Regulation of sulfate transport and assimilation in plants

International Review of Cell and Molecular Biology

Volumn 281, Issue C, 2010, Pages 129-159

  Takahashi, Hideki ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

Arabidopsis; Metabolism; Plants; Sulfate; Sulfur; Transporter

Indexed keywords

CYSTEINE SYNTHASE; CYTOKININ; MICRORNA; MOLYBDIC ACID; SULFATE; ANION TRANSPORT PROTEIN; ARABIDOPSIS PROTEIN; MOLYBDENUM; VEGETABLE PROTEIN;

ARABIDOPSIS; BINDING AFFINITY; BOOK; DOWN REGULATION; FEEDBACK SYSTEM; GENE TRANSFER; NONHUMAN; PHLOEM CELL; PHYLOGENETIC TREE; PLANT METABOLISM; PLANT STOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHOOT; SULFATE ASSIMILATION; SYMBIOSIS; TONOPLAST; TRANSCRIPTION REGULATION; BIOLOGICAL MODEL; CELL VACUOLE; GENETICS; ION TRANSPORT; METABOLISM; PHLOEM; PHYLOGENY; PLANT; PLANT GENE; PLANT LEAF; PLANT ROOT; PLANT SEED; REVIEW;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

ANION TRANSPORT PROTEINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENES, PLANT; ION TRANSPORT; MODELS, BIOLOGICAL; MOLYBDENUM; PHLOEM; PHYLOGENY; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANT SHOOTS; PLANTS; SEEDS; SULFATES; VACUOLES;

EID: 77955915565     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1937-6448(10)81004-4     Document Type: Article

References (112)

1. Allen, E., Xie, Z., Gustafson, A.M., Carrington, J.C., 2005. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207-221.
2. Aravind, L., Koonin, E.V., 2000. The STAS domain-a link between anion transporters and antisigma-factor antagonists. Curr. Biol. 10, R53-R55.
3. Awazuhara, M., Kim, H., Goto, D.B., Matsu, A., Hayashi, H., Chino, M., et al., 2002. A 235-bp region from a nutritionally regulated soybean seed-specific gene promoter can confer its sulfur and nitrogen response to a constitutive promoter in aerial tissues of Arabidopsis thaliana. Plant Sci. 163, 75-82.
4. Awazuhara, M., Fujiwara, T., Hayashi, H., Watanabe-Takahashi, A., Takahashi, H., Saito, K., 2005. The function of SULTR2;1 sulfate transporter during seed development in Arabidopsis thaliana. Physiol. Plant. 125, 95-105.
5. Barberon, M., Berthomieu, P., Clairotte, M., Shibagaki, N., Davidian, J.-C., Gosti, F., 2008. Unequal functional redundancy between the two Arabidopsis thaliana high-affinity sulphate transporters SULTR1;1 and SULTR1;2. New Phytol. 180, 608-619.
6. Baxter, I., Muthukumar, B., Park, H.C., Buchner, P., Lahner, B., Danku, J., et al., 2008. Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet. 4, e1000004.
7. Benning, C., 1998. Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 53-75.
8. Berkowitz, O., Wirtz, M., Wolf, A., Kuhlmann, J., Hell, R., 2002. Use of biomolecular interaction analysis to elucidate the regulatory mechanism of the cysteine synthase complex from Arabidopsis thaliana. J. Biol. Chem. 277, 30629-30634.
9. Bianchini, F., Vainio, H., 2001. Allium vegetables and organosulfur compounds: do they help prevent cancer? Environ. Health Perspect. 109, 893-902.
10. Bolchi, A., Petrucco, S., Tenca, P.L., Foroni, C., Ottonello, S., 1999. Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response to variations in sulfur nutritional status: stereospecific down-regulation by L-cysteine. Plant Mol. Biol. 39, 527-537.
11. Bourgis, F., Roje, S., Nuccio, M.L., Fisher, D.B., Tarczynski, M.C., Li, C., et al., 1999. S-Methylmethionine plays a major role in phloem sulfur transport and is synthesized by a novel type of methyltransferase. Plant Cell 11, 1485-1498.
12. Buchanan, B.B., Balmer, Y., 2005. Redox regulation: a broadening horizon. Annu. Rev. Plant Biol. 56, 187-220.
13. 2S and pedospheric sulfate nutrition. Plant Physiol. 136, 3396-3408.
14. Buchner, P., Takahashi, H., Hawkesford, M.J., 2004b. Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J. Exp. Bot. 55, 1765-1773.
15. Cairns, N.G., Pasternak, M., Wachter, A., Cobbett, C.S., Meyer, A.J., 2006. Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol. 141, 446-455.
16. 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.
17. Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W., Ecker, J.R., 1997. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89, 1133-1144.
18. Cherest, H., Davidian, J.-C., Thomas, D., Benes, V., Ansorge, W., Surdin-Kerjan, Y., 1997. Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics 145, 627-635.
19. Clarkson, D.T., Smith, F.W., Vanden Berg, P.J., 1983. Regulation of sulfate transport in a tropical legume, Macroptilium atropurpureum cv. Siratro. J. Exp. Bot. 34, 1463-1483.
20. Crawford, N.M., Kahn, M.L., Leustek, T., Long, S.R., 2000. Nitrogen and sulfur. In: Buchanan, B.B., Gruissem, W., Jones, R.L. (Eds.), Biochemistry & Molecular Biology of Plants. American Society of Plant Biologists, Rockville, MD, pp. 824-849.
21. Deane-Drummond, C.E., 1987. The regulation of sulfate uptake following growth of Pisum sativum L. seedlings in S nutrient limiting conditions. Interaction between nitrate and sulphate transport. Plant Sci. 50, 27-35.
22. Droux, M., Ruffet, M.L., Douce, R., Job, D., 1998. Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants-structural and kinetic properties of the free and bound enzymes. Eur. J. Biochem. 255, 235-245.
23. Dubousset, L., Abdallah, M., Desfeux, A.S., Etienne, P., Meuriot, F., Hawkesford, M.J., et al., 2009. Remobilization of leaf S compounds and senescence in response to restricted sulphate supply during the vegetative stage of oilseed rape are affected by mineral N availability. J. Exp. Bot. 60, 3239-3253.
24. El Kassis, E., Cathala, N., Rouached, H., Fourcroy, P., Berthomieu, P., Terry, N., et al., 2007. Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol. 143, 1231-1241.
25. Fisher, R.F., Long, S.R., 1992. Rhizobium-plant signal exchange. Nature 357, 655-660.
26. Fitzpatrick, K.L., Tyerman, S.D., Kaiser, B.N., 2008. Molybdate transport through the plant sulfate transporter SHST1. FEBS Lett. 582, 1508-1513.
27. Franco-Zorrilla, J.M., Martin, A.C., Solano, R., Rubio, V., Leyva, A., Paz-Ares, J., 2002. Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. Plant J. 32, 353-360.
28. Gigolashvili, T., Berger, B., Mock, H.P., Müller, C., Weisshaar, B., Flügge, U.I., 2007a. The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 50, 886-901.
29. Gigolashvili, T., Yatusevich, R., Berger, B., Müller, C., Flügge, U.I., 2007b. The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 51, 247-261.
30. Gross, A., Brückner, G., Heldt, H.W., Flügge, U.-I., 1990. Comparison of the kinetic properties, inhibition and labelling of the phosphate translocators from maize and spinach mesophyll chloroplasts. Planta 180, 262-271.
31. Grubb, C., Abel, S., 2006. Glucosinolate metabolism and its control. Trends Plant Sci. 11, 89-100.
32. Guo, H., Ecker, J.R., 2004. The ethylene signaling pathway: new insights. Curr. Opin. Plant Biol. 7, 40-49.
33. Gutierrez-Marcos, J.F., Roberts, M.A., Campbell, E.J., Wray, J.L., 1996. Three members of a novel small gene-familiy from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and "APS reductase" activity. Proc. Natl. Acad. Sci. USA 93, 13377-13382.
34. Hagen, G., Guilfoyle, T.J., 2002. Auxin-responsive gene expression, genes, promoters and regulatory factors. Plant Mol. Biol. 49, 373-385.
35. Halkier, B.A., Gershenzon, J., 2006. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303-333.
36. Hawkesford, M.J., Davidian, J.-C., Grignon, C., 1993. Sulphate/proton cotransport in plasma-membrane vescicles isolated from roots of Brassica napus L.: increased transport in membranes isolated from sulphur-starved plants. Planta 190, 297-304.
37. Herschbach, C., Rennenberg, H., 1991. Influence of glutathione (GSH) on sulfate influx, xylem loading and exudation in excised tobacco roots. J. Exp. Bot. 42, 1021-1029.
38. 2S. Plant Physiol. 124, 461-473.
39. Hirai, M.Y., Fujiwara, T., Chino, M., Naito, S., 1995. Effects of sulfate concentrations on the expression of a soybean seed storage protein gene and its reversibility in transgenic Arabidopsis thaliana. Plant Cell Physiol. 36, 1331-1339.
40. Hirai, M.Y., Fujiwara, T., Awazuhara, M., Kimura, T., Noji, M., Saito, K., 2003. Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 33, 651-663.
41. Hirai, M.Y., Yano, M., Goodenowe, D.B., Kanaya, S., Kimura, T., Awazuhara, M., et al., 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.
42. Hirai, M.Y., Sugiyama, K., Sawada, Y., Tohge, T., Obayashi, T., Suzuki, A., et al., 2007. Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl. Acad. Sci. USA 104, 6478-6483.
43. Hopkins, L., Parmar, S., Blaszczyk, A., Hesse, H., Hoefgen, R., Hawkesford, M.J., 2005. O-Acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol. 138, 433-440.
44. Howarth, J.R., Fourcroy, P., Davidian, J.-C., Smith, F.W., Hawkesford, M.J., 2003. Cloning of two contrasting high-affinity sulphate transporters from tomato induced by low sulphate and infection by the vascular pathogen Verticillium dahlia. Planta 218, 58-64.
45. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., et al., 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409, 1060-1063.
46. Jones, M.G., Hughes, J., Tregova, A., Milne, J., Tomsett, A.B., Collin, H.A., 2004. Biosynthesis of the flavour precursors of onion and garlic. J. Exp. Bot. 55, 1903-1918.
47. Jones-Rhoades, M.W., Bartel, D.P., 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14, 787-799.
48. Jones-Rhoades, M.W., Bartel, D.P., Bartel, B., 2006. MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19-53.
49. 2. J. Plant Physiol. 133, 756-763.
50. Kataoka, T., Watanabe-Takahashi, A., Hayashi, N., Ohnishi, M., Mimura, T., Buchner, P., et al., 2004a. Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16, 2693-2704.
51. Kataoka, T., Hayashi, N., Yamaya, T., Takahashi, H., 2004b. Root-to-shoot transport of sulfate in Arabidopsis: evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol. 136, 4198-4204.
52. Kawashima, C.G., Berkowitz, O., Hell, R., Noji, M., Saito, K., 2005. Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol. 137, 220-230.
53. Kawashima, C.G., Yoshimoto, N., Maruyama-Nakashita, A., Tsuchiya, Y.N., Saito, K., Takahashi, H., et al., 2009. Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J. 57, 313-321.
54. Ketter, J.S., Jarai, G., Fu, Y.H., Marzluf, G.A., 1991. Nucleotide sequence, messenger RNA stability, and DNA recognition elements of cys-14, the structural gene for sulfate permease II in Neurospora crassa. Biochemistry 30, 1780-1787.
55. Koprivova, A., Suter, M., Op den Camp, R., Brunold, C., Kopriva, S., 2000. Regulation of sulfur assimilation by nitrogen in Arabidopsis. Plant Physiol. 122, 737-746.
56. Krusell, L., Krause, K., Ott, T., Desbrosses, G., Krämer, U., Sato, S., et al., 2005. The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell 17, 1625-1636.
57. Kutz, A., Müller, A., Hennig, P., Kaiser, W.M., Piotrowski, M., Weiler, E.W., 2002. A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J. 30, 95-106.
58. Kuzuhara, Y., Isobe, A., Awazuhara, M., Fujiwara, T., Hayashi, H., 2000. Glutathione levels in phloem sap of rice plants under sulfur deficient conditions. Soil Sci. Plant Nutr. 46, 265-270.
59. 2--uptake in intact canola. The role of phloem-translocated glutathione. Plant Physiol. 111, 147-157.
60. Lappartient, A.G., Vidmar, J.J., Leustek, T., Glass, A.D.M., Touraine, B., 1999. Inetr-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J. 18, 89-95.
61. Lass, B., Ullrich-Eberius, C.L., 1984. Evidence for proton/sulfate cotransport and its kinetics in Lemna gibba G1. Planta 161, 53-60.
62. Laudenbach, D.E., Grossman, A.R., 1991. Characterization and mutagenesis of sulfurregulated genes in a cyanobacterium: evidence for function in sulfate transport. J. Bacteriol. 173, 2739-2750.
63. Leggett, J.E., Epstein, E., 1956. Kinetics of sulfate absorption by barley roots. Plant Physiol. 31, 222-226.
64. Leustek, T., Martin, M.N., Bick, J.A., 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.
65. Lindberg, P., Melis, A., 2008. The chloroplast sulfate transport system in the green alga Chlamydomonas reinhardtii. Planta 228, 951-961.
66. Martin, A.C., del Pozo, J.C., Iglesias, J., Rubio, V., Solano, R., de la Pena, A., et al., 2000. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J. 24, 559-567.
67. Martinoia, E., Massonneau, A., Frangne, N., 2000. Transport processes of solutes across the vacuolar membrane of higher plants. Plant Cell Physiol. 41, 1175-1186.
68. Martinoia, E., Maeshima, M., Neuhaus, H.E., 2007. Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 58, 83-102.
69. Maruyama-Nakashita, A., Inoue, E., Watanabe-Takahashi, A., Yamaya, T., Takahashi, H., 2003. Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effect on sulfur nutrition on multiple metabolic pathways. Plant Physiol. 132, 597-605.
70. Maruyama-Nakashita, A., Nakamura, Y., Watanabe-Takahashi, A., Yamaya, T., Takahashi, H., 2004a. Induction of SULTR1;1 sulfate transporter in Arabidopsis roots involves protein phosphorylation/dephosphorylation circuit for transcriptional regulation. Plant Cell Physiol. 45, 340-345.
71. Maruyama-Nakashita, A., Nakamura, Y., Yamaya, T., Takahashi, H., 2004b. A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J. 38, 779-789.
72. Maruyama-Nakashita, A., Nakamura, Y., Watanabe-Takahashi, A., Inoue, E., Yamaya, T., Takahashi, H., 2005. Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J. 42, 305-314.
73. Maruyama-Nakashita, A., Nakamura, Y., Tohge, T., Saito, K., Takahashi, H., 2006. Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18, 3235-3251.
74. Mount, D.B., Romero, M.F., 2004. The SLC26 gene family of multifunctional anion exchangers. Pflugers Arch. 447, 710-721.
75. Mugford, S.G., Yoshimoto, N., Reichelt, M., Wirtz, M., Hill, L., Mugford, S.T., et al., 2009. Disruption of adenosine-5'-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21, 910-927.
76. Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H., Hoefgen, R., 2003. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J. 33, 633-650.
77. Noji, M., Inoue, K., Kimura, N., Gouda, A., Saito, K., 1998. Isoform-dependent differences in feedback regulation and subcellular localization of serine acetyltransferase involved in cysteine biosynthesis from Arabidopsis thaliana. J. Biol. Chem. 273, 32739-32745.
78. Ohkama, N., Takei, K., Sakakibara, H., Hayashi, H., Yoneyama, T., Fujiwara, T., 2002. Regulation of sulfur-responsive gene expression by exogenously applied cytokinins in Arabidopsis thaliana. Plant Cell Physiol. 43, 1493-1501.
79. Ohkama-Ohtsu, N., Kasajima, I., Fujiwara, T., Naito, S., 2004. Isolation and characterization of an Arabidopsis mutant that overaccumulates O-acetyl-L-Ser. Plant Physiol. 136, 3209-3222.
80. Page, R.D.M., 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357-358.
81. Rae, A.L., Smith, F.W., 2002. Localisation of expression of a high-affinity sulfate transporter in barley roots. Planta 215, 565-568.
82. Rouached, H., Berthomieu, P., El Kassis, E., Cathala, N., Catherinot, V., Labesse, G., et al., 2005. Structural and functional analysis of the C-terminal STAS (sulfate transporter and anti-sigma antagonist) domain of the Arabidopsis thaliana sulfate transporter SULTR1.2. J. Biol. Chem. 280, 15976-15983.
83. Rouached, H., Wirtz, M., Alary, R., Hell, R., Arpat, A.B., Davidian, J.-C., et al., 2008. Differential regulation of the expression of two high-affinity sulfate transporters, SULTR1.1 and SULTR1.2, in Arabidopsis. Plant Physiol. 147, 897-911.
84. Ruffet, M.L., Droux, M., Douce, R., 1994. Purification and kinetic properties of serine acetyltransferase free of O-acetylserine(thiol)lyase from spinach chloroplasts. Plant Physiol. 104, 597-604.
85. Saito, K., 2000. Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Plant Biol. 3, 188-195.
86. Saito, K., 2004. Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol. 136, 2443-2450.
87. Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
88. Setya, A., Murillo, M., Leustek, T., 1996. Sulfate reduction in higher plants: molecular evidence for a novel 5'-adenylylsulfate reductase. Proc. Natl. Acad. Sci. USA 93, 13383-13388.
89. Shibagaki, N., Grossman, A.R., 2004. Probing the function of STAS domains of the Arabidopsis sulfate transporters. J. Biol. Chem. 279, 30791-30799.
90. Shibagaki, N., Grossman, A.R., 2006. The role of the STAS domain in the function and biogenesis of a sulfate transporter as probed by random mutagenesis. J. Biol. Chem. 281, 22964-22973.
91. Shibagaki, N., Rose, A., Mcdermott, J.P., Fujiwara, T., Hayashi, H., Yoneyama, T., et al., 2002. Selenate-resistant mutants of Arabidopsis thaliana identify SULTR1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J. 29, 475-486.
92. Sirko, A., Hryniewicz, M., Hulanicka, D., Böck, A., 1990. Sulfate and thiosulfate transport in Escherichia coli K-12: nucleotide sequence and expression of the cysTWAM gene cluster. J. Bacteriol. 172, 3351-3357.
93. Skirycz, A., Reichelt, M., Burow, M., Birkemeyer, C., Rolcik, J., Kopka, J., et al., 2006. DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J. 47, 10-24.
94. Smith, F.W., Hawkesford, M.J., Prosser, I.M., Clarkson, D.T., 1995a. Isolation of a cDNA from Saccharomyces cerevisiae that encodes a high affinity sulphate transporter at the plasma membrane. Mol. Gen. Genet. 247, 709-715.
95. Smith, F.W., Ealing, P.M., Hawkesford, M.J., Clarkson, D.T., 1995b. Plant members of a family of sulfate transporters reveal functional subtypes. Proc. Natl. Acad. Sci. USA 92, 9373-9377.
96. Smith, F.W., Hawkesford, M.J., Ealing, P.M., Clarkson, D.T., Vanden Berg, P.J., Belcher, A.R., et al., 1997. Regulation of expression of a cDNA from barley roots encoding a high affinity sulfate transporter. Plant J. 12, 875-884.
97. Tabe, L.M., Droux, M., 2001. Sulfur assimilation in developing lupin cotyledons could contribute significantly to the accumulation of organic sulfur reserves in the seed. Plant Physiol. 126, 176-187.
98. Takahashi, H., Yamazaki, M., Sasakura, N., Watanabe, A., Leustek, T., de Almeida Engler, J., et al., 1997. Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate starved roots plays a central role in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94, 11102-11107.
99. Takahashi, H., Watanabe-Takahashi, A., Smith, F.W., Blake-Kalff, M., Hawkesford, M.J., Saito, K., 2000. The role of three functional sulfate transporters involved in uptake and translocation of sulfate in Arabidopsis thaliana. Plant J. 23, 171-182.
100. Takahashi, H., Yoshimoto, N., Saito, K., 2006. Anionic nutrient transport in plants: the molecular bases of sulfate transporter gene family. In: Setlow, J.K. (Ed.), Genetic Engineering, Vol. 27. Springer, New York, NY, pp. 67-80.
101. Talalay, P., Fahey, J.W., 2001. Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. J. Nutr. 131, 3027S-3033S.
102. Tejada-Jiménez, M., Llamas, A., Sanz-Luque, E., Galván, A., Fernández, E., 2007. A highaffinity molybdate transporter in eukaryotes. Proc. Natl. Acad. Sci. USA 104, 20126-20130.
103. Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
104. Tomatsu, H., Takano, J., Takahashi, H., Watanabe-Takahashi, A., Shibagaki, N., Fujiwara, T., 2007. An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc. Natl. Acad. Sci. USA 104, 18807-18812.
105. Ulmasov, T., Hagen, G., Guilfoyle, T.J., 1999. Dimerization and DNA binding of auxin response factors. Plant J. 19, 309-319.
106. Vauclare, P., Kopriva, S., Fell, D., Suter, M., Sticher, L., von Ballmoos, P., et al., 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.
107. Vidmar, J.J., Schjoerring, J.K., Touraine, B., Glass, A.D.M., 1999. Regulation of the hvst1 gene encoding a high-affinity sulfate transporter from Hordeum vulgare. Plant Mol. Biol. 40, 883-892.
108. Vidmar, J.J., Tagmount, A., Cathala, N., Touraine, B., Davidian, J.-C.E., 2000. Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. FEBS Lett. 475, 65-69.
109. Wirtz, M., Hell, R., 2006. Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J. Plant Physiol. 163, 273-286.
110. Yoshimoto, N., Takahashi, H., Smith, F.W., Yamaya, T., Saito, K., 2002. Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J. 29, 465-473.
111. Yoshimoto, N., Inoue, E., Saito, K., Yamaya, T., 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.
112. Yoshimoto, N., Inoue, E., Watanabe-Takahashi, A., Saito, K., Takahashi, H., 2007. Posttranscriptional regulation of high-affinity sulphate transporters in Arabidopsis by sulphur nutrition. Plant Physiol. 145, 378-388.