartase/fumarase superfamily: a common catalytic strategy involving general base-catalyzed formation of a highly stabilized aci-carboxylate intermediate (2012) Biochemistry, 51, pp. 4237-4243
  • Yogev, O., Naamati, A., Pines, O., Fumarase: a paradigm of dual targeting and dual localized functions (2011) FEBS J, 278, pp. 4230-4242
  • Suzuki, T., Yoshida, T., Tuboi, S., Evidence that rat liver mitochondrial and cytosolic fumarases are synthesized from one species of mRNA by alternative translational initiation at two in-phase AUG codons (1992) Eur J Biochem, 207, pp. 767-772
  • Sass, E., Blachinsky, E., Karniely, S., Pines, O., Mitochondrial and cytosolic isoforms of yeast fumarase are derivatives of a single translation product and have identical amino termini (2001) J Biol Chem, 276, pp. 46111-46117
  • Yogev, O., Yogev, O., Singer, E., Shaulian, E., Goldberg, M., Fox, T.D., Pines, O., Fumarase: a mitochondrial metabolic enzyme and a cytosolic/nuclear component of the DNA damage response (2010) PLoS Biol, 8
  • Pracharoenwattana, I., Zhou, W., Keech, O., Francisco, P.B., Udomchalothorn, T., Tschoep, H., Stitt, M., Smith, S.M., Arabidopsis has a cytosolic fumarase required for the massive allocation of photosynthate into fumaric acid and for rapid plant growth on high nitrogen (2010) Plant J, 62, pp. 785-795
  • Araújo, W.L., Nunes-Nesi, A., Fernie, A.R., Fumarate: multiple functions of a simple metabolite (2011) Phytochemistry, 72, pp. 838-843
  • Chia, D.W., Yoder, T.J., Reiter, W.D., Gibson, S.I., Fumaric acid: an overlooked form of fixed carbon in Arabidopsis and other plant species (2000) Planta, 211, pp. 743-751
  • Lee, C.P., Eubel, H., Millar, A.H., Diurnal changes in mitochondrial function reveal daily optimization of light and dark respiratory metabolism in Arabidopsis (2010) Mol Cell Proteomics, 9, pp. 2125-2139
  • Sweetlove, L.J., Beard, K.F., Nunes-Nesi, A., Fernie, A.R., Ratcliffe, R.G., Not just a circle: flux modes in the plant TCA cycle (2010) Trends Plant Sci, 15, pp. 462-470
  • Kosower, N.S., Kosower, E.M., Formation of disulfides with diamide (1987) Methods Enzymol, 143, pp. 264-270
  • Snedden, W.A., Blumwald, E., Alternative splicing of a novel diacylglycerol kinase in tomato leads to a calmodulin-binding isoform (2000) Plant J, 24, pp. 317-326
  • Werneke, J.M., Chatfield, J.M., Ogren, W.L., Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis (1989) Plant Cell, 1, pp. 815-825
  • Krebs, H.A., The equilibrium constants of the fumarase and aconitase systems (1953) Biochem J, 54, pp. 78-82
  • Estévez, M., Skarda, J., Spencer, J., Banaszak, L., Weaver, T.M., X-ray crystallographic and kinetic correlation of a clinically observed human fumarase mutation (2002) Protein Sci, 11, pp. 1552-1557
  • Pines, O., Even-Ram, S., Elnathan, N., Battat, E., Aharonov, O., Gibson, D., Goldberg, I., The cytosolic pathway of L-malic acid synthesis in Saccharomyces cerevisiae: the role of fumarase (1996) Appl Microbiol Biotechnol, 46, pp. 393-399
  • Winter, H., Robinson, D., Heldt, H., Subcellular volumes and metabolite concentrations in barley leaves (1993) Planta, 191, pp. 180-190
  • Winter, H., Robinson, D.G., Heldt, H.W., Subcellular volumes and metabolite concentrations in spinach leaves (1994) Planta, 193, pp. 530-535
  • Weiner, H., Heldt, H., Inter- and intracellular distribution of amino acids and other metabolites in maize (Zea mays L.) leaves (1992) Planta, 187, pp. 242-246
  • Jones, D.L., Organic acids in the rhizosphere – a critical review (1998) Plant Soil, 205, pp. 25-44
  • Scheible, W.R., Krapp, A., Stitt, M., Reciprocal diurnal changes of phosphoenolpyruvate carboxylase expression and cytosolic pyruvate kinase, citrate synthase and NADP-isocitrate dehydrogenase expression regulate organic acid metabolism during nitrate assimilation in tobacco leaves (2000) Plant Cell Environ, 23, pp. 1155-1167
  • Igarashi, D., Tsuchida, H., Miyao, M., Ohsumi, C., Glutamate: glyoxylate aminotransferase modulates amino acid content during photorespiration (2006) Plant Physiol, 142, pp. 901-910
  • Scheible, W.R., Gonzalez-Fontes, A., Lauerer, M., Muller-Rober, B., Caboche, M., Stitt, M., Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco (1997) Plant Cell, 9, pp. 783-798
  • Tschoep, H., Gibon, Y., Carillo, P., Armengaud, P., Szecowka, M., Nunes-Nesi, A., Fernie, A.R., Stitt, M., Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis (2009) Plant Cell Environ, 32, pp. 300-318
  • Wang, R., Guegler, K., LaBrie, S.T., Crawford, N.M., Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate (2000) Plant Cell, 12, pp. 1491-1509
  • Behal, R.H., Oliver, D.J., Biochemical and molecular characterization of fumarase from plants: purification and characterization of the enzyme–cloning, sequencing, and expression of the gene (1997) Arch Biochem Biophys, 348, pp. 65-74
  • Yoshida, K., Noguchi, K., Motohashi, K., Hisabori, T., Systematic exploration of thioredoxin target proteins in plant mitochondria (2013) Plant Cell Physiol, 54, pp. 875-892
  • Daloso, D.M., Müller, K., Obata, T., Florian, A., Tohge, T., Bottcher, A., Riondet, C., Nunes-Nesi, A., Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant mitochondria (2015) Proc Natl Acad Sci U S A, 112, pp. E1392-E1400
  • Chi, Y.H., Paeng, S.K., Kim, M.J., Hwang, G.Y., Melencion, S.M.B., Oh, H.T., Lee, S.Y., Redox-dependent functional switching of plant proteins accompanying with their structural changes (2013) Front Plant Sci, 4, p. 277
  • Couturier, J., Chibani, K., Jacquot, J.-P., Rouhier, N., Cysteine-based redox regulation and signaling in plants (2013) Front Plant Sci, 4, p. 105
  • Sweetlove, L.J., Heazlewood, J.L., Herald, V., Holtzapffel, R., Day, D.A., Leaver, C.J., Millar, A.H., The impact of oxidative stress on Arabidopsis mitochondria (2002) Plant J, 32, pp. 891-904
  • Baxter, C.J., Redestig, H., Schauer, N., Repsilber, D., Patil, K.R., Nielsen, J., Selbig, J., Sweetlove, L.J., The metabolic response of heterotrophic Arabidopsis cells to oxidative stress (2007) Plant Physiol, 143, pp. 312-325
  • Schmidtmann, E., König, A.-C., Orwat, A., Leister, D., Hartl, M., Finkemeier, I., Redox regulation of Arabidopsis mitochondrial citrate synthase (2014) Mol Plant, 7, pp. 156-169
  • Verniquet, F., Gaillard, J., Neuburger, M., Douce, R., Rapid inactivation of plant aconitase by hydrogen peroxide (1991) Biochem J, 276, pp. 643-648
  • Tretter, L., Adam-Vizi, V., Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of [alpha]-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress (2000) J Neurosci, 20, pp. 8972-8979
  • Araujo, W.L., Nunes-Nesi, A., Nikoloski, Z., Sweetlove, L.J., Fernie, A.R., Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues (2012) Plant Cell Environ, 35, pp. 1-21
  • Zhang, Y., Beard, K.F.M., Swart, C., Bergmann, S., Krahnert, I., Nikoloski, Z., Graf, A., Fernie, A.R., Protein-protein interactions and metabolite channelling in the plant tricarboxylic acid cycle (2017) Nat Commun, 8, p. 15212
  • Cavalcanti, J.H., Esteves-Ferreira, A.A., Quinhones, C.G., Pereira-Lima, I.A., Nunes-Nesi, A., Fernie, A.R., Araujo, W.L., Evolution and functional implications of the tricarboxylic acid cycle as revealed by phylogenetic analysis (2014) Genome Biol Evol, 6, pp. 2830-2848
  • Murat, F., Louis, A., Maumus, F., Armero, A., Cooke, R., Quesneville, H., Crollius, H.R., Salse, J., Understanding Brassicaceae evolution through ancestral genome reconstruction (2015) Genome Biol, 16, p. 262
  • Kagale, S., Robinson, S.J., Nixon, J., Xiao, R., Huebert, T., Condie, J., Kessler, D., Links, M.G., Polyploid evolution of the Brassicaceae during the Cenozoic era (2014) Plant Cell, 26, pp. 2777-2791
  • Wang, J., Marowsky, N.C., Fan, C., Divergent evolutionary and expression patterns between lineage specific new duplicate genes and their parental paralogs in Arabidopsis thaliana (2013) PLoS One, 8
  • Dyson, B.C., Miller, M.A.E., Feil, R., Rattray, N., Bowsher, C., Goodacre, R., Lunn, J.E., Johnson, G.N., FUM2, a cytosolic fumarase, is essential for acclimation to low temperature in Arabidopsis thaliana (2016) Plant Physiol, 172, pp. 118-127
  • Scott, I.M., Ward, J.L., Miller, S.J., Beale, M.H., Opposite variations in fumarate and malate dominate metabolic phenotypes of Arabidopsis salicylate mutants with abnormal biomass under chilling (2014) Physiol Plant, 152, pp. 660-674
  • Riewe, D., Jeon, H.J., Lisec, J., Heuermann, M.C., Schmeichel, J., Seyfarth, M., Meyer, R.C., Altmann, T., A naturally occurring promoter polymorphism of the Arabidopsis FUM2 gene causes expression variation, and is associated with metabolic and growth traits (2016) Plant J, 88, pp. 826-838
  • Kim, S.H., Lee, W.S., Participation of extracellular fumarase in the utilization of malate in cultured carrot cells (2002) Plant Cell Rep, 20, pp. 1087-1092
  • Pedersen, A.G., Nielsen, H., Neural network prediction of translation initiation sites in eukaryotes: perspectives for EST and genome analysis (1997) Proc Int Conf Intell Syst Mol Biol, 5, pp. 226-233
  • Claros, M.G., Vincens, P., Computational method to predict mitochondrially imported proteins and their targeting sequences (1996) Eur J Biochem, 241, pp. 779-786
  • Emanuelsson, O., Nielsen, H., Brunak, S., von Heijne, G., Predicting subcellular localization of proteins based on their N-terminal amino acid sequence (2000) J Mol Biol, 300, pp. 1005-1016
  • Petersen, T.N., Brunak, S., von Heijne, G., Nielsen, H., SignalP 4.0: discriminating signal peptides from transmembrane regions (2011) Nat Methods, 8, pp. 785-786
  • Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput (2004) Nucleic Acids Res, 32, pp. 1792-1797
  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Huelsenbeck, J.P., MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space (2012) Syst Biol, 61, pp. 539-542
  • Wang, J., Tao, F., Marowsky, N.C., Fan, C., Evolutionary fates and dynamic functionalization of young duplicate genes in arabidopsis genomes (2016) Plant Physiol, 172, pp. 427-440
  • Duarte, J.M., Wall, P.K., Edger, P.P., Landherr, L.L., Ma, H., Pires, J.C., Leebens-Mack, J., dePamphilis, C.W., Identification of shared single copy nuclear genes in Arabidopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels (2010) BMC Evol Biol, 10, p. 61
  • Han, F., Peng, Y., Xu, L., Xiao, P., Identification, characterization, and utilization of single copy genes in 29 angiosperm genomes (2014) BMC Genom, 15, p. 504
  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., MEGA6: molecular evolutionary genetics analysis version 6.0 (2013) Mol Biol Evol, 30, pp. 2725-2729
  • Detarsio, E., Wheeler, M.C., Campos Bermudez, V.A., Andreo, C.S., Drincovich, M.F., Maize C4 NADP-malic enzyme. Expression in Escherichia coli and characterization of site-directed mutants at the putative nucleoside-binding sites (2003) J Biol Chem, 278, pp. 13757-13764
  • Annett, R.G., Kosicki, G.W., ICeto-Enol tautomerase (1969) J Biol Chem, 244, pp. 2059-2067
  • Laemmly, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4 (1970) Nature, 227, pp. 680-685

Citas:

---------- APA ----------
Zubimendi, J.P., Martinatto, A., Valacco, M.P., Moreno, S., Andreo, C.S., Drincovich, M.F. & Tronconi, M.A. (2018) . The complex allosteric and redox regulation of the fumarate hydratase and malate dehydratase reactions of Arabidopsis thaliana Fumarase 1 and 2 gives clues for understanding the massive accumulation of fumarate. FEBS Journal, 285(12), 2205-2224.
http://dx.doi.org/10.1111/febs.14483
---------- CHICAGO ----------
Zubimendi, J.P., Martinatto, A., Valacco, M.P., Moreno, S., Andreo, C.S., Drincovich, M.F., et al. "The complex allosteric and redox regulation of the fumarate hydratase and malate dehydratase reactions of Arabidopsis thaliana Fumarase 1 and 2 gives clues for understanding the massive accumulation of fumarate" . FEBS Journal 285, no. 12 (2018) : 2205-2224.
http://dx.doi.org/10.1111/febs.14483
---------- MLA ----------
Zubimendi, J.P., Martinatto, A., Valacco, M.P., Moreno, S., Andreo, C.S., Drincovich, M.F., et al. "The complex allosteric and redox regulation of the fumarate hydratase and malate dehydratase reactions of Arabidopsis thaliana Fumarase 1 and 2 gives clues for understanding the massive accumulation of fumarate" . FEBS Journal, vol. 285, no. 12, 2018, pp. 2205-2224.
http://dx.doi.org/10.1111/febs.14483
---------- VANCOUVER ----------
Zubimendi, J.P., Martinatto, A., Valacco, M.P., Moreno, S., Andreo, C.S., Drincovich, M.F., et al. The complex allosteric and redox regulation of the fumarate hydratase and malate dehydratase reactions of Arabidopsis thaliana Fumarase 1 and 2 gives clues for understanding the massive accumulation of fumarate. FEBS J. 2018;285(12):2205-2224.
http://dx.doi.org/10.1111/febs.14483