Exploring the Arabidopsis sulfur metabolome

Plant Journal

Volumn 77, Issue 1, 2014, Pages 31-45

  Gläser, Katharina ^a   Kanawati, Basem ^b   Kubo, Tobias ^a   Schmitt Kopplin, Philippe ^b   Grill, Erwin ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

glutamyl transferase; Arabidopsis thaliana; GGT4; glutathione conjugates; ICR FTMS; isotope labeling; metabolomics

Indexed keywords

ARABIDOPSIS THALIANA; GGT4; GLUTATHIONES; ICR-FTMS; ISOTOPE LABELING; METABOLOMICS;

DETOXIFICATION; ISOTOPES; MASS SPECTROMETERS; PEPTIDES; SULFUR COMPOUNDS; SULFUR DETERMINATION;

SULFUR;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; GAMMA GLUTAMYLTRANSFERASE; GLUTATHIONE; SULFUR;

ARABIDOPSIS; CELL VACUOLE; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; GENETICS; ISOTOPE LABELING; MASS SPECTROMETRY; METABOLISM; METABOLOME; MUTATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CLUSTER ANALYSIS; GAMMA-GLUTAMYLTRANSFERASE; GENE EXPRESSION REGULATION, PLANT; GLUTATHIONE; ISOTOPE LABELING; MASS SPECTROMETRY; METABOLOME; MUTATION; SULFUR; VACUOLES;

EID: 84891016345     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12359     Document Type: Article

References (86)

1. Afendi, F.M., Okada, T., Yamazaki, M., et al. (2012) KNApSAcK family databases: integrated metabolite-plant species databases for multifaceted plant research. Plant Cell Physiol. 53, e1.
2. Agerbirk, N., and, Olsen, C.E., (2012) Glucosinolate structures in evolution. Phytochemistry, 77, 16-45.
3. Allwood, J.W., Parker, D., Beckmann, M., Draper, J., and, Goodacre, R., (2012) Fourier transform ion cyclotron resonance mass spectrometry for plant metabolite profiling and metabolite identification. Methods Mol. Biol. 860, 157-176.
4. Altman, T., Travers, M., Kothari, A., Caspi, R., and, Karp, P.D., (2013) A systematic comparison of the MetaCyc and KEGG pathway databases. BMC Bioinformatics, 40, 112.
5. Beck, A., Lendzian, K.J., Oven, M., Christmann, A., and, Grill, E., (2003) Phytochelatin synthase catalyzes key step in turnover of glutathione conjugates. Phytochemistry, 62, 423-431.
6. Bednarek, P., Piślewska-Bednarek, M., Ver Loren van Themaat, E., Maddula, R.K., Svatoš, A., and, Schulze-Lefert, P., (2011) Conservation and clade-specific diversification of pathogen-inducible tryptophan and indole glucosinolate metabolism in Arabidopsis thaliana relatives. New Phytol. 132, 713-726.
7. Blake-Kalff, M.M.A., Harrison, K.R., Hawkesford, M.J., Zhao, F.J., and, McGrath, S.P., (1998) Distribution of sulfur within oilseed rape leaves in response to sulfur deficiency during vegetative growth. Plant Physiol. 118, 1337-1344.
8. Blum, R., Beck, A., Korte, A., Stengel, A., Letzel, T., Lendzian, K.J., and, Grill, E., (2007) Function of phytochelatin synthase in catabolism of glutathione-conjugates. Plant J. 49, 740-749.
9. Blum, R., Meyer, K.C., Wünschmann, J., Lendzian, K.J., and, Grill, E., (2010) Cytosolic action of phytochelatin synthase. Plant Physiol. 153, 159-169.
10. Böttcher, C., Westphal, L., Schmotz, C., Prade, E., Scheel, D., and, Glawischnig, E., (2009) The multifunctional enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of Arabidopsis thaliana. Plant Cell, 21, 1830-1845.
11. Brown, P.D., Tokuhisa, J.G., Reichelt, M., and, Gershenzon, J., (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry, 62, 471-481.
12. 2S and pedospheric sulfate nutrition. Plant Physiol. 136, 3396-3408.
13. Creek, D.J., Chokkathukalam, A., Jankevics, A., Burgess, K.E.V., Breitling, R., and, Barrett, M.P., (2012) Stable isotope-assisted metabolomics for network-wide metabolic pathway elucidation. Anal. Chem. 84, 8442-8447.
14. Cummins, I., Dixon, D.P., Freitag-Pohl, S., Skipsey, M., and, Edwards, R., (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab. Rev. 43, 266-280.
15. Davoine, C., Falletti, O., Douki, T., Iacazio, G., Ennar, N., Montillet, J.-L., and, Triantaphylidès, C., (2006) Adducts of oxylipin electrophiles to glutathione reflect a 13 specificity of the downstream lipoxygenase pathway in the tobacco hypersensitive response. Plant Physiol. 140, 1484-1493.
16. Destro, T., Prasad, D., Martignago, D., Bernet, I.L., Trentin, A.R., Renu, I.K., Ferretti, M., and, Masi, A., (2011) Compensatory expression and substrate inducibility of gamma-glutamyl transferase GGT2 isoform in Arabidopsis thaliana. J. Exp. Bot. 62, 805-814.
17. Dixon, D.P., and, Edwards, R., (2009) Selective binding of glutathione conjugates of fatty acid derivatives by plant glutathione transferases. J. Biol. Chem. 284, 21249-21256.
18. Dixon, D.P., Skipsey, M., and, Edwards, R., (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry, 71, 338-350.
19. Draper, J., Enot, D.P., Parker, D., Beckmann, M., Snowdon, S., Lin, W., and, Zubair, H., (2009) Metabolite signal identification in accurate mass metabolomics data with MZedDB, an interactive m/z annotation tool utilising predicted ionisation behaviour 'rules'. BMC Bioinformatics, 10, 227.
20. Edwards, R., and, Dixon, D.P., (2005) Plant glutathione transferases. Methods Enzymol. 401, 169-186.
21. Fahey, J.W., Zalcmann, A.T., and, Talalay, P., (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry, 56, 5-51.
22. Geu-Flores, F., Nielsen, M.T., Nafisi, M., Møldrup, M.E., Olsen, C.E., Motawia, M.S., and, Halkier, B.A., (2009) Glucosinolate engineering identifies a γ-glutamyl peptidase. Nat. Chem. Biol. 5, 575-577.
23. Geu-Flores, F., Møldrup, M.E., Böttcher, C., Olsen, C.E., Scheel, D., and, Halkier, B.A., (2011) Cytosolic γ-glutamyl peptidases process glutathione conjugates in the biosynthesis of glucosinolates and camalexin in Arabidopsis. Plant Cell, 23, 2456-2469.
24. 13C metabolome isotope labeling allows unambiguous assignment of chemical sum formulas. Anal. Chem. 80, 9417-9425.
25. 34S isotope labelling, in combination with high-resolution mass spectrometry. Plant J. 68, 364-376.
26. Glazebrook, J., and, Ausubel, F.M., (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc. Natl Acad. Sci. USA, 91, 8955-8959.
27. Grzam, A., Martin, M.N., Hell, R., and, Meyer, A.J., (2007) Γ-Glutamyl transpeptidase GGT4 initiates vacuolar degradation of glutathione S-conjugates in Arabidopsis. FEBS Lett. 581, 3131-3138.
28. Halkier, B.A., and, Gershenzon, J., (2006) Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303-333.
29. Hegeman, A.D., Schulte, C.F., Cui, Q., Lewis, I.A., Huttlin, E.L., Eghbalnia, H., Harms, A.C., Ulrich, E.L., Markley, J.L., and, Sussman, M.R., (2007) Stable isotope assisted assignment of elemental compositions for metabolomics. Anal. Chem. 79, 6912-6921.
30. Hell, R., and, Wirtz, M., (2011) Molecular biology, biochemistry and cellular physiology of cysteine metabolism in Arabidopsis thaliana. Arabidopsis Book, 9, e0154.
31. Hertkorn, N., Frommberger, M., Witt, M., Koch, B.P., Schmitt-Kopplin, P., and, Perdue, E.M., (2008) Natural organic matter and the event horizon of mass spectrometry. Anal. Chem. 80, 8908-8919.
32. Herzsprung, P., Hertkorn, N., Friese, K., and, Schmitt-Kopplin, P., (2010) Photochemical degradation of natural organic sulfur compounds (CHOS) from iron-rich mine pit lake pore waters-an initial understanding from evaluation of single-elemental formulae using ultra-high-resolution mass spectrometry. Rapid Commun. Mass Spectrom. 24, 2909-2924.
33. Hesse, H., Kreft, O., Maimann, S., Zeh, M., and, Hoefgen, R., (2004) Current understanding of the regulation of methionine biosynthesis in plants. J. Exp. Bot. 55, 1799-1808.
34. Hirai, M.Y., Yano, M., Goodenowe, D.B., Kanaya, S., Kimura, T., Awazuhara, M., Arita, M., Fujiwara, T., and, Saito, K., (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 101, 10205-10210.
35. 34S-metabolic labelling. Phytochem. Anal. 23, 324-331.
36. Iijima, Y., Nakamura, Y., Ogata, Y., et al. (2008) Metabolite annotations based on the integration of mass spectral information. Plant J. 54, 949-962.
37. Janz, D., Behnke, K., Schnitzler, J.-P., Kanawati, B., Schmitt-Kopplin, P., and, Polle, A., (2010) Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Biol. 10, 150.
38. Joosen, R.V., Arends, D., Li, Y., Willems, L.A., Keurentjes, J.J., Ligterink, W., Jansen, R.C., and, Hilhorst, H.W., (2013) Identifying genotype-by-environment interactions in the metabolism of germinating Arabidopsis seeds using generalized genetical genomics. Plant Physiol. 162, 553-566.
39. Kanawati, B., von Saint Paul, V., Herrmann, C., Schäffner, A.R., and, Schmitt-Kopplin, P., (2011) Mass spectrometric stereoisomeric differentiation between α- and β-ascorbic acid 2-O-glucosides. Experimental and density functional theory study. Rapid Commun. Mass Spectrom. 25, 806-814.
40. Kind, T., and, Fiehn, O., (2006) Metabolomic database annotations via query of elemental compositions: mass accuracy is insufficient even at less than 1 ppm. BMC Bioinformatics, 7, 234.
41. Kind, T., and, Fiehn, O., (2007) Seven golden rules for heuristic filtering of molecular formulas obtained by accurate mass spectrometry. BMC Bioinformatics, 8, 105.
42. Kopriva, S., Mugford, S.G., Matthewman, C., and, Koprivova, A., (2009) Plant sulfate assimilation genes: redundancy versus specialization. Plant Cell Rep. 28, 1769-1780.
43. Krajewski, M.P., Kanawati, B., Fekete, A., Kowalski, N., Schmitt-Kopplin, P., and, Grill, E., (2013) Analysis of Arabidopsis glutathione-transferases in yeast. Phytochemistry, 91, 198-207.
44. Kruve, A., Kaupmees, K., Liigand, J., Oss, M., and, Leito, I., (2013) Sodium adduct formation efficiency in ESI source. J. Mass Spectrom. 48, 695-702.
45. Lee, B.-R., Huseby, S., Koprivova, A., et al. (2012) Effects of fou8/fry1 mutation on sulfur metabolism: is decreased internal sulfate the trigger of sulfate starvation response? PLoS One, 7, e39425.
46. Li, X., Fekete, A., Englmann, M., Frommberger, M., Lv, S., Chen, G., and, Schmitt-Kopplin, P., (2007) At-line coupling of UPLC to chip-electrospray- FTICR-MS. Anal. Bioanal. Chem. 389, 1439-1446.
47. Liao, S., Ewing, N.P., Boucher, B., Materne, O., and, Brummel, C.L., (2012) High-throughput screening for glutathione conjugates using stable-isotope labeling and negative electrospray ionization precursor-ion mass spectrometry. Rapid Commun. Mass Spectrom. 26, 659-669.
48. Martin, M.N., Saladores, P.H., Lambert, E., Hudson, A.O., and, Leustek, T., (2007) Localization of members of the γ-glutamyl transpeptidase family identifies sites of glutathione and glutathione S-conjugate hydrolysis. Plant Physiol. 114, 1715-1732.
49. Maruyama-Nakashita, A., Inoue, E., Watanabe-Takahashi, A., Yamaya, T., and, Takahashi, H., (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol. 132, 597-605.
50. Matsuda, F., Shinbo, Y., Oikawa, A., Hirai, M.Y., Fiehn, O., Kanaya, S., Saito, K., and, El-Shemy, H.A., (2009) Assessment of metabolome annotation quality: a method for evaluating the false discovery rate of elemental composition searches. PLoS One, 4, e7490.
51. May, M.J., and, Leaver, C.J., (1993) Oxidative stimulation of glutathione synthesis in arabidopsis thaliana suspension cultures. Plant Physiol. 103, 621-627.
52. Mugford, S.G., Yoshimoto, N., Reichelt, M., et al. (2009) Disruption of adenosine-5′-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell, 21, 910-927.
53. Mugford, S.G., Lee, B.-R., Koprivova, A., Matthewman, C., and, Kopriva, S., (2011) Control of sulfur partitioning between primary and secondary metabolism. Plant J. 65, 96-105.
54. Nakabayashi, R., and, Saito, K., (2013) Metabolomics for unknown plant metabolites. Anal. Bioanal. Chem. 405, 5005-5011.
55. 13C- labeling for chemical assignment of sulfur-containing metabolites in onion bulbs. Anal. Chem. 85, 1310-1315.
56. Nikiforova, V.J., Gakière, B., Kempa, S., Adamik, M., Willmitzer, L., Hesse, H., and, Hoefgen, R., (2004) Towards dissecting nutrient metabolism in plants: a systems biology case study on sulphur metabolism. J. Exp. Bot. 55, 1861-1870.
57. Nikiforova, V.J., Kopka, J., Tolstikov, V., Fiehn, O., Hopkins, L., Hawkesford, M.J., Hesse, H., and, Hoefgen, R., (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol. 138, 304-318.
58. Noctor, G., Queval, G., Mhamdi, A., Chaouch, S., and, Foyer, C.H., (2011) Glutathione. Arabidopsis Book, 9, e0142.
59. Ohkama-Ohtsu, N., Radwan, S., Peterson, A., Zhao, P., Badr, A.F., Xiang, C., and, Oliver, D.J., (2007a) Characterization of the extracellular γ-glutamyl transpeptidases, GGT1 and GGT2, in Arabidopsis. Plant J. 49, 865-877.
60. Ohkama-Ohtsu, N., Zhao, P., Xiang, C., and, Oliver, D.J., (2007b) Glutathione conjugates in the vacuole are degraded by γ-glutamyl transpeptidase GGT3 in Arabidopsis. Plant J. 49, 878-888.
61. Ohkama-Ohtsu, N., Oikawa, A., Zhao, P., Xiang, C., Saito, K., and, Oliver, D.J., (2008) A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol. 148, 1603-1613.
62. Ohkama-Ohtsu, N., Sasaki-Sekimoto, Y., Oikawa, A., et al. (2011) 12-oxo-phytodienoic acid-glutathione conjugate is transported into the vacuole in Arabidopsis. Plant Cell Physiol. 52, 205-209.
63. Ohta, D., Kanaya, S., and, Suzuki, H., (2010) Application of Fourier-transform ion cyclotron resonance mass spectrometry to metabolic profiling and metabolite identification. Curr. Opin. Biotechnol. 21, 35-44.
64. Omranian, N., Mueller-Roeber, B., and, Nikoloski, Z., (2012) PageRank-based identification of signaling crosstalk from transcriptomics data: the case of Arabidopsis thaliana. Mol. BioSyst. 8, 1121-1127.
65. Öztetik, E., (2008) A tale of plant glutathione S-transferases: since 1970. Bot. Rev. 74, 419-437.
66. Payne, T.G., Southam, A.D., Arvanitis, T.N., and, Viant, M.R., (2009) A signal filtering method for improved quantification and noise discrimination in Fourier transform ion cyclotron resonance mass spectrometry-based metabolomics data. J. Am. Soc. Mass Spectrom. 20, 1087-1095.
67. Petersen, B.L., Chen, S., Hansen, C.H., Olsen, C.E., and, Halkier, B.A., (2002) Composition and content of glucosinolates in developing Arabidopsis thaliana. Planta, 214, 562-571.
68. Ravilious, G.E., and, Jez, J.M., (2012) Structural biology of plant sulfur metabolism: from assimilation to biosynthesis. Nat. Prod. Rep. 29, 1138-1152.
69. von Saint Paul, V., Zhang, W., Kanawati, B., Geist, B., Faus-Kessler, T., Schmitt-Kopplin, P., and, Schäffner, A.R., (2011) The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell, 23, 4124-4145.
70. Saito, K., and, Matsuda, F., (2010) Metabolomics for functional genomics, systems biology, and biotechnology. Annu. Rev. Plant Biol. 61, 463-489.
71. Sauter, M., Cornell, K.A., Beszteri, S., and, Rzewuski, G., (2004) Functional analysis of methylthioribose kinase genes in plants. Plant Physiol. 136, 4061-4071.
72. Schmid, D.G., Grosche, P., Bandel, H., and, Jung, G., (2000) FTICR-mass spectrometry for high-resolution analysis in combinatorial chemistry. Biotechnol. Bioeng. 71, 149-161.
73. Schütz, W., Hausmann, N., Krug, K., Hampp, R., and, Macek, B., (2011) Extending SILAC to proteomics of plant cell lines. Plant Cell, 23, 1701-1705.
74. Shinbo, Y., Nakamura, Y., Altaf-Ul-Amin, M., Asahi, H., Kurokawa, K., Arita, M., Saito, K., Ohta, D., Shibata, D., and, Kanaya, S., (2006) KNApSAcK: a comprehensive species-metabolite relationship database. Biotechnol. Agric. For. 57, 165-181.
75. Singh, R., White, M.A., Ramana, K.V., Petrash, J.M., Watowich, S.J., Bhatnagar, A., and, Srivastava, S.K., (2006) Structure of a glutathione conjugate bound to the active site of aldose reductase. Proteins, 64, 101-110.
76. Smith, R., (2000) Evolution of ESI-mass spectrometry and Fourier transform ion cyclotron resonance for proteomics and other biological applications. Int. J. Mass Spectrom. 200, 509-544.
77. Sønderby, I.E., Geu-Flores, F., and, Halkier, B.A., (2010) Biosynthesis of glucosinolates-gene discovery and beyond. Trends Plant Sci. 15, 283-290.
78. Sousa Silva, M., Gomes, R.A., Ferreira, A.E.N., Ponces Freire, A., and, Cordeiro, C., (2013) The glyoxalase pathway: the first hundred years. and beyond. Biochem. J. 453, 1-15.
79. Stewart, B.J., Navid, A., Kulp, K.S., Knaack, J.L.S., and, Bench, G., (2013) d -Lactate production as a function of glucose metabolism in Saccharomyces cerevisiae. Yeast, 30, 81-91.
80. Storozhenko, S., Belles-Boix, E., Babiychuk, E., Hérouart, D., Davey, M.W., Slooten, L., van Montagu, M., Inzé, D., and, Kushnir, S., (2002) γ-glutamyl transpeptidase in transgenic tobacco plants. Cellular localization, processing, and biochemical properties. Plant Physiol. 128, 1109-1119.
81. Tate, S.S., and, Meister, A., (1985) γ-Glutamyl transpeptidase from kidney. Methods Enzymol. 113, 400-419.
82. Tsuboi, S., Kobayashi, M., Nanba, M., Imaoka, S., and, Ohmori, S., (1990) S-(1,2-dicarboxyethyl)glutathione and activity for its synthesis in rat tissues. J. Biochem. 107, 539-545.
83. Tsuboi, S., Fujiwara, E., Ogata, K., Sakaue, A., Nakayama, T., and, Ohmori, S., (1993) Inhibitory effects of S-(1,2-dicarboxyethyl)glutathione on collagen-induced platelet aggregation; enhancements of cyclic AMP level and adenylate cyclase activity in platelets by S-(1,2-dicarboxyethyl)glutathione. Biol. Pharm. Bull. 16, 1083-1086.
84. Walker, S.H., Budhathoki-Uprety, J., Novak, B.M., and, Muddiman, D.C., (2011) Stable-isotope labeled hydrophobic hydrazide reagents for the relative quantification of N-linked glycans by electrospray ionization mass spectrometry. Anal. Chem. 83, 6738-6745.
85. Yoshimoto, N., Inoue, E., Saito, K., Yamaya, T., and, Takahashi, H., (2003) Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol. 131, 1511-1517.
86. Zhao, F.J., Hawkesford, M.J., and, McGrath, S.P., (1999) Sulphur assimilation and effects on yield and quality of wheat. J. Cereal Sci. 30, 1-17.