Sulfur and cysteine metabolism

Sulfur: A Missing Link between Soils, Crops, and Nutrition

Volumn , Issue , 2015, Pages 83-104

  Hoefgen, Rainer ^a   Hesse, Holger ^a  

^a Wissenschaftspark Golm   (Germany)

Author keywords

Biochemical activation; Crop productivity; Cysteine metabolism; Cysteine synthesis; Reductive pathway; Sulfate reduction; Sulfate uptake; Sulfur metabolism

Indexed keywords

EID: 85103041141     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.2134/agronmonogr50.c6     Document Type: Chapter

References (126)

1. Anderson, J.W. 1990. Sulfur metabolism in plants. p. 327-381. In B.J. Mifl in and P.J. Lea (ed.) The biochemistry of plants. Vol. 16. Academic Press, New York.
2. Awazuhara, M., T. Fujiwara, H. Hayashi, A. Watanabe-Takahashi, H. Takahashi, and K. Saito. 2005. The function of SULTR2;1 sulfate transporter during seed development in Arabidopsis thaliana. Physiol. Plant. 125:95-105.
3. Azevedo, R.A., P. Arruda, W.L. Turner, and P.J. Lea. 1997. The biosynthesis and metabolism of the aspartate derived amino acids in higher plants. Phytochemistry 46:395-419.
4. Baxter, I., B. Muthukumar, H.C. Park, P. Buchner, B. Lahner, J. Danku, K. Zhao, J. Lee, M.J. Hawkesford, M.L. Guerinot, and D.E. Salt. 2008. Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet. 4:e1000004, doi:10.1371/ journal.pgen.1000004
5. Benning, C. 1998. Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:53-75.
6. Blake-Kalff, M.M.A. 2000. Diagnosing sulfur defi ciency in fi eld-grown oilseed rape (Brassica napus). Plant Soil 225:95-107.
7. Blaszczyk, A., R. Brodzik, and A. Sirko. 1999. Increased resistance to oxidative stress in transgenic tobacco plants overexpressing bacterial serine acetyltransferase. Plant J. 20:237-243.
8. Bork, C., J.D. Schwenn, and R. Hell. 1998. Isolation and characterization of a gene for assimilatory sulfi te reductase from Arabidopsis thaliana. Gene 212:147-153.
9. Bourgis, F., S. Roje, M.L. Nuccio, D.B. Fisher, M.C. Tarczynski, C.J. Li, C. Herschbach, H. Rennenberg, M.J. Pimenta, T.L. Shen, D.A. Gage, and A.D. Hanson. 1999. S-methylmethionine plays a major role in phloem sulfur transport and is synthesized by a novel type of methyltransferase. Plant Cell 11:1485-1497.
10. Bryan, J.K. 1990. Advances in the biochemistry of amino acid biosynthesis. p. 161-196. In B.J. Mifl in (ed.) The biochemistry of plants. Vol. 5. Academic Press, New York.
11. Bryan, J.K. 1980. Synthesis of the aspartate family and branched-chain amino acids. p. 403-452. In B.J. Mifl in (ed.) The biochemistry of plants. Vol. 5. Academic Press, New York.
12. Buchner, P., C.E.E. Stuiver, S. Westerman, M. Wirtz, R. Hell, M.J. Hawkesford, and L.J. de Kok. 2004a. Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as aff ected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiol. 136:3396-3408.
13. Buchner, P., H. Takahashi, and M.J. Hawkesford. 2004b. Plant sulfate transporters: Co-ordination of uptake, intracellular and long distance transport. J. Exp. Bot. 55:1765-1773.
14. Burandt, P., A. Schmidt, and J. Papenbrock. 2002. Three O-acetyl-L-serine(thiol)lyase isoenzymes from Arabidopsis catalyse cysteine synthesis and cysteine desulfuration at diff erent pH values. J. Plant Physiol. 159:111-119.
15. Chiaiese, P., N. Ohkama-Ohtsu, L. Molvig, R. Godfree, H. Dove, C. Hocart, T. Fujiwara, T.J.V. Higgins, and L.M. Tabe. 2004. Sulphur and nitrogen nutrition infl uence the response of chickpea seeds to an added, transgenic sink for organic sulphur. J. Exp. Bot. 55:1889-1901.
16. Chi-Ham, C.L., M.A. Keaton, G.C. Cannon, and S. Heinhorst. 2002. The DNA-compacting protein DCP68 from soybean chloroplasts is ferredoxin: Sulfi te reductase and co-localizes with the organellar nucleoid. Plant Mol. Biol. 49:621-631.
17. de Kok, L.J., M. Durenkamp, L. Yang, and I. Stulen. 2007. Atmospheric sulfur. p. 91-1006. In M.J. Hawkesford and L.J. de Kok (ed.) Sulfur in plants: An ecological perspective. Springer, Dordrecht, the Netherlands.
18. Dominguez-Solis, J., G. Gutierrez-Alcala, L. Romero, and C. Gotor C. 2001. The cytosolic O-acetylserine(thiol)lyase gene is regulated by heavy metals and can function in cadmium tolerance. J. Biol. Chem. 276:9297-9302.
19. Droux, M. 2003. Plant serine acetyltransferase: New insights for regulation of sulphur metabolism in plant cells. Plant Physiol. Biochem. 41:619-627.
20. Droux, M. 2004. Sulfur assimilation and the role of sulfur in plant metabolism: A survey. Photosynth. Res. 79:331-348.
21. Droux, M., M.-L. Ruff et, R. Douce, and D. Job. 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.
22. Durenkamp, M., and L.J. de Kok. 2004. Impact of pedospheric and atmospheric sulphur nutrition on sulphur metabolism of Allium cepa L., a species with a potential sink capacity for secondary sulphur compounds. J. Exp. Bot. 55:1821-1830.
23. Durenkamp, M., L.J. de Kok, and S. Kopriva S. 2007. Adenosine 5′-phosphosulphate reductase is regulated diff erently in Allium cepa L. and Brassica oleracea L. upon exposure to H2S. J. Exp. Bot 58:1571-1579.
24. Francois, J.A., S. Kumaran, and J.M. Jez. 2006. Structural basis for interaction of O-acetylserine sulfh ydrylase and serine acetyltransferase in the Arabidopsis cysteine synthase complex. Plant Cell 18:3647-3655.
25. Frentzen, M. 2004. Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: Anionic membrane lipids and phosphate regulation. Curr. Opin. Plant Biol. 7:270-276.
26. Galili, G., R. Amir, R. Hoefgen, and H. Hess. 2005. Improving the levels of essential amino acids and sulfur metabolites in plants. Biol. Chem. 386:817-831.
27. Galili, G., and R. Hoefgen. 2002. Metabolic engineering of amino acids and storage proteins in plants. Metab. Eng. 4:3-11.
28. Grossman, A., and H. Takahashi. 2001. Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annu. Rev. Plant. Phys. Plant. Mol. Biol. 52:163-210.
29. Hagan, N.D., N. Upadhyaya, L.M. Tabe, and T.J.V. Higgins. 2003. The redistribution of protein sulfur in transgenic rice expressing a gene for a foreign, sulfur-rich protein. Plant J. 34:1-11.
30. Halkier, B.A., and J. Gershenzon. 2006. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57:303-333.
31. Haneklaus, S., E. Bloem, and E. Schnug. 2003. The global sulfur cycle and its links to plant environment. p. 1-28. In Y.P. Abrol and A. Ahmad (ed.) Sulfur in plants. Kluwer Academic Publishers, Dordrecht, the Netherlands.
32. Hänsch, R., C. Lang, H. Rennenberg, and R.R. Mendel. 2007. Signifi cance of plant sulfi te oxidase. Plant Biol. 9:589-595.
33. Hänsch, R., and R.R. Mendel. 2005. Sulfi te oxidation in plant peroxisomes. Photosynth. Res. 86:337-343.
34. Harms, K., P. von Ballmoos, C. Brunold, R. Hoefgen, and H. Hesse. 2000. Expression of a bacterial serine acetyltransferase in transgenic potato plants leads to increased levels of cysteine and glutathione. Plant J. 22:335-343.
35. Hatzfeld, Y., N. Cathala, C. Grignon, and J.C. Davidian. 1998. Eff ect of ATP sulfurylase overexpression in Bright Yellow 2 tobacco cells-regulation of ATP sulfurylase and SO4 2- transport activities. Plant Physiol. 116:1307-1313.
36. Hawkesford, M.J. 2000. Plant responses to sulphur defi ciency and the genetic manipulation of sulphate transporters to improve S-utilization effi ciency. J. Exp. Bot. 51:131-138.
37. Hawkesford, M.J. 2003. Transporter gene families in plants: The sulfate transporter gene family-Redundancy or specialization? Physiol. Plant. 117:155-163.
38. Hawkesford, M.J. 2007. Sulfur and Plant ecology: A central role of sulfate transportersin response to sulfur availability. p. 61-79. In M.J. Hawkesford and L.J. de Kok (ed.) Sulfur in plants: An ecological perspective. Springer, Dordrecht, the Netherlands.
39. Hawkesford, M.J., P. Buchner, L. Hopkins, and J.R. Howarth. 2003. The plant sulfate transporter family: Specialized functions and integration with whole plant nutrition. p. 1-10. In J.C. Davidian et al. (ed.) Sulfur transport and assimilation in plants-Regulation, interaction and signaling. Backhuys Publishers, Leiden, the Netherlands.
40. Hawkesford, M.J., and L.J. de Kok. 2006. Managing sulphur metabolism in plants. Plant Cell Environ. 29:382-395.
41. Hawkesford, M., R. Hoefgen, G. Galili, R. Amir, G. Angenon, H. Hesse, D. Rentsch, J. Schaller, I. Van der Meer, J. Rouster, Z. Banfalvi, P. Zsolt, L. Szabados, J. Szopa, and A. Sirko. 2006. Optimising nutritional quality of crops. p. 85-116. In P.K. Jaiwal (ed.) Plant genetic engineering. Vol. 7, Plant metabolic engineering and molecular farming. Studium Press LLC, Houston, TX.
42. Hell, R. 1997. Molecular physiology of plant sulfur metabolism. Planta 202:138-148.
43. Hell, R., R. Jost, O. Berkowitz, and M. Wirtz. 2002. Molecular and biochemical analysis of the enzymes of cysteine biosynthesis in the plant Arabidopsis thaliana. Amino Acids 22:245-257.
44. Hell, R., and H. Rennenberg. 1998. The plant sulfur cycle. Sulfur Agroecosys. 2:135-173.
45. Hesse, H., and R. Hoefgen. 2006. On the way to understand biological complexity in plants: S-nutrition as a case study for systems biology. Cell. Mol. Biol. Lett. 11:37-55.
46. Hesse, H., and R. Hoefgen. 2001. Application of genomics in agriculture. p. 61-79. In M.J. Hawkesford and P. Buchner (ed.) Molecular analysis of plant adaptation to the environment. Kluwer AP, Dordrecht, the Netherlands.
47. Hesse, H., and R. Hoefgen. 2003. Molecular aspects of methionine biosynthesis in Arabidopsis and potato. Trends Plant Sci. 8:259-262.
48. Hesse, H., O. Kreft, S. Maimann, M. Zeh, and R. Hoefgen. 2004b. Current understanding of the regulation of methionine biosynthesis in plants. J. Exp. Bot. 55:1799-1808.
49. Hesse, H., J. Lipke, T. Altmann, and R. Hoefgen. 1999. Molecular cloning and expression analysis of mitochondrial and plastidic isoforms of cysteine synthase (O-acetylserine (thiol)lyase) from Arabidopsis thaliana. Amino Acids 16:113-131.
50. Hesse, H., V. Nikiforova, B. Gakière, and R. Hoefgen. 2004a. Molecular analysis and control of cysteine biosynthesis: Integration of nitrogen and sulfur metabolism. J. Exp. Bot. 55:1283-1292.
51. Hesse, H., N. Trachsel, M. Suter, S. Kopriva, P. von Ballmoos, H. Rennenberg, and C. Brunold. 2003. Eff ect of glucose on assimilatory sulphate reduction in Arabidopsis thaliana roots. J. Exp. Bot. 54:1701-1709.
52. Hirai, M.Y., T. Fujiwara, M. Awazuhara, T. Kimura, N. Masaaki, and K. Saito. 2003. Global expression profi ling 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.
53. Hirai, M.Y., M. Klein, Y. Fujikawa, M. Yano, D.B. Goodenowe, Y. Yamazaki, S. Kanaya, Y. Nakamura, M. Kitayama, H. Suzuki, N. Sakurai, D. Shibata, J. Tokuhisa, M. Reichelt, J. Gershenzon, J. Papenbrock, and K. Saito. 2005. Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J. Exp. Biol. Chem. 280:25590-25595.
54. Hirai, M.Y., and K. Saito. 2004. Post-genomics approaches for the eleucidation of plant adaptive mechanisms to sulphur defi ciency. J. Exp. Bot. 55:1871-1879.
55. Ho, C.L., and K. Saito. 2001. Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana. Amino Acids 20:243-259.
56. Hoefgen, R., and H. Hesse. 2007. Sulfur in plants as part of a metabolic network. p. 107-142. In M.J Hawkesford and L.J. de Kok (ed.) Sulfur in plants: An ecological perspective. Springer, Dordrecht, the Netherlands.
57. Hoefgen, R., O. Kreft, L. Willmitzer, and H. Hesse. 2001. Manipulation of thiol contents in plants. Amino Acids 20:291-299.
58. Hopkins, L., S. Parmar, A. Blaszczyk, H. Hesse, R. Hoefgen, and M.J. Hawkesford. 2005. O-acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol. 138:433-440.
59. Kataoka, T., N. Hayashi, T. Yamaya, and H. Takahashi. 2004a. Root-to-shoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affi nity sulfate transport system in the root vasculature. Plant Physiol. 136:4198-4204.
60. Kataoka, T., A. Watanabe-Takahashi, N. Hayashi, M. Ohnishi, T. Mimura, P. Buchner, M.J. Hawkesford, T. Yamaya, and H. Takahashi. 2004b. Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693-2704.
61. Kertesz, M.A., and P. Mirleau. 2004. The role of microbes in plant sulphur nutrition. J. Exp. Bot. 55:1939-1945.
62. Kessler, D., and J. Papenbrock. 2005. Iron-sulfur cluster biosynthesis in photosynthetic organisms. Photosynth. Res. 86:391-407.
63. Klein, M., and J. Papenbrock. 2004. The multi-protein family of Arabidopsis sulphotransferases and their relatives in other plant species. J. Exp. Bot. 55:1809-1820.
64. Klonus, D., R. Hoefgen, L. Willmitzer, and J.W. Riesmeier. 1994. Isolation and characterization of two cDNA clones encoding ATP-sulfurylases from potato by complementation of a yeast mutant. Plant J. 6:105-112.
65. Kopriva, S. 2006. Regulation of sulfate assimilation in Arabidopsis and beyond. Ann. Bot. (Lond.) 97:479-495.
66. Kopriva, S., and A. Koprivova. 2004. Plant adenosine 5′-phosphosulphate reductase: The past, the present, and the future. J. Exp. Bot. 55:1775-1783.
67. Kopriva, S., and H. Rennenberg. 2004. Control of sulphate assimilation and glutathione synthesis: Interaction with N and C metabolism. J. Exp. Bot. 55:1831-1842.
68. Kopriva, S., M. Suter, P. von Ballmoos, H. Hesse, U. Krahenbuhl, H. Rennenberg, and C. Brunold. 2002. Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol. 130:1406-1413.
69. Koralewska, A., F.S. Posthumus, C.E.E. Stuiver, P. Buchner, M.J. Hawkesford, and L.J. De Kok. 2007. The characteristic high sulfate content in Brassica oleracea is controlled by the expression and activity of sulfate transporters. Plant Biol. 9:654-661.
70. Kredich, N.M. 1996. Biosynthesis of cysteine in Escherichia coli and Salmonella typhimurium. p. 514-527. In F.C. Neidhardt et al. (ed.) Cellular and molecular biology. ASM Press, Washington, DC.
71. Kredich, N.M., M.A. Becker, and G.M. Tomkin. 1969. Purifi cation and characterization of cysteine synthetase, a bifunctional protein complex, from Salmonella typhimurium. J. Biol. Chem. 244: 2428-2439.
72. Kreft, O., R. Hoefgen, and H. Hesse. 2003. Functional Analysis of cystathionine gammasynthase in genetically engineered potato plants. Plant Physiol. 131:1843-1854.
73. Kumaran, S., and J.M. Jez. 2007. Thermodynamics of the interaction between O-acetylserine sulfh ydrylase and the C-terminus of serine acetyltransferase. Biochemistry 46:5586-5594.
74. Lang, C., Popko, M. Wirtz, R. Hell, C. Herschbach, J. Kreuzwieser, H. Rennenberg, R.R. Mendel, and R. Hänsch. 2007. Sulphite oxidase as key enzyme for protecting plants against sulphur dioxide. Plant Cell Environ. 30:447-455.
75. Leustek, T., M.N. Martin, J.A. Bick, and J.P. Davies. 2000. Pathways and regulation of sulphur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:141-165.
76. Leustek, T., and K. Saito. 1999. Sulfate transport and assimilation in plants. Plant Physiol. 120:637-643.
77. Lillig, C.H., S. Schiff mann, C. Berndt, A. Berken, R. Tischka, and J.D. Schwenn. 2001. Molecular and catalytic properties of Arabidopsis thaliana adenylyl sulfate (APS)-kinase. Arch. Biochem. Biophys. 392:303-310.
78. Lorbiecke, R., M. Steff ens, J.M. Tomm, S. Scholten, P. von Wiegen, E. Kranz, U. Wienand, and M. Sauter. 2005. Phytosulphokine gene regulation during maize (Zea mays L.) reproduction. J. Exp. Bot. 56:1805-1819.
79. Loudet, O., V. Saliba-Colombani, C. Camilleri, F. Calenge, V. Gaudon, A. Koprivova, A.K. North, S. Kopriva, and F. Daniel-Vedele. 2007. Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat. Genet. 39:896-900.
80. Maimann, S., C. Wagner, O. Kreft, M. Zeh, L. Willmitzer L, R. Hoefgen R, and H. Hesse. 2000. Transgenic potato plants reveal the indispensable role of cystathionine ?-lyase in plant growth and development. Plant J. 23:747-758.
81. Maruyama-Nakashita, A., E. Inoue, A. Watanabe-Takahashi, T. Yarnaya, and H. Takahashi. 2003. Transcriptome profi ling of sulfur-responsive genes in Arabidopsis reveals global eff ects of sulfur nutrition on multiple metabolic pathways. Plant Physiol. 132:597-605.
82. Maruyama-Nakashita, A., Y. Nakamura, T. Yamaya, and H. Takahashi. 2004. Regulation of high-affi nity sulfate transporters in plants: Towards systematic analysis of sulfur signalling and regulation. J. Exp. Bot. 55:1843-1849.
83. Maruyama-Nakashita, A., A. Watanabe-Takahashi, E. Inoue, T. Yarnaya, and H. Takahashi. 2005. Identifi cation of a novel cis-acting element conferring sulfur defi ciency response in Arabidopsis roots. Plant J. 42:305-314.
84. Matityahu, I., L. Kachan, I.B. Ilan, and R. Amir. 2006. Transgenic tobacco plants overexpressing the Met25 gene of Saccharomyces cerevisiae exhibit enhanced levels of cysteine and glutathione and increased tolerance to oxidative stress. Amino Acids 30:185-194.
85. Matt hews, B. 1999. Lysine, threonine and methionine biosynthesis. p. 205-225. In B.K. Singh (ed.) Plant amino acids. Marcel Dekker, New York.
86. Melis, A., and H.C. Chen. 2005. Chloroplast sulfate transport in green algae- genes, proteins and eff ects. Photosynth. Res. 86:299-307.
87. Mendel, R.R. 2007. Biology of the molybdenum cofactor. J. Exp. Bot. 58:2289-2296.
88. Molvig, L., L.M. Tabe, J. Hamblin, V. Ravindran, W.L. Bryden, C.L. White, and T.J.V. Higgins. 2003. Nutritional improvement of lupin seed protein using gene technology. Appl. Gen. Legumin. Biotech. 10:213-219.
89. Nikiforova, V.J., C.O. Daub, H. Hesse, L. Willmitzer, and R. Hoefgen. 2005b. Integrative gene-metabolite network with implemented causality deciphers informational fl uxes of sulfur stress response. J. Exp. Bot. 56:1887-1896.
90. Nikiforova, V., J. Freitag, S. Kempa, M. Adamik, H. Hesse, and R. Hoefgen. 2003. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: Interlacing of biosynthetic pathways provides response specifi city. Plant J. 33:633-650.
91. Nikiforova, V.J., B. Gakière B, S. Kempa, M. Adamik, L. Willmitzer L, H. Hesse, and R. Hoefgen. 2004. Towards dissecting nutrient metabolism in plants: A systems biology case study on sulfur metabolism. J. Exp. Bot. 55:1861-1870.
92. Nikiforova, V., S. Kempa, M. Zeh, S. Maimann, O. Kreft, A.P. Casazza, K. Riedel, E. Tauberger, R. Hoefgen, and H. Hesse. 2002. Engineering of cysteine and methionine biosynthesis in potato. Amino Acids 22:259-278.
93. Nikiforova, V.J., J. Kopka, V. Tolstikov, O. Fiehn, L. Hopkins, M.J. Hawkesford, H. Hesse, and R. Hoefgen. 2005a. Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol. 138:304-318.
94. Papenbrock, J., A. Riemenschneider, A. Kamp, H.N. Schulz-Vogt, and A. Schmidt. 2007. Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants-From the fi eld to the test tube and back. Plant Biol. 9:582-588.
95. Pilon-Smits, E.A.H., S.B. Hwang, C.M. Lytle, Y.L. Zhu, J.C. Tai, R.C. Bravo, Y.C. Chen, T. Leustek, and N. Terry. 1999. Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol. 119:123-132.
96. Ranocha, P., S.D. McNeil, M.J. Ziemak, C.J. Li, M.C. Tarczynski, and A.D. Hanson. 2001. The S-methylmethionine cycle in angiosperms: Ubiquity, antiquity and activity. Plant J. 25:575-584.
97. Rébeillé, F., S. Ravanel, S. Jabrin, R. Douce, S. Storozhenko, and D. Van Der Straeten. 2006. Folates in plants: Biosynthesis, distribution, and enhancement. Physiol. Plant. 126:330-342.
98. Riemenschneider, A., K. Riedel, R. Hoefgen, J. Papenbrock, and H. Hesse. 2005. Impact of reduced O-acetylserine(thiol)lyase isoform contents on potato plant metabolism. Plant Physiol. 137:892-900.
99. Rouached, H., P. Berthomieu, E. El Kassis, N. Cathala, V. Catherinot, G. Labesse, J.C. Davidian, and P. Fourcroy. 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.
100. Saito, K. 2000. Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Plant Biol. 3:188-195.
101. Saito, K. 2004. Sulfur assimilatory metabolism. The long and smelling road. Plant 136:2443-2450.
102. Saito, K. 2008. Decoding genes with coexpression networks and metabolomics- ‘majority report by precogs’. Trends Plant Sci. 13:36-43.
103. Saito, K., M. Kurosawa, K. Tatsuguchi, Y. Takagi, and I. Murakoshi. 1994. Modulation of cysteine biosynthesis in chloroplasts of transgenic tobacco overexpressing cysteine synthase [O-acetylserine(thiol)-lyase]. Plant Physiol. 106:887-895.
104. Sanda, S., T. Leustek, M.J. Theisen, R.M. Garavito, and C. Benning. 2001. Recombinant Arabidopsis SQD1 converts UDP-glucose and sulfi te to the sulfolipid head group precursor UDP-sulfoquinovose in vitro. J. Biol. Chem. 276:3941-3946.
105. Schwenn, J.D. 1994. Photosynthetic sulfate reduction. Z. Natforsch. C-A. J. Biosci. 49:531-539.
106. Sekine, K., M. Fujiwara, M. Nakayama, T. Takao, T. Hase, and N. Sato. 2007. DNA binding and partial nucleoid localization of the chloroplast stromal enzyme ferredoxin: Sulfi te reductase. FEBS J. 274:2054-2069.
107. Sekine, K., T. Hase, and N. Sato. 2002. Reversible DNA compaction by sulfi te reductase regulates transcriptional activity of chloroplast nucleoids. J. Biol. Chem. 277:24399-24404.
108. Setya, A., M. Murillo, and T. Leustek. 1996. Sulfate reduction in higher plants- molecular evidence for a novel 5′-adenylylsulfate reductase. Proc. Natl. Acad. Sci. USA 93:13383-13388.
109. Shibagaki, N., A. Rose, J. Mcdermott, T. Fujiwara, H. Hayashi, T. Yoneyama, and J. Davies. 2002. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for effi cient transport of sulfate into roots. Plant J. 29:475-486.
110. Stefels, J. 2007. Sulfur in the marine environment. p. 77-90. In M.J Hawkesford and L.J. de Kok (ed.) Sulfur in plants: An ecological perspective. Springer, Dordrecht, the Netherlands.
111. Stiller, I., G. Dancs, H. Hesse, R. Hoefgen, and Z. Banfalvi. 2007. Improving the nutritive value of tubers: Elevation of cysteine and glutathione contents in the potato cultivar White Lady by marker-free transformation. J. Biotechnol. 128:335-343.
112. Suter, M., P. von Ballmoos, S. Kopriva, R.O. den Camp, J. Schaller, C. Kuhlemeier, P. Schurmann, and C. Brunold. 2000. Adenosine 5′-phosphosulfate sulfotransferase and adenosine 5¢-phosphosulfate reductase are identical enzymes. J. Biol. Chem. 275:930-936.
113. Tejada-Jimenez, M., A. Llamas, E. Sanz-Luque, A. Galvan, and E. Fernandez. 2007. A high-affi nity molybdate transporter in eukaryotes. Proc. Natl. Acad. Sci. USA 104:20126-20130.
114. Tomatsu, H., J. Takano, H. Takahashi, A. Watanabe-Takahashi, N. Shibagaki, and T. Fujiwara. 2007. An Arabidopsis thaliana high-affi nity molybdate transporter required for effi cient uptake of molybdate from soil. Proc. Natl. Acad. Sci. USA 104:18807-18812.
115. Tsakraklides, G., M. Martin, R. Chalam, M.C. Tarczynski, A. Schmidt, and T. Leustek. 2002. CSulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5′-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J. 32:879-889.
116. Wirtz, M., and M. Droux. 2005. Synthesis of the sulfur amino acids: Cysteine and methionine. Photosynth. Res. 86:345-362.
117. Wirtz, M., M. Droux, and R. Hell. 2004. O-acetylserine(thiol)lyase: An enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J. Exp. Bot. 55:1785-1798.
118. Wirtz, M., and R. Hell. 2006. Functional analysis of the cysteine synthase protein complex from plants: Structural, biochemical and regulatory properties. Plant Physiol. 163:273-286.
119. Wirtz, M., and R. Hell. 2007. Dominant-negative modifi cation reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19:625-639.
120. Yoshimoto, N., E. Inoue, K. Saito K, T. Yamaya, and H. Takahashi. 2003. Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol. 131:1511-1517.
121. Yoshimoto, N., E. Inoue, A. Watanabe-Takahashi, K. Saito, and H. Takahashi. 2007. Postt ranscriptional regulation of high-affi nity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol. 145:378-388.
122. Yoshimoto, N., H. Takahashi, F.W. Smith, T. Yamaya, and K. Saito. 2002. Two distinct highaffi nity sulfate transporters with diff erent inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J. 29:465-473.
123. Youssefi an, S., M. Nakamura, E. Orudgev, and N. Kondo. 2001. Increased cysteine biosynthesis capacity of transgenic tobacco overexpressing an O-acetylserine(thiol) lyase modifi es plant responses to oxidative stress. Plant Physiol. 126:1001-1011.
124. Youssefi an, S., M. Nakamura, and H. Sano. 1993. Tobacco plants transformed with the O-acetylserine(thiol) lyase gene of wheat are resistant to toxic levels of hydrogen sulphide gas. Plant J. 4:759-769.
125. Zeh, M., A.P. Casazza, O. Kreft, U. Roessner, K. Bieberich, L. Willmitzer, R. Hoefgen, and H. Hesse. 2001. Antisense inhibition of threonine synthase leads to high methionine content in transgenic potato plants. Plant Physiol. 127:792-802.
126. Zeh, M., G. Leggewie, R. Hoefgen, and H. Hesse. 2002. Cloning and characterization of a cDNA encoding a cobalamin-independent methionine synthase from potato (Solanum tuberosum L.). Plant Mol. Biol. 48:255-265.