Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana

Plant Cell

Volumn 22, Issue 4, 2010, Pages 1216-1231

  Khan, Muhammad Sayyar ^a   Haas, Florian Heinrich ^a   Samami, Arman Allboje ^a   Gholami, Amin Moghaddas ^b   Bauer, Andrea ^b   Fellenberg, Kurt ^c   Reichelt, Michael ^d   Hänsch, Robert ^e   Mendel, Ralf R ^e   Meyer, Andreas J ^a   Wirtz, Markus ^a   Hell, Rüdiger ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^e TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77953190149     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.074088     Document Type: Article

References (78)

1. 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.
2. Benning, C. (2007). Questions remaining in sulfolipid biosynthesis: A historical perspective. Photosynth. Res. 92: 199-203.
3. Blake-Kalff, M.M., 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.
4. Bork, C., Schwenn, J.D., and Hell, R. (1998). Isolation and character-ization of a gene for assimilatory sulfite reductase from Arabidopsis thaliana. Gene 212: 147-153.
5. Bradford, M.M. (1976). A rapid and sensitive method for the quantita-tion of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
6. Brown, P., Tokuhisa, J., Reichelt, M., and Gershenzon, J. (2003). Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62: 471-481.
7. Brychkova, G., Xia, Z., Yang, G., Yesbergenova, Z., Zhang, Z., Davydov, O., Fluhr, R., and Sagi, M. (2007). Sulfite oxidase protects plants against sulfur dioxide toxicity. Plant J. 50: 696-709.
8. Cairns, N.G., Pasternak, M., Wachter, A., Cobbett, C.S., and Meyer, A.J. (2006). Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol. 141: 446-455.
9. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
10. Cobbett, C.S., May, M.J., Howden, R., and Rolls, B. (1998). The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabi-dopsis thaliana is deficient in g-glutamylcysteine synthetase. Plant J. 16: 73-78.
11. Crane, B.R., Siegel, L.M., and Getzoff, E.D. (1995). Sulfite reductase structure at 1.6 A: Evolution and catalysis for reduction of inorganic anions. Science 270: 59-67.
12. Edwards, K., Johnstone, C., and Thompson, C. (1991). A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 19: 1349
13. Eilers, T., Schwarz, G., Brinkmann, H., Witt, C., Richter, T., Nieder, J., Koch, B., Hille, R., Hansch, R., and Mendel, R.R. (2001). Identification and biochemical characterization of Arabidopsis thaliana sulfite oxidase. A new player in plant sulfur metabolism. J. Biol. Chem. 276: 46989-46994.
14. Fell, D., and Thomas, S. (1995). Physiological control of metabolic flux: The requirement for multisite modulation. Biochem. J. 311: 35-39.
15. Fellenberg, K., Hauser, N.C., Brors, B., Neutzner, A., Hoheisel, J.D., and Vingron, M. (2001). Correspondence analysis applied to micro-array data. Proc. Natl. Acad. Sci. USA 98: 10781-10786.
16. Fujiwara, T., Nambara, E., Yamagishi, K., Goto, D.B., and Naito, S. (2002). Storage proteins. In The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Rockville, MD: American Society of Plant Biologists), doi/10.1199/tab.0020, http://www.aspb.org/publications/arabidopsis/
17. Furihata, T., Pomprasirt, S., and Sakurai, H. (1997). Characteristics of sulfite transport by Chlorella vulgaris. Plant Cell Physiol. 38: 398-403.
18. Gardner, M.J., and Osmond, C. (1984). Interpretation of time trends in disease rates in the presence of generation effects. Stat. Med. 3: 113-130.
19. Ha, S.-B., Smith, A.P., Howden, R., Dietrich, W.M., Bugg, S., O'Connell, M.J., Goldsbrough, P.B., and Cobbett, C.S. (1999). Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11: 1153-1164.
20. Haas, F.H., Heeg, C., Queiroz, R., Bauer, A., Wirtz, M., and Hell, R. (2008). Mitochondrial serine acetyltransferase functions as a pace-maker of cysteine synthesis in plant cells. Plant Physiol. 148: 1055-1067.
21. Hänsch, R., Lang, C., Rennenberg, H., and Mendel, R.R. (2007). Significance of plant sulfite oxidase. Plant Biol. (Stuttg.) 9: 589-595.
22. Hänsch, R., and Mendel, R. (2005). Sulfite oxidation in plant perox-isomes. Photosynth. Res. 86: 337-342.
23. Haughn, G.W., and Somerville, C. (1986). Sulfonylurea-resistant mu-tants of Arabidopsis thaliana. Mol. Gen. Genet. 204: 430-434.
24. Hawkesford, M.J. (2008). Uptake, distribution and subcellular transport of sulfate. In Sulfur Metabolism in Phototrophic Prganisms, R. Hell, C. Dahl, and T. Leustek, eds (Dordrecht, The Netherlands: Springer), pp. 17-32.
25. Heeg, C., Kruse, C., Jost, R., Gutensohn, M., Ruppert, T., Wirtz, M., and Hell, R. (2008). Analysis of the Arabidopsis O-acetylserine(thiol) lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. Plant Cell 20: 168-185.
26. Hell, R., and Wirtz, M. (2008). Metabolism of cysteine in plants and phototrophic bacteria. In Sulfur Metabolism in Phototrophic Orga-nisms, R. Hell, C. Dahl, and T. Leustek, eds (Dordrecht, The Nether-lands: Springer), pp. 61-94.
27. Henkes, S., Sonnewald, U., Badur, R., Flachmann, R., and Stitt, M. (2001). A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell 13: 535-551.
28. Hirai, M.Y., et al. (2005). Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J. Biol. Chem. 280: 25590-25595.
29. Hirai, M.Y., et al. (2007). Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl. Acad. Sci. USA 104: 6478-6483.
30. Höfgen, R., and Nikiforova, V.J. (2008). Metabolomics integrated with transcriptomics: Assessing systems response to sulfur-deficiency stress. Physiol. Plant. 132: 190-198.
31. Hothorn, M., Wachter, A., Gromes, R., Stuwe, T., Rausch, T., and Scheffzek, K. (2006). Structural basis for the redox control of plant glutamate cysteine ligase. J. Biol. Chem. 281: 27557-27565.
32. Houba, V.J.G., and Uittenbogaard, J. (1994). International plant- analytical exchange (IPE). In Chemical Composition of Various Plant Species, V.J.G. Houba and J. Uittenbogaard, eds (Wageningen, The Netherlands: Wageningen Agricultural University), pp. 8-219.
33. Jez, J.M., Cahoon, R.E., and Chen, S. (2004). Arabidopsis thaliana glutamate-cysteine ligase: functional properties, kinetic mechanism, and regulation of activity. J. Biol. Chem. 279: 33463-33470.
34. Kopriva, S. (2006). Regulation of sulfate assimilation in Arabidopsis and beyond. Ann. Bot. (Lond.) 97: 479-495.
35. Kopriva, S., Muheim, R., Koprivova, A., Trachsel, N., Catalano, C. Suter, M., and Brunold, C. (1999). Light regulation of assimilatory sulphate reduction in Arabidopsis thaliana. Plant J. 20: 37-44.
36. Koprivova, A., Suter, M., den Camp, R.O., Brunold, C., and Kopriva, S. (2000). Regulation of sulfate assimilation by nitrogen in Arabidop-sis. Plant Physiol. 122: 737-746.
37. Krueger, S., Niehl, A., Lopez Martin, M., Steinhauser, D., Donath, A., Hildebrandt, T., Romero, L., Hoefgen, R., Gotor, C., and Hesse, H. (2009). Analysis of cytosolic and plastidic serine acetyltransferase mutants and subcellular metabolite distributions suggests interplay of the cellular compartments for cysteine biosynthesis in Arabidopsis. Plant Cell Environ. 32: 349-367.
38. 4 interaction in spinach ferredoxin-sulfite reductase. Biochemistry 21: 2905-2909.
39. Kruse, C., Jost, R., Lipschis, M., Kopp, B., Hartmann, M., and Hell, R. (2007). Sulfur-enhanced defence: Effects of sulfur metabolism, nitrogen supply, and pathogen lifestyle. Plant Biol. 9: 608-619.
40. Laemmli, U.K. (1970). Cleavage of structural proteins during the as-sembly of the head of bacteriophage T4. Nature 227: 680-685.
41. Lang, C., Popko, J., Wirtz, M., Hell, R., Herschbach, C., Kreuzwieser, J., Rennenberg, H., Mendel, R., and Hänsch, R. (2007). Sulphite oxidase as key enzyme for protecting plants against sulphur dioxide. Plant Cell Environ. 30: 447-455.
42. Leustek, T. (2002). Sulfate metabolism. In The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Rockville, MD: American Society of Plant Biologists), doi/10.1199/tab.0017, http://www.aspb.org/publications/arabidopsis/
43. Leustek, T., Martin, M.N., Bick, J.-A., and Davies, J.P. (2000). Pathways and regulation of sulfur metabolism revealed through mo-lecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 141-165.
44. Liu, Y., Ahn, J.-E., Datta, S., Salzman, R.A., Moon, J., Huyghues-Despointes, B., Pittendrigh, B., Murdock, L.L., Koiwa, H., and Zhu-Salzman, K. (2005). Arabidopsis vegetative storage protein is an anti-insect acid phosphatase. Plant Physiol. 139: 1545-1556.
45. Loudet, O., Saliba-Colombani, V., Camilleri, C., Calenge, F., Gaudon, V., Koprivova, A., North, K., Kopriva, S., and Daniel-Vedele, F. (2007). Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat. Genet. 39: 896-900.
46. Martin, M.N., Tarczynski, M.C., Shen, B., and Leustek, T. (2005). The role of 59-adenylylsulfate reductase in controlling sulfate reduction in plants. Photosynth. Res. 86: 1-15.
47. Meyer, A. (2008). The integration of glutathione homeostasis and redox signaling. J. Plant Physiol. 165: 1390-1403.
48. Meyer, A.J., and Hell, R. (2005). Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth. Res. 86: 435-457.
49. Miseta, A., and Csutora, P. (2000). Relationship between the occur-rence of cysteine in proteins and the complexity of organisms. Mol. Biol. Evol. 17: 1232-1239.
50. Mugford, S.G., et al. (2009). Disruption of adenosine-59-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabo-lites. Plant Cell 21: 910-927.
51. Nakayama, M., Akashi, T., and Hase, T. (2000). Plant sulfite reductase: Molecular structure, catalytic function and interaction with ferredoxin. J. Inorg. Biochem. 82: 27-32.
52. Nakamura, K., Hayama, A., Masada, M., Fukushima, K., and Tamura, G. (1987). Measurement of serine acetyltransferase activity in crude plant extracts by a coupled assay system using cysteine synthase. Plant Cell Physiol. 28: 885-891.
53. 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.
54. Pasternak, M., Lim, B., Wirtz, M., Hell, R., Cobbett, C.S., and Meyer, A.J. (2008). Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J. 53: 999-1012.
55. Patron, N.J., Durnford, D.G., and Kopriva, S. (2008). Sulfate assim-ilation in eukaryotes: Fusions, relocations and lateral transfers. BMC Evol. Biol. 8: 39
56. Pe'er, I., Felder, C., Man, O., Silman, I., Sussman, J., and Beckmann, J. (2004). Proteomic signatures: Amino acid and oligopeptide com-positions differentiate among phyla. Proteins 54: 20-40.
57. Rotte, C., and Leustek, T. (2000). Differential subcellular localization and expression of ATP sulfurylase and 59-adenylylsulfate reductase during ontogenesis of Arabidopsis leaves indicates that cytosolic and plastid forms of ATP sulfurylase may have specialized functions. Plant Physiol. 124: 715-724.
58. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press). Schmidt, A., and Jäger, K. (1992). Open questions about sulfur metabolism in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 325-349.
59. Sirko, A., Blaszczyk, A., and Liszewska, F. (2004). Overproduction of SAT and/or OASTL in transgenic plants: A survey of effects. J. Exp. Bot. 55: 1881-1888.
60. Smith, A.M., and Zeeman, S.C. (2006). Quantification of starch in plant tissues. Nat. Protoc. 1: 1342-1345.
61. Smith, F.W., Hawkesford, M.J., Ealing, P.M., Clarkson, D.T., Vanden Berg, P.J., Belcher, A.R., and Warrilow, A.G. (1997). Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J. 12: 875-884.
62. Smyth, G.K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3: Article3
63. Stitt, M., and Sonnewald, U. (1995). Regulation of metabolism in transgenic plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 341-368.
64. Swamy, U., Wang, M., Tripathy, J., Kim, S., Hirasawa, M., Knaff, D., and Allen, J. (2005). Structure of spinach nitrite reductase: implications for multi-electron reactions by the iron-sulfur: siroheme cofactor. Biochemstry 44: 16054-16063.
65. Takahashi, H., and Saito, K. (2008). Molecular biology and functional genomics for identification of regulatory networks of plant sulfate uptake and assimilatory metabolism. In Sulfur Metabolism in Photo- trophic Organisms, R. Hell, C. Dahl, and T. Leustek, eds (Dordrecht, The Netherlands: Springer), pp. 151-164.
66. Takahashi, H., Watanabe-Takahashi, A., Smith, F.W., Blake-Kalff, M., Hawkesford, M.J., and Saito, K. (2000). The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J. 23: 171-182.
67. Tocquin, P., Corbesier, L., Havelange, A., Pieltain, A., Kurtem, E., Bernier, G., and Perilleux, C. (2003). A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flower-ing of Arabidopsis thaliana. BMC Plant Biol. 3: 2
68. Tsakraklides, G., Martin, M., Chalam, R., Tarczynski, M.C., Schmidt, A., and Leustek, T. (2002). Sulfate reduction is increased in trans-genic Arabidopsis thaliana expressing 59-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J. 32: 879-889.
69. Vauclare, P., Kopriva, S., Fell, D., Suter, M., Sticher, L., von Ballmoos, P., Krahenbuhl, U., den Camp, R.O., and Brunold, C. (2002). Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 59-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J. 31: 729-740.
70. Vernoux, T., Wilson, R.C., Seeley, K.A., Reichheld, J.P., Muroy, S., Brown, S., Maughan, S.C., Cobbett, C.S., Van Montagu, M., Inze, D., May, M.J., and Sung, Z.R. (2000). The ROOT MERISTEMLESS1/ CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12: 97-110.
71. Watanabe, M., Kusano, M., Oikawa, A., Fukushima, A., Noji, M., and Saito, K. (2008a). Physiological roles of the b-substituted alanine synthase gene family in Arabidopsis. Plant Physiol. 146: 310-320.
72. Watanabe, M., Mochida, K., Kato, T., Tabata, S., Yoshimoto, N., Noji, M., and Saito, K. (2008b). Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyl-transferase gene family in Arabidopsis. Plant Cell 20: 2484-2496.
73. Wirtz, M., Droux, M., and Hell, R. (2004). O-acetylserine (thiol) lyase: An enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J. Exp. Bot. 55: 1785-1798.
74. Wirtz, M., and Hell, R. (2003). Production of cysteine for bacterial and plant biotechnology: Application of cysteine feedback-insensitive isoforms of serine acetyltransferase. Amino Acids 24: 195-203.
75. Wirtz, M., and Hell, R. (2006). Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J. Plant Physiol. 163: 273-286.
76. Wirtz, M., and Hell, R. (2007). Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19: 625-639.
77. Yonekura-Sakakibara, K., Onda, Y., Ashikari, T., Tanaka, Y., Kusumi, T., and Hase, T. (2000). Analysis of reductant supply sys-tems for ferredoxin-dependent sulfite reductase in photosynthetic and nonphotosynthetic organs of maize. Plant Physiol. 122: 887-894.
78. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136: 2621-2632.