The multi-protein family of sulfotransferases in plants: Composition, occurrence, substrate specificity, and functions

Frontiers in Plant Science

Volumn 5, Issue OCT, 2014, Pages

  Hirschmann, Felix ^a   Krause, Florian ^a   Papenbrock, Jutta ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

Arabidopsis thaliana; Glucosinolate; Histidine residue; Phosphoadenosine 5 Phosphosulfate; Sulfotransferase

Indexed keywords

EID: 84907979876     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00556     Document Type: Article

References (97)

1. Alexandratos, S. D. (1999). Synthesis and purification of zosteric acid. US Patent 5990336.
2. Allali-Hassani, A., Pan, P. W., Dombrovski, L., Najmanovich, R., Tempel, W., Dong, A., et al. (2007). Structural and chemical profiling of the human cytosolic sulfotransferases. Plos Biol. 5:e97. doi: 10.1371/journal.pbio.0050097
3. Amano, Y., Tsubouchi, H., Shinohara, H., Ogawa, M., and Matsubayashi, Y. (2007). Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, 18333–18338. doi: 10.1073/pnas.0706403104
4. Aquino, R. S., Grativol, C., Mourão, P. S., and Meyer, P. (2011). Rising from the sea: correlations between sulfated polysaccharides and salinity in plants. Plos One 6:e18862. doi: 10.1371/journal.pone.0018862
5. Aquino, R. S., Landeira-Fernandez, A. M., Valente, A. P., Andrade, L. R., and Mourão, P. A. (2005). Occurrence of sulfated galactans in marine angiosperms: evolutionary implications. Glycobiology 15, 11–20. doi: 10.1093/glycob/cwh138
6. Baek, D., Pathange, P., Chung, J.-S., Jiang, J., Gao, L., Oikawa, A., et al. (2010). A stress-inducible sulphotransferase sulphonates salicylic acid and confers pathogen resistance in Arabidopsis. Plant Cell Environ. 33, 1383–1392. doi: 10.1111/j.1365-3040.2010.02156.x
7. Berger, I., Guttman, C., Amar, D., Zarivach, R., and Aharoni, A. (2011). The molecular basis for the broad substrate specificity of human sulfotransferase 1A1. Plos One 6:e26794. doi: 10.1371/journal.pone.0026794
8. Bidwell, L. M., Mcmanus, M. E., Gaedigk, A., Kakuta, Y., Negishi, M., Pedersen, L., et al. (1999). Crystal structure of human catecholamine sulfotransferase. J. Mol. Biol. 293, 521–530. doi: 10.1006/jmbi.1999.3153
9. 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. doi: 10.1016/S0031-9422(02)00549-6
10. Celenza J. L., Quiel, J. A., Smolen, G. A., Merrikh, H., Silvestro, A. R., Normanly, J., et al. (2005). The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol. 137, 253–262. doi: 10.1104/pp.104.054395
11. Chen, R., Jiang, Y., Dong, J., Zhang, X., Xiao, H., Xu, Z., etal. (2012). Genome-wide analysis and environmental response profiling of sot family genes in rice (Oryza sativa). Genes Genom. 34, 549-560. doi: 10.1007/s13258-012-0053-5
12. Clarke, D. B. (2010). Glucosinolates, structures and analysis in food. Anal. Methods 2, 310-325. doi: 10.1039/B9AY00280D
13. Cook, I., Wang, T., Falany, C. N., and Leyh, T. S. (2012). A nucleotide-gated molecular pore selects sulfotransferase substrates. Biochemistry 51, 5674-5683. doi: 10.1021/bi300631g
14. Cook, I., Wang, T., Falany, C. N., and Leyh, T. S. (2013). High accuracy in silico sulfotransferase models. J. Biol. Chem. 288, 34494-34501. doi: 10.1074/jbc.M113.510974
15. Dajani, R., Cleasby, A., Neu, M., Wonacott, A. J., Jhoti, H., Hood, A. M., et al. (1999). X-ray crystal structure of human dopamine sulfotransferase, SULT1A3: molecular modeling and quantitative structure-activity relationship analysis demonstrate a molecular basis for sulfotransferase substrate specificity. J. Biol. Chem. 274, 37862-37868. doi: 10.1074/jbc.274.53.37862
16. Dantas-Santos, N., Gomes, D. L., Costa, L. S., Cordeiro, S. L., Costa, M. S. S. P., Trindade, E. S., etal. (2012). Freshwater plants synthesize sulfated polysaccharides: heterogalactans from water hyacinth (Eicchornia crassipes). Int. J. Mol. Sci. 13, 961-976. doi: 10.3390/ijms13010961
17. Estavillo, G. M., Crisp, P. A., Pomsiriwong, W., Wirtz, M., Collinge, D., Carrie, C., etal. (2011). Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23, 3992-4012. doi: 10.1105/tpc.111.091033
18. Faulkner, I. J., and Rubery, P. H. (1992). Flavonoids and flavonoid sulphates as probes of auxin-transport regulation in Cucurbita pepo hypocotyl segments and vesicles. Planta 186, 618-625. doi: 10.1007/BF00198044
19. Fenwick, G. R., and Heaney, R. K. (1983). Glucosinolates and their breakdown products in cruciferous crops, foods and feedingstuffs. Food Chem. 11, 249-271. doi: 10.1016/0308-8146(83)90074-90072
20. Finn, R. D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R. Y., Eddy, S. R., et al. (2014). Pfam: the protein families database. Nucl. Acids Res. 42,D222-D230. doi: 10.1093/nar/gkt1223
21. Frerigmann, H., and Gigolashvili, T. (2014). MYB34, MYB51, and MYB122 distinctly regulate indolic glucosinolate biosynthesis in Arabidopsis thaliana. Mol. Plant 7, 814-828. doi: 10.1093/mp/ssu004
22. Fukuta, M., Kobayashi,Y,andUchimura, K. (1998). Molecular cloning and expression of human chondroitin 6-sulfotransferase. Biochim. Biophys. Acta 1399, 57-61.
23. Gamage, N., Barnett, A., Hempel, N., Duggleby, R. G., Windmill, K. F., Martin, J. L., et al. (2006). Human sulfotransferases and their role in chemical metabolism. Toxicol. Sci. 90, 5-22. doi: 10.1093/toxsci/kfj061
24. Gidda, S. K., Miersch, O., Levitin, A., Schmidt, J., Wasternack, C, and Varin, L. (2003). Biochemical and molecular characterization of a hydroxyjasmonate sulfotransferase from Arabidopsis thaliana. J. Biol. Chem. 278, 17895-17900. doi: 10.1074/jbc.M211943200
25. Gidda, S. K., and Varin, L. (2006). Biochemical and molecular characterization og flavonoid 7-sulfotransferase from Arabidopsis thaliana. Plant Physiol. Biochem. 44, 628-636 doi: 10.1074/jbc.M211943200
26. Gigolashvili, T., Berger, B., Mock, H. -P., Muller, C, Weisshaar, B., and Flügge, U.-I. (2007a). The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 50, 886-901. doi: 10.1111/j.1365-313X.2007.03099.x
27. Gigolashvili, T., Yatusevich, R., Berger, B., Müller, C, and Flügge, U.-I. (2007b). TheR2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 51, 247-261. doi: 10.1111/j.1365-313X.2007.03133.x
28. Gigolashvili, T., Engqvist, M., Yatusevich, R., Müller, C, and Flügge, U.-I. (2008). HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytol. 177, 627-642. doi: 10.1111/j.1469-8137.2007.02295.x
29. Gigolashvili, T., Geier, M., Ashykhmina, N., Frerigmann, H., Wulfert, S., Krueger, S., etal. (2012). The Arabidopsis thylakoidADP/ATP carrier TAAC has an additional role in supplying plastidic phosphoadenosine 5-phosphosulfate to the cytosol. Plant Cell 24, 4187-4204. doi: 10.1105/tpc.112.101964
30. ;-phosphosulfate: desulfoglucosinolate sulfotransferase from cress (Lepidium sativum). Plant Physiol. 94, 811-818. doi: 10.1104/pp.94.2.811
31. Graser, G., Oldham, N. J., Brown, P. D., Temp, U., and Gershenzon, J. (2001). The biosynthesis of benzoic acid glucosinolate esters in Arabidopsis thaliana. Phy tochemistry 57,23-32. doi: 10.1016/S0031-9422(00)00501-X
32. Halkier, B.A. (1999). “Glucosinolates,” in Naturally Occurring Glycosides: Chemistry, Distribution and Biological Properties, ed. R. Ikan (New York: John Wiley & Sons Ltd), 193-223.
33. Hanai, H., Nakayama, D., Yang, H., Matsubayashi, Y, Hirota, Y, and Sakagami, Y (2000). Existence of a plant tyrosylprotein sulfotransferase: novel plant enzyme catalyzing tyrosine O-sulfation of preprophytosulfokine variants in vitro. FEBS Lett. 470, 97-101. doi: 10.1016/S0014-5793(00)01299-0
34. Harborne, J. B., and Williams, C. A. (1976). Occurrence of sulphated flavones and caffeic acid esters in members of the fluviales. Biochem. Syst. Ecol 4, 37-41. doi: 10.1016/0305-1978(76)90007-7
35. Hashiguchi, T., Sakakibara, Y, Hara, Y, Shimohira, T., Kurogi, K., Akashi, R., et al. (2013). Identification and characterization of a novel kaempferol sulfotransferase from Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 434, 829-835. doi: 10.1016/j.bbrc.2013.04.022
36. Hashiguchi, T., Sakakibara, Y, Shimohira, T., Kurogi, K., Yamasaki, M., Nishiyama, K., etal. (2014). Identification of a novel flavonoid glycoside sulfotransferase in Arabidopsis thaliana. J. Biochem. 155, 91-97. doi: 10.1093/jb/mvt102
37. Hernàndez-Sebastiá, C., Varin, L., and Marsolais, F. (2008). “Sulfotransferases from plants, algae and phototrophic bacteria,” in Sulfur Metabolism in Phototrophic Organisms, eds R. Hell, C. Dahl, D. Knaff, and T. Leustek (Amsterdam: Springer), 111-130.
38. Hirai, M. Y, Klein, M., Fujikawa, Y, Yano M., Goodenowe, D. B., Yamazaki, Y, et al. (2005). Elucidation of gene-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J. Biol. Chem. 280, 25590-25595. doi: 10.1074/jbc.M502332200
39. Hirai, M. Y, Sugiyama, K., Sawada, Y, Tohge, T., Obayashi, T., Suzuki, A., etal. (2007). Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 6478-6483. doi: 10.1073/pnas.0611629104
40. Huseby, S., Koprivova, A., Lee, B.-R., Saha, S., Mithen, R., Wold, A.-B., etal. (2013). Diurnal and light regulation of sulphur assimilation and glucosinolate biosynthesis in Arabidopsis. J. Exp. Bot. 64, 1039-1048. doi: 10.1093/jxb/ers378
41. Jensen, L. M., Halkier, B. A., and Burow, M. (2014). How to discover a metabolic pathway? An update on gene identification in aliphatic glucosinolate biosynthesis, regulation and transport. Biol. Chem. 395, 529-543. doi: 10.1515/hsz-2013-0286
42. Kakuta, Y, Pedersen, L. G., Carter, C. W, Negishi, M., and Pedersen, L. C. (1997). Crystal structure of estrogen sulphotransferase. Nature Struct. Biol. 4, 904-908. doi: 10.1038/nsb1197-904
43. Kakuta, Y, Petrotchenko, E. V., Pedersen, L. C, and Negishi, M. (1998). The sulfuryl transfer mechanism. J. Biol. Chem. 273, 27325-27330. doi: 10.1074/jbc.273.42.27325
44. ;-phosphosulfate (PAPS) in the regulation of sulfation. FASEB J. 11, 404-418.
45. 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. doi: 10.1093/jxb/erh183
46. Klein, M., and Papenbrock, J. (2008).“Sulfotransferases and their tole in glucosinolate biosynthesis,” in Sulfur Assimilation and Abiotic Stress in Plants, eds. N. Khan, S. Singh, and S. Umar (Berlin: Springer), 149-166. doi: 10.1007/978-3-540-76326-0_7
47. Klein, M., and Papenbrock, J. (2009). Kinetic parameters of desulfoglucosi-nolate sulfotransferases. Physiol. Plant. 135, 140-149. doi: 10.1111/j.1399-3054.2008.01182.x
48. Klein, M., Reichelt, M., Gershenzon, J., and Papenbrock, J. (2006). The three desulfo-glucosinolate sulfotransferase proteins in Arabidopsis have different substrate specificities and are differentially expressed. FEBS J. 273, 122-136. doi: 10.1111/j.1742-4658.2005.05048.x
49. Kliebenstein, D. J., Kroymann, J., Brown, P., Figuth, A., Pedersen, D., Gershenzon, J., etal. (2001a). Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 126,811-825. doi: 10.1104/pp.126.2.811
50. Kliebenstein, D. J., Lambrix, V. M., Reichelt, M., and Gershenzon, J. (2001b). Gene duplication in the diversification of secondary metabolism: Tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13, 681-693. doi: 10.1105/tpc.13.3.681
51. Komori, R., Amano, Y, Ogawa-Ohnishi, M., and Matsubayashi, Y (2009). Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106, 15067-15072. doi: 10.1073/pnas.0902801106
52. Kusche-Gullberg, M., and Kjellén, L. (2003). Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 13, 605-611. doi: 10.1016/j.sbi.2003.08.002
53. Labonne, J. J. D., Goultiaeva, A., and Shore, J. S. (2009). High-resolution mapping of the S-locus in Turnera leads to the discovery of three genes tightly associated with the S-alleles. Mol Genet. Genomics 281, 673-685. doi: 10.1007/s00438-009-0439-5
54. Lacomme, C, and Roby, D. (1996). Molecular cloning of a sulfotransferase in Arabidopsis thaliana and regulation during development and in response to infection with pathogenic bacteria. Plant Mol. Biol. 30, 995-1008. doi: 10.1007/BF00020810
55. Lee, B. R., Huseby, S., Koprivova, A., Chételat, A., Wirtz, M., Mugford, S. T., etal. (2012). Effects of fou8/fry1 mutation on sulfur metabolism: is decreased internal sulfate the trigger of sulfate starvation response? Plos One 7:e39425. doi: 10.1371/journal.pone.0039425
56. Lewis, D. R., Ramirez, M. V., Miller, N. D., Vallabhaneni, P., Ray, W K., Helm, R. F., etal. (2011). Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiol. 156, 144-164. doi: 10.1104/pp.111.172502
57. Li, Y, Sawada, Y, Hirai, A., Sato, M., Kuwahara, A., Yan, X., etal. (2013). Novel insights into the function of Arabidopsis R2R3-MYB transcription factors regulating aliphatic glucosinolate biosynthesis. Plant Cell Physiol. 54,1335-1344. doi: 10.1093/pcp/pct085
58. Luczak, S., Forlani, F., and Papenbrock, J. (2013). Desulfo-glucosinolate sulfotransferases isolated from several Arabidopsis thaliana ecotypes differ in their sequence and enzyme activities. Plant Physiol. Biochem. 63, 15-23. doi: 10.1016/j.plaphy.2012.11.005
59. Malitsky, S., Blum, E., Less, H., Venger, I., Elbaz, M., Morin, S., etal. (2008). The transcript and metabolite networks affected by the two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol. 148, 2021-2049. doi: 10.1104/pp.108.124784
60. Marsolais, F., Boyd, J., Paredes, Y, Schinas, A.-M., Garcia, M., Elzein, S., et al. (2007). Molecular and biochemical characterization of two brassinosteroid sulfotransferases from Arabidopsis, AtST4a (At2g14920) and AtST1 (At2g03760). Planta 225, 1233-1244. doi: 10.1007/s00425-006-0413-y
61. Marsolais, F., Gidda, S. K., Boyd, J., and Varin, L. (2000). Structural and functional similarity with mammalian enzymes. Rec. Adv. Phytochem. 34, 433-456. doi: 10.1371/journal.pone.0104594
62. Marsolais, F., Sebastià, C. H., Rousseau, A., and Varin, L. (2004). Molecular and biochemical characterization of BNST4, an ethanol-inducible steroid sulfotransferase from Brassica napus, and regulation of BNST genes by chemical stress and during development. Plant Sci. 166, 1359-1370. doi: 10.1016/j.plantsci.2004.01.019
63. Marsolais, F., and Varin, L. (1995). Identification of amino acid residues critical for catalysis and cosubstrate binding in the flavonol 3-sulfotransferase. J. Biol. Chem. 270, 30458-30463. doi: 10.1074/jbc.270.51.30458
64. Matsubayashi, Y, and Sakagami, Y (1996). Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc. Natl. Acad. Sci. U.S.A. 93, 7623-7627. doi: 10.1073/pnas.93.15.7623
65. Matsuzaki, Y., Ogawa-Ohnishi, M., Mori, A., and Matsubayashi, Y (2010). Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329,1065-1067. doi: 10.1126/science.1191132
66. Mithen, R. (2001). Glucosinolates - biochemistry, genetics and biological activity. Plant Growth Regul. 34, 91-103. doi: 10.1023/A:1013330819778
67. Møldrup, M. E., Geu-Flores, F., Olsen, C. E., and Halkier, B.A. (2011). Modulation of sulfur metabolism enables efficient glucosinolate engineering. BMC Biotechnol. 11:12. doi: 10.1186/1472-6750-11-12.
68. ;-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21, 910-927. doi: 10.1105/tpc.109.065581
69. Newby, B.-M. Z., Cutright, T., Barrios, C, and Xu, Q. (2006). Zosteric acid—An effective antifoulant for reducing fresh water bacterial attachment on coatings. JCTRes. 3, 69-76. doi: 10.1007/s11998-006-0007-4
70. Ngo, D.-H., and Kim, S.-K. (2013). Sulfated polysaccharides as bioactive agents from marine algae. Int. J. Biol. Macromol. 62, 70-75. doi: 10.1016/j.ijbiomac.2013.08.036
71. Niehrs, C, Beisswanger, R., and Huttner, W. B. (1994). Protein tyrosine sulfation, 1993 - an update. Chem. Biol. Interact. 92, 257-271. doi: 10.1016/0009-2797(94)90068-X
72. Pi, N., Hoang, M. B., Gao, H., Mougous, J. D., Bertozzi, C. R., and Leary, J. A. (2005). Kinetic measurements and mechanism determination of Stf0 sulfotransferase using mass spectrometry. Anal. Biochem. 341, 94-104. doi: 10.1016/j.ab.2005.02.004
73. Pi, N., Yu, Y., Mougous, J. D., and Leary, J. A. (2004). Observation of a hybrid random ping-pong mechanism of catalysis for NodST: a mass spectrometry approach. Protein Sci. 13, 903-912. doi: 10.1110/ps.03581904
74. Piotrowski, M., Schemenewitz, A., Lopukhina, A., Muller, A., Janowitz, T., Weiler, E. W., et al. (2004). Desulfoglucosinolate sulfotransferases from Arabidopsis thaliana catalyze the final step in the biosynthesis of the glucosinolate core structure. J. Biol. Chem. 279,50717-50725. doi: 10.1074/jbc.M407681200
75. Rausch, T., and Wachter, A. (2005). Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci. 10, 503-509. doi: 10.1016/j.tplants.2005.08.006
76. Rivoal, J., and Hanson, A. D. (1994). Choline-O-sulfate biosynthesis in plants (Identification and partial characterization of a salinity-inducible choline sul-fotransferase from species of Limonium (Plumbaginaceae). Plant Physiol. 106, 1187-1193.
77. Rouleau, M., Marsolias, F., Richard, M., Nicolle, L., Voigt, B., Adam, G., etal. (1999). Inactivation of brassinosteroid biological activity by a salicylate-inducible steroid sulfotransferase from Brassicanapus.J. Biol. Chem. 274,20925-20930. doi: 10.1074/jbc.274.30.20925
78. Sandhu, K. S., andNeff, M. M. (2013). The Arabidopsis gene ATST4a in not a typical brassinosteroid catabolic gene. Plant Signal. Behav. 8, 10. doi: 10.4161/psb.26847
79. Shimojima, M., Hoffmann-Benning, S., Garavito, R. M., and Benning, C. (2005). Ferredoxin-dependent glutamate synthase moonlights in plant sulfolipid biosynthesis by forming a complex with SQD1. Arch. Biochem. Biophys. 436, 206-214. doi: 10.1016/j.abb.2005.02.005
80. Smith, D.W., Johnson, K. A., Bingman, C. A., Aceti, D. J., Blommel, P. G., Wrobel, R. L., et al. (2004). Crystal structure of At2g03760, a putative steroid sulfotransferase from Arabidopsis thaliana. Proteins 57, 854-857. doi: 10.1002/prot.20258
81. Sønderby, I. E., Burow, M., Rowe, H. C., Kliebenstein, D. J., and Halkier, B. A. (2010). A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis. Plant Physiol. 153, 348-363. doi: 10.1104/pp.109.149286
82. Sønderby, I. E., Hansen, B. G., Bjarnholt, N., Ticconi, C., Halkier, B. A., and Kliebenstein, D. J. (2007). A system biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. Plos One 2:e1322. doi: 10.1371/journal.pone.0001322
83. Song, C. M., Lim, S. J., and Tong, J. C. (2009). Recent advances in computer-aided drug design. Brief. Bioinf. 10, 579-591. doi: 10.1093/bib/bbp023
84. Vakiani, E., Luz, J. G., and Buck, J. (1998). Substrate specificity and kinetic mechanism of the insect sulfotransferase, retinol dehydratase. J. Biol. Chem. 273, 35381-35387. doi: 10.1074/jbc.273.52.35381.
85. Varin, L., Chamberland, H., Lafontaine, J. G., and Richard, M. (1997a). The enzyme involved in sulfation of the turgorin, gallic acid 4-O-(beta-D-glucopyranosyl-6'-sulfate) is pulvini-localized in Mimosa pudica. Plant J. 12, 831-837. doi: 10.1046/j.1365-313X.1997.12040831.x
86. Varin, L., Marsolais, F., Richard, M., and Rouleau, M. (1997b). Biochemistry and molecular sulfotransferases biology of plant sulfotransferases. FASEB J. 11, 517-525.
87. Varin, L., Deluca, V., Ibrahim, R. K., and Brisson, N. (1992). Molecular characterization of two plant flavonol sulfotransferases. Proc. Natl. Acad. Sci. U.S.A. 89, 1286–1290. doi: 10.1073/pnas.89.4.1286
88. Varin, L., and Ibrahim, R. K. (1992). Novel flavonol 3-sulfotransferase. Purification, kinetic properties, and partial amino acid sequence. J. Biol. Chem. 267, 1858–1863.
89. Varin, L., and Spertini, D. (2003). Desulfoglucosinolate sulfotransferases, sequences coding the same and uses thereof for modulating glucosinolate biosynthesis in plants. Patent WO 2003010318.
90. Wang, H., Wu, J., Sun, S., Liu, B., Cheng, F., Sun, R., etal. (2011). Glucosinolate biosynthetic genes in Brassica rapa. Gene 487, 135–142. doi: 10.1016/j.gene.2011.07.021
91. Wang, T., Cook, I., Falany, C. N., and Leyh, T. S. (2014). Paradigms of sulfotrans-ferase catalysis – the mechanism of SULT2A1. J. Biol. Chem. 289, 26474–2680. doi: 10.1074/jbc.M114.573501
92. Weinshilboum, R. M., and Otterness, D. M. (1994). “Sulfotransferase enzymes,” in Handbook of Experimental Pharmacology, ed. Kauffman (Berlin: Springer-Verlag), 45–78.
93. Wittstock, U., and Halkier, B. A. (2002). Glucosinolate research in the Ara-bidopsis era. Trends Plant Sci. 7, 263–270. doi: 10.1016/S1360-1385(02)02273-2
94. Yamashino, T., Kitayama, M., and Mizuno, T. (2013). Transcription of ST2A encoding a sulfotransferase family protein that is involved in jas-monic acid metabolism is controlled according to the circadian clock-and PIF4/PIF5-mediated external coincidence mechanism in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 77, 2454–2460. doi: 10.1271/bbb.130559
95. Zang, Y.-X., Kim, H. U., Kim, J. A., Lim, M.-H., Jin, M., Lee, S. C., et al. (2009). Genome-wide identification of glucosinolate synthesis genes in Brassica rapa. FEBS J. 276, 3559–3574. doi: 10.1111/j.1742-4658.2009.07076.x
96. Zhai, G., Lehmler, H.-J., and Schnoor, J. L. (2013). Sulfate metabolites of 4-monochlorobiphenyl in whole poplar plants. Environ. Sci. Technol. 47, 557–562. doi: 10.1021/es303807f
97. Zhang, H., Varmalova, O., Vargas, F. M., Falany, C. N., and Leyh, T. S. (1998). Sulfuryl transfer: the catalytic mechanism of human estrogen sulfotransferase. J. Biol. Chem. 273, 10888–10892.doi: 10.1074/jbc.273.18.10888