Abstract
This chapter describes the physiological and biochemical background of sulphate transport in relation to current molecular approaches. Following identification and isolation of the first plant gene encoding H+/sulphate co-transporter, a large gene family has now been identified. Phylogenetic analysis of this gene family suggests a specialisation of function of subgroups defined by the patterns of gene expression and tissue, cellular and sub-cellular localisation. Functional characteristics of the cloned transporters have been determined by expression in a heterologous yeast expression system, utilising sulphate transporter deficient mutants. A range of affinity constants for sulphate has been determined. An analysis of conserved amino acids together with site-directed mutagenesis indicates residues of probable functional importance.
The control of sulphate uptake and assimilation can be described by a model of a ‘highly regulated circuit’, mediated by feedback loops involving key metabolites of cysteine biosynthesis. In this model, expression of genes involved in uptake and assimilation are under positive regulation by O-acetylserine, which accumulates when insufficient sulphide is available to utilise the O-acetylserine for cysteine synthesis. This modulates the activity of the serine acetyltransferase/O-acetylserine-thiol-lyase complex. A negative feedback mechanism, mediated by reduced S-compounds may also act at the level of gene expression.
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References
Aravind L and Koonin EV (2000) The STAS domain–a link between anion transporters and antisigma-factor antagonists. Curr Biol 10: R53–55
Biedlingmaier S and Schmidt A (1989) Sulfate transport in normal and S-deprived Chlorella fusca. Z Naturforsch 44: 495–503
Bolchi A, Petrucco S, Tenca PL, Foroni C and Ottonello S (1999) Coordinate modulation of maize permease and ATP sulpfurylase mRNAs in response to variations in sulfur nutritional status: stereospecific down-regulation by L-cysteine. Plant Mol Biol 39: 527–537
Bourgis F, Roje S, Nuccio ML, Fisher DB, Tarczynski MC, Li CJ, Herschbach C, Rennenberg H, Pimenta MJ, Shen TL, Gage DA and Hanson AD (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
Brandl CJ and Deber CM (1986) Hypothesis about the function of membrane-buried proline residues in transport proteins. Proc Nat Acad Sci USA 83: 917–921
Breton A and Surdin-Kerjan Y (1977) Sulfate uptake in Saccharomyces cerevisiae: biochemical and genetic study. J Bacteriol 132: 224–232
Clarkson DT, Smith FW and Vandenberg PJ (1983) Regulation of sulfate transport in a tropical legume, Macroptilium atropurpureum cv Sirato. JExp Bot 34: 1463–1483
Clarkson DT, Hawkesford MJ, Davidian J-C and Grignon C (1992) Contrasting responses of sulfate and phosphate-transport in barley (Hordeum vulgare L) roots to protein-modifying reagents and inhibition of protein-synthesis. Planta 187: 306–314
Datko AH and Mudd SH (1984) Sulfate uptake and its regulation in Lemna paucicostata Hegelm.6746. Plant Physiol 75: 466–473
Davies JP, Yildiz F and Grossman AR (1994) Mutants of Chlamydomonas with aberrant responses to sulfur deprivation. Plant Cell 6: 53–63
Davies JP, Yildiz FH and Grossman A (1996) Sac 1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15: 2150–2159
Davies JP, Yildiz FH and Grossman AR (1999) Sac3, an Snfl-like serine/threonine kinase that positively and negatively regulates the responses of Chlamydomonas to sulfur limitation. Plant Cell 11: 1179–1190
Gede I, Adiputra K and Anderson JW (1995) Effect of sulphur nutrition on redistribution of sulphur in vegetative barley. Physiol Plant 95: 643–650
Hästbacka J, de la Chapelle A, Mahtani MM, Clines G, Reeve-Daly MP, Daly M, Hamilton BA, Kusumi K, Trivedi B, Weaver A, Coloma A, Lovett M, Buckler A, Kaitila I and Lander ES (1994) The diastrophic dysplasia gene encodes a novel sulfate transporter: positional cloning by fine-structure linkage disequilibrium mapping. Cell 78: 1073–1087
Hatzfeld Y, Cathala N, Grignon C and Davidian J-C (1998) Effect of ATP sulfurylase overexpression in Bright Yellow 2 tobacco cells. Regulation of ATP sulfurylase and sulphate transport activities. Plant Physiol 116: 1307–1313
Hawkesford MJ (2000) Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S-utilisation efficiency. J Exp Bot 51: 131–138
Hawkesford MJ and Smith FW (1997) Molecular biology of higher plant sulphate transporters. In: Cram WJ, De Kok LJ, Stulen I, Brunold C and Rennenberg H (eds) Sulphur Metabolism in Higher Plants, pp 13 25. Backhuys Publishers, Leiden
Hawkesford MJ and Wray JL (2000) Molecular genetics of sulphur assimilation. Adv Bot Res 33: 159–223
Hawkesford MJ, Davidian J-C and Grignon C (1993) Sulfate proton cotransport in plasma membrane vesicles isolated from roots of Brassica napus L. Increased transport in membranes isolated from sulfur-starved plants. Planta 190: 297–304
Heiss S, Schäfer HJ, 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
Herschbach C and Rennenberg H (1994) Influence of glutathione (GSH) on net uptake of sulfate and sulfate transport in tobacco plants. JExp Bot 45: 1069–1076
Jones SL and Smith IK (1981) Sulfate transport in cultured tobacco cells. Effects of calcium and sulfate concentration. Plant Physiol. 67: 445–448
Khurana OK, Coupland LA, Shelden MC and Howitt SM (2000) Homologous mutations in two diverse sulphate transporters have similar effects. FEBS Lett 477: 118–122
Kredich NM (1992) The molecular basis for positive regulation of cys promoters in Salmonella typhimurium and Escherichia coli. Mol Microbiol 6: 2747–2753
Kredich NM (1993) Gene regulation of sulfur assimilation. In: De Kok LJ, Stulen I, Rennenberg H, Brunold C and Rauser WE (eds) Sulfur Nutrition and Assimilation in Higher Plants, pp 37–47. SPB Academic Publishers, The Hague Lappartient AG and Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and sulfate uptake in intact canola. Plant Physiol 111: 147–157
Lappartient AG, Vidmar JJ, Leustek T, Glass ADM and Touraine B (1999) Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloemtranslocated compound. Plant J 18: 89–95
Lee RB (1982) Selectivity and kinetics of ion uptake by barley plants following nutrient deficiency. Ann Bot 50: 429–449
Leggett JE and Epstein E (1956) Kinetics of sulfate absorption by barley roots. Plant Physiol 31: 222–226
Logan HM, 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. Expression studies in yeast and in relation to plant sulfur nutrition. JBiol Chem 271: 12227–12233
Neuenschwander U, Suter M and Brunold C (1991) Regulation of sulfate assimilation by light and O-acetylL-serine in Lemna minor L. Plant Physiol 97: 253–258
Ng AYN, Blomstedt CK, Gianello R, Hamill JD, Neale AD and Gaff DF (1996) Isolation and characterisation of a lowly expressed cDNA from the resurrection grass Sporobolus stapfianus with homology to eukaryotic sulfate transporter proteins (Acc. No. X96761) (PGR96–032). Plant Physiol 111: 651
Nissen P (1971) Uptake of sulfate by roots and leaf slices of barley: mediated by single, multiphasic mechanisms. Physiol Plant 24: 315–324
Passera C and Ferretti M (1988) Sulphate uptake by leaf mesophyll and bundle sheath cells of maize plants. Biol Plant 30: 451–456
Reizer J, Reizer A and Saier MH (1994) A functional superfamily of sodium/solute symporters. Biochim Biophys Acta 1197: 133–166
Rennenberg H, Schmitz K and Bergmann L (1979) Long-distance transport of sulfur in Nicotiana tabacum. Planta 147: 57–62
Shelden MC, Loughlin P, Tiemey ML and Howitt SM (2001) Proline residues in two tightly coupled helices of the sulphate transporter, SHST1, are important for sulphate transport. Biochem J356: 589–594 Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yomeyama T and Davis JP (2002) Selenateresistant mutants of Arabidopsis thaliana identify Sultrl; 2,a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29: 475–486
Smith FW, Ealing, PM, Hawkesford MJ and Clarkson DT (1995a) Plant members of a family of sulfate transporters reveal functional subtypes. Proc Nat Acad Sci USA 92: 9373–9377
Smith FW, Hawkesford M.1, Prosser IM and Clarkson DT (1995b) Isolation of a cDNA from Saccharomyces cerevisiae that encodes a high affinity sulphate transporter at the plasma membrane. Mol Gen Genet 247: 709–715
Smith FW, Hawkesford MJ, Ealing PM, Clarkson, DT, Vandenberg PJ, Belcher A and Warrilow AGS (1997) Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J 12: 875–884
Smith IK (1975) Sulfate transport in cultured tobacco cells. Plant Physiol 55: 303–307
Takahashi H, Sasakura N, Noji M and Saito K (1996) Isolation and characterization of a cDNA encoding a sulfate transporter from Arabidopsis thaliana. FEBS Lett 392: 95–99
Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, de Almeida Engler J, Engler G, van Montagu M and Saito K (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
Takahashi H, Asanuma W and Saito K (1999a) Cloning of an Arabidopsis cDNA encoding a chloroplast localizing sulphate transporter isoform. J Exp Bot 50: 1713–1714
Takahashi H, Sasakura N, Kimura A, Watanabe A and Saito K (1999b) Identification of two leaf-specific sulfate transporters in Arabidopsis thaliana (Ace. No. ABO12048 and AB004060) (PGR99–154). Plant Physiol 121: 686
Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalf M, Hawkesford MJ 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
Vange MS, Holmem K and Nissen P (1974) Mutiphasic uptake of sulfate by barley roots. I. Effects of analogues, phosphate, and pH. Physiol Plant 31: 292–301
Vidmar JJ, Schjoerring JK, Touraine B and Glass ADM (1999) Regulation of the hvstl gene encoding a high-affinity sulfate transporter from Hordeum volgare. Plant Mol Biol 40: 883–892
Vidmar JJ, Tagmount A, Cathala N, Touraine B and Davidian J-C (2000) Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. FEBS Lett 475: 65–69
von Heijne G (1992) Membrane-protein structure prediction-hydrophobicity analysis and the positive-inside rule. J Mol Biol 225: 487–494
Yildiz FH, Davies JP and Grossman A (1996) Sulfur availability and the SAC] gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii. Plant Physiol 112: 669–675
Yoshimoto N, Takahashi H, Smith FW, Yamaya T and Saito K (2002) Two distinct high-affinity sulfate tran sporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29: 465–473
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Hawkesford, M.J., Buchner, P., Hopkins, L., Howarth, J.R. (2003). Sulphate Uptake and Transport. In: Abrol, Y.P., Ahmad, A. (eds) Sulphur in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-0289-8_4
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DOI: https://doi.org/10.1007/978-94-017-0289-8_4
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