Structure and mechanism of soybean ATP sulfurylase and the committed step in plant sulfur assimilation

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10919-10929

  Herrmann, Jonathan ^a   Ravilious, Geoffrey E ^a   McKinney, Samuel E ^a   Westfall, Corey S ^a   Lee, Soon Goo ^a   Baraniecka, Patrycja ^b   Giovannetti, Marco ^b,c   Kopriva, Stanislav ^b   Krishnan, Hari B ^d   Jez, Joseph M ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b JOHN INNES CENTRE   (United Kingdom)

^c UNIVERSITY OF TURIN   (Italy)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYSIS; INTERFACES (MATERIALS); MAMMALS; SULFUR; SULFUR COMPOUNDS; SYNTHESIS (CHEMICAL);

ENERGETIC BARRIERS; ENVIRONMENTAL STRESS; NUCLEOPHILIC ATTACK; NUCLEOTIDE STRUCTURE; REACTION MECHANISM; STEADY-STATE KINETICS; TRANSITION STATE STABILIZATION; X RAY CRYSTAL STRUCTURES;

NITROGEN FIXATION;

ADENOSINE 3' PHOSPHATE 5' PHOSPHOSULFATE; ADENOSINE 5' PHOSPHOSULFATE; ARGININE; ASPARAGINE; HISTIDINE; ISOENZYME; SULFATE; SULFATE ADENYLYLTRANSFERASE; SULFUR;

ARABIDOPSIS; ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ENZYME SYNTHESIS; GENE MAPPING; GENE MUTATION; MEMBRANE STABILIZATION; NONHUMAN; NUCLEOPHILICITY; NUCLEOTIDE SEQUENCE; PLANT METABOLISM; PRIORITY JOURNAL; PROTEIN MOTIF; SOYBEAN; STEADY STATE; X RAY CRYSTALLOGRAPHY;

ENZYME MECHANISMS; ENZYME STRUCTURE; PLANT; PLANT BIOCHEMISTRY; PROTEIN STRUCTURE;

ADENOSINE PHOSPHOSULFATE; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ARABIDOPSIS; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HAPLOTYPES; HYDROGEN BONDING; KINETICS; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SOYBEANS; SUBSTRATE SPECIFICITY; SULFATE ADENYLYLTRANSFERASE; SULFUR;

EID: 84898668026     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.540401     Document Type: Article

References (69)

1. Leustek, T., Martin, M. N., Bick, J. A., and Davies, J. P. (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 141-165
2. Krishnan, H. B. (2005) Engineering soybean for enhanced sulfur amino acid content. Crop Sci. 45, 454-461
3. Patron, N. J., Durnford, D. G., and Kopriva, S. (2008) Sulfate assimilation in eukaryotes: Fusions, relocations, and lateral transfers. BMC Evol. Biol. 8, 39
4. Yi, H., Galant, A., Ravilious, G. E., Preuss, M. L., and Jez, J. M. (2010) Sensing sulfur conditions: Simple to complex protein regulatory mechanisms in plant thiol metabolism. Mol. Plant 3, 269-279
5. Yi, H., Ravilious, G. E., Galant, A., Krishnan, H. B., and Jez, J. M. (2010) From sulfur to homoglutathione: Thiol metabolism in soybean. Amino Acids 39, 963-978
6. Takahashi, H., Kopriva, S., Giordano, M., Saito, K., and Hell, R. (2011) Sulfur assimilation in photosynthetic organisms: Molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62, 157-184
7. Kopriva, S., Mugford, S. G., Baraniecka, P., Lee, B. R., Matthewman, C. A., and Koprivova, A. (2012) Control of sulfur partitioning between primary and secondary metabolism in Arabidopsis. Front. Plant Sci. 3, 163
8. Ravilious, G. E., and Jez, J. M. (2012) Structural biology of plant sulfur metabolism: From assimilation to biosynthesis. Nat. Prod. Rep. 29, 1138-1152
9. Höfgen, R., Kreft, O., Willmitzer, L., and Hesse, H. (2001) Manipulation of thiol contents in plants. Amino Acids 20, 291-299
10. Hawkesford, M. J., and De Kok, L. J. (2006) Managing sulphur metabolism in plants. Plant Cell Environ. 29, 382-395
11. White, P. J., and Brown, P. H. (2010) Plant nutrition for sustainable development and global health. Ann. Bot. 105, 1073-1080
12. Ohkama-Ohtsu, N., and Wasaki, J. (2010) Recent progress in plant nutrition research: Cross-talk between nutrients, plant physiology, and soil microorganisms. Plant Cell Physiol. 51, 1255-1264
13. Shin, R., Jez, J. M., Basra, A., Zhang, B., and Schachtman, D. P. (2011) 14-3-3 proteins fine-tune plant nutrient metabolism. FEBS Lett. 585, 143-147
14. Aharoni, A., and Galili, G. (2011) Metabolic engineering of the plant primary- secondary metabolism interface. Curr. Opin. Biotechnol. 22, 239-244
15. Chan, K. X., Wirtz, M., Phua, S. Y., Estavillo, G. M., and Pogson, B. J. (2013) Balancing metabolites in drought: The sulfur assimilation conundrum. Trends Plant Sci. 18, 18-29
16. Asahi, T. (1964) Sulfur metabolism in higher plants: IV. Mechanism of sulfate reduction in chloroplasts. Biochim. Biophys. Acta 82, 58-66
17. Osslund, T., Chandler, C., and Segel, I. (1982) ATP sulfurylase from higher plants: Purification and preliminary kinetics studies of the cabbage leaf enzyme. Plant Physiol. 70, 39-45
18. Murillo, M., and Leustek, T. (1995) Adenosine-5′-triphosphate sulfurylase from Arabidopsis thaliana and Escherichia coli are functional equivalent but structurally and kinetically divergent: Nucleotide sequence of two adenosine-5′-triphosphate sulfurylase cDNAs from Arabidopsis thaliana and analysis of a recombinant enzyme. Arch. Biochem. Biophys. 323, 195-204
19. Phartiyal, P., Kim, W. S., Cahoon, R. E., Jez, J. M., and Krishnan, H. B. (2006) Soybean ATP sulfurylase, a homodimeric enzyme involved in sulfur assimilation, is abundantly expressed in roots and induced by cold treatment. Arch. Biochem. Biophys. 450, 20-29
20. Klein, M., and Papenbrock, J. (2004) The multi-protein family of Arabidopsis sulphotransferases and their relatives in other plant species. J. Exp. Bot. 55, 1809-1820
21. Mugford, S. G., Yoshimoto, N., Reichelt, M., Wirtz, M., Hill, L., Mugford, S. T., Nakazato, Y., Noji, M., Takahashi, H., Kramell, R., Gigolashvili, T., Flügge, U. I., Wasternack, C., Gershenzon, J., Hell, R., Saito, K., and Kopriva, S. (2009) Disruption of adenosine-5′- phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21, 910-927
22. Mugford, S. G., Matthewman, C. A., Hill, L., and Kopriva, S. (2010) Adenosine- 5′-phosphosulfate kinase is essential for Arabidopsis viability. FEBS Lett. 584, 119-123
23. Yatusevich, R., Mugford, S. G., Matthewman, C., Gigolashvili, T., Frerigmann, H., Delaney, S., Koprivova, A., Flügge, U. I., and Kopriva, S. (2010) Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J. 62, 1-11
24. Ravilious, G. E., Nguyen, A., Francois, J. A., and Jez, J. M. (2012) Structural basis and evolution of redox regulation in plant adenosine-5′- phosphosulfate kinase. Proc. Natl. Acad. Sci. U.S.A. 109, 309-314
25. Ravilious, G. E., and Jez, J. M. (2012) Nucleotide binding site communication in Arabidopsis thaliana adenosine 5′-phosphosulfate kinase. J. Biol. Chem. 287, 30385-30394
26. Ravilious, G. E., Westfall, C. S., and Jez, J. M. (2013) Redox-linked gating of nucleotide binding by the N-terminal domain of adenosine 5′-phosphosulfate kinase. J. Biol. Chem. 288, 6107-6115
27. Zhang, M., Ravilious, G. E., Hicks, L. M., Jez, J. M., and McCulla, R. (2012) Redox switching of adenosine-5′-phosphosulfate kinase with photoactivatable atomic oxygen precursors. J. Am. Chem. Soc. 134, 16979-16982
28. Leustek, T., Murillo, M., and Cervantes, M. (1994) Cloning of a cDNA encoding ATP sulfurylase from Arabidopsis thaliana by functional expression in Saccharomyces cerevisiae. Plant Physiol. 105, 897-902
29. Klonus, D., Höfgen, R., Willmitzer, L., and Riesmeier, J. W. (1994) Isolation and characterization of two cDNA clones encoding ATP-sulfurylases from potato by complementation of a yeast mutant. Plant J. 6, 105-112
30. Klonus, D., Riesmeier, J. W., and Willmitzer, L. (1995) A cDNA clone for an ATP-sulfurylase from Arabidopsis thaliana. Plant Physiol. 107, 653-654
31. Logan, H. M., Cathala, N., Grignon, C., and Davidian, J. C. (1996) Cloning of a cDNA encoded by a member of the Arabidopsis thaliana ATP sulfurylase multigene family. J. Biol. Chem. 271, 12227-12233
32. Heiss, S., Schäfer, H. J., Haag-Kerwer, A., and Rausch, T. (1999) Cloning sulfur assimilation genes of Brassica juncea L.: Cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase. Plant Mol. Biol. 39, 847-857
33. Hatzfeld, Y., Lee, S., Lee, M., Leustek, T., and Saito, K. (2000) Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248, 51-58
34. Zhu, L., Deng, W. W., Ye, A. H., Yu, M., Wang, Z. X., and Jiang, C. J. (2008) Cloning of two cDNAs encoding a family of ATP sulfurylase from Camellia sinensis related to selenium or sulfur metabolism and functional expression in Escherichia coli. Plant Physiol. Biochem. 46, 731-738
35. Renosto, F., Patel, H. C., Martin, R. L., Thomassian, C., Zimmerman, G., and Segel, I. H. (1993) ATP sulfurylase from higher plants: kinetic and structural characterization of the chloroplast and cytosol enzymes from spinach leaf. Arch. Biochem. Biophys. 307, 272-285
36. Rotte, C., and Leustek, T. (2000) Differential subcellular localization and expression of ATP sulfurylase and 5′-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
37. Brunold, C., and Suter, M. (1984) Regulation of sulfate assimilation by nitrogen nutrition in the duckweed Lemna minor L. Plant Physiol. 76, 579-583
38. Cacco, G., Saccomani, M., and Ferrari, G. (1977) Development of sulfate uptake capacity and ATP-sulfurylase activity during root elongation in maize. Plant Physiol. 60, 582-584
39. Vauclare, P., Kopriva, S., Fell, D., Suter, M., Sticher, L., von Ballmoos, P., Krähenbühl, U., den Camp, R. O., and Brunold, C. (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: Adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J. 31, 729-740
40. Liang, G., Yang, F., and Yu, D. (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J. 62, 1046-1057
41. Kawashima, C. G., Matthewman, C. A., Huang, S., Lee, B. R., Yoshimoto, N., Koprivova, A., Rubio-Somoza, I., Todesco, M., Rathjen, T., Saito, K., Takahashi, H., Dalmay, T., and Kopriva, S. (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J. 66, 863-876
42. Mougous, J. D., Lee, D. H., Hubbard, S. C., Schelle, M. W., Vocadlo, D. J., Berger, J. M., and Bertozzi, C. R. (2006) Molecular basis for G-protein control of the prokaryotic ATP sulfurylase. Mol. Cell 21, 109-122
43. Beynon, J. D., MacRae, I. J., Huston, S. L., Nelson, D. C., Segel, I. H., and Fisher, A. J. (2001) Crystal structure of ATP sulfurylase from the bacterial symbiont of the hydrothermal vent tubeworm Riftia pachyptila. Biochemistry 40, 14509-14517
44. Taguchi, Y., Sugishima, M., and Fukuyama, K. (2004) Crystal structure of a novel zinc-binding ATP sulfurylase from Thermus thermophilus HB8. Biochemistry 43, 4111-4118
45. Yu, Z., Lansdon, E. B., Segel, I. H., and Fisher, A. J. (2007) Crystal structure of the biofunctional ATP sulfurylase-APS kinase from the chemolithotrophic thermophile Aquifex aeolicus. J. Mol. Biol. 365, 732-743
46. Parey, K., Demmer, U., Warkentin, E., Wynen, A., Ermler, U., and Dahl, C. (2013) Structural, biochemical, and genetic characterization of dissimilatory ATP sulfurylase from Allochromatium vinosum. PLoS One 8, e74707
47. Ullrich, T. C., Blaesse, M., and Huber, R. (2001) Crystal structure of ATP sulfurylase from Saccharomyces cerevisiae, a key enzyme in sulfate activation. EMBO J. 20, 316-329
48. Ullrich, T. C., and Huber, R. (2001) The complex structures of ATP sulfurylase with thiosulfate, ADP, and chlorate reveal new insights in inhibitory effects and the catalytic cycle. J. Mol. Biol. 313, 1117-1125
49. MacRae, I. J., Segel, I. H., and Fisher, A. J. (2001) Crystal structure of ATP sulfurylase from Penicillium chrysogenum: Insights into the allosteric regulation of sulfate assimilation. Biochemistry 40, 6795-6804
50. MacRae, I. J., Segel, I. H., and Fisher, A. J. (2002) Allosteric inhibition via R-state destabilization in ATP sulfurylase from Penicillium chrysogenum. Nat. Struct. Biol. 9, 945-949
51. Harjes, S., Bayer, P., and Scheidig, A. J. (2005) The crystal structure of human PAPS synthetase 1 reveals asymmetry in substrate binding. J. Mol. Biol. 347, 623-635
52. Ravilious, G. E., Herrmann, J., Goo Lee, S., Westfall, C. S., and Jez, J. M. (2013) Kinetic mechanism of a dimeric ATP sulfurylase from plants. Biosci. Rep. 33, e00053
53. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
54. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
55. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
56. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc- Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
57. Trott, O., and Olson, A. J. (2010) AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-461
58. Holm, L., and Rosenström, P. (2010) Dali server: Conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
59. Koprivova, A., Giovannetti, M., Baraniecka, P., Lee, B. R., Grondin, C., Loudet, O., and Kopriva, S. (2013) Natural variation in the ATPS1 isoform of ATP sulfurylase contributes to the control of sulfate levels in Arabidopsis. Plant Physiol. 163, 1133-1141
60. Gan, X., Stegle, O., Behr, J., Steffen, J. G., Drewe, P., Hildebrand, K. L., Lyngsoe, R., Schultheiss, S. J., Osborne, E. J., Sreedharan, V. T., Kahles, A., Bohnert, R., Jean, G., Derwent, P., Kersey, P., Belfield, E. J., Harberd, N. P., Kemen, E., Toomajian, C., Kover, P. X., Clark, R. M., Rätsch, G., and Mott, R. (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419-423
61. Phartiyal, P., Kim, W. S., Cahoon, R. E., Jez, J. M., and Krishnan, H. B. (2008) The role 5′-adenylylsulfate reductase in the sulfur assimilation pathway of soybean: Molecular cloning, kinetic characterization, and gene expression. Phytochemistry 69, 356-364
62. Bradley, M. E., Rest, J. S., Li, W. H., and Schwartz, N. B. (2009) Sulfate activation enzymes: phylogeny and association with pyrophosphatase. J. Mol. Evol. 68, 1-13
63. Deyrup, A. T., Singh, B., Krishnan, S., Lyle, S., and Schwartz, N. B. (1999) Chemical modification and site-directed mutagenesis of conserved HXXH and PP-loop motif arginines and histidines in the murine bifunctional ATP sulfurylase/adenosine 5′-phosphosulfate kinase. J. Biol. Chem. 274, 28929-28936
64. Venkatachalam, K. V., Fuda, H., Koonin, E. V., and Strott, C. A. (1999) Site-selected mutagenesis of a conserved nucleotide bindingHXGHmotif located in theATPsulfurylase domain of human bifunctional 3′-phosphoadenosine 5′-phosphosulfate synthase. J. Biol. Chem. 274, 2601-2604
65. Perona, J. J., Rould, M. A., and Steitz, T. A. (1993) Structural basis for transfer RNA aminoacylation by Escherichia coli glutaminyl-tRNA synthetase. Biochemistry 32, 8758-8771
66. Park, Y. S., Gee, P., Sanker, S., Schurter, E. J., Zuiderweg, E. R., and Kent, C. (1997) Identification of functional conserved residues of CTP:glycerol-3- phosphate cytidylyltransferase: Role of histidines in the conserved HXGH in catalysis. J. Biol. Chem. 272, 15161-15166
67. Weber, C. H., Park, Y. S., Sanker, S., Kent, C., and Ludwig, M. L. (1999) A prototypical cytidylyltransferase: CTP:glycerol-3-phosphate cytidylyltransferase from Bacillus subtilis. Structure 7, 1113-1124
68. Parey, K., Fritz, G., Ermler, U., and Kroneck, P. M. (2013) Conserving energy with sulfate around 100°C-Structure and mechanism of key metal enzymes in hyperthermophilic Archaeoglobus fulgidus. Metallomics 5, 302-317
69. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890