Skip to main content
SpringerLink
Log in

Sulfate Transport

  • Chapter
  • First Online:
Book cover The Plant Plasma Membrane

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 19))

Abstract

The SulP gene family in plants consists of approximately 14 genes, depending on species, of which around 10 are thought to encode plasma membrane sulfate transporters. On the basis of sequence, five clades or Groups are distinguishable, of which three contain probable plasma membrane sulfate transporters. Isoforms with both high (Group 1) and low affinities (Group 2) for sulfate catalyse cellular uptake in many tissues throughout the plant, particularly at the soil/root interface, and in vascular tissues, respectively. Differential expression of the individual isoforms in response to sulfur nutrition, and in relation to tissue specificity, optimises the uptake and distribution of sulfate depending upon supply and demand. A major contribution to regulation is at the transcriptional level, with transcript abundance and sulfate uptake capacity increasing markedly when sulfur supply is limiting. The sulfate transporters comprise 12 MSDs with long amino and carboxyl regions, the latter containing a STAS domain, which may be involved in functional regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aravind L, Koonin EV (2000) The STAS domain – a link between anion transporters and antisigma-factor antagonists. Curr Biol 10:R53–R55

    Article  PubMed  CAS  Google Scholar 

  • Baxter I, Muthukumar B, Park HC, Buchner P, Lahner B, Danku J, Zhao K, Lee J, Hawkesford MJ, Guerinot ML, Salt DE (2008) Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet 4:e1000004

    Article  PubMed  Google Scholar 

  • Buchner P, Prosser IM, Hawkesford MJ (2004a) Phylogeny and expression of paralogous and orthologous sulphate transporter genes in diploid and hexaplold wheats. Genome 47:526–534

    Article  PubMed  CAS  Google Scholar 

  • Buchner P, Stuiver CEE, Westerman S, Wirtz M, Hell R, Hawkesford MJ, De Kok LJ (2004b) Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiol 136:3396–3408

    Article  PubMed  CAS  Google Scholar 

  • Buchner P, Parmar S, Kriegel A, Carpentier M, Hawkesford MJ (2010) The sulphate transporter gene family in wheat: tissue-specific gene expression in relation to nutrition. Molec Plant 3:374–389

    Article  CAS  Google Scholar 

  • Clarkson DT, Smith FW, Vandenberg PJ (1983) Regulation of sulfate transport in a tropical legume, Macroptilium atropurpureum, cv Siratro. J Exp Bot 34:1463–1483

    Article  CAS  Google Scholar 

  • Clarkson DT, Hawkesford MJ, Davidian J-C, 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

    Article  CAS  Google Scholar 

  • Diatloff E, Roberts M, Sanders D, Roberts SK (2004) Characterization of anion channels in the plasma membrane of Arabidopsis epidermal root cells and the identification of a citrate-permeable channel induced by phosphate starvation. Plant Physiol 136:4136–4149

    Article  PubMed  CAS  Google Scholar 

  • Frachisse JM, Thomine S, Colcombet J, Guern J, Barbier-Brygoo H (1999) Sulfate is both a substrate and an activator of the voltage-dependent anion channel of Arabidopsis hypocotyl cells. Plant Physiol 121:253–261

    Article  PubMed  CAS  Google Scholar 

  • Hawkesford MJ (2003) Transporter gene families in plants: the sulphate transporter gene family – redundancy or specialization? Physiol Plant 117:155–163

    Article  CAS  Google Scholar 

  • Hawkesford MJ, De Kok LJ (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29:382–395

    Article  PubMed  CAS  Google Scholar 

  • Hawkesford MJ, Wray JL (2000) Molecular genetics of sulphate assimilation. Adv Bot Res 33:159–223

    Article  CAS  Google Scholar 

  • Hawkesford MJ, Zhao FJ (2007) Strategies for increasing the selenium content of wheat. J Cereal Sci 46:282–292

    Article  CAS  Google Scholar 

  • Hawkesford MJ, Davidian J-C, 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

    Article  CAS  Google Scholar 

  • Hopkins L, Parmar S, Błaszczyk A, Hesse H, Hoefgen R, Hawkesford MJ (2005) O-acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol 138:433–440

    Article  PubMed  CAS  Google Scholar 

  • Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004a) 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

    Article  PubMed  CAS  Google Scholar 

  • Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004b) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704

    Article  PubMed  CAS  Google Scholar 

  • Ketter JS, Jarai G, Fu YH, Marzluf GA (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

    Article  PubMed  CAS  Google Scholar 

  • Koralewska A, Posthumus FS, Stuiver CEE, Buchner P, Hawkesford MJ, De Kok LJ (2007) The characteristic high sulfate content in Brassica oleracea is controlled by the expression and activity of sulfate transporters. Plant Biol 9:654–661

    Article  PubMed  CAS  Google Scholar 

  • Koralewska A, Stuiver CEE, Posthumus FS, Kopriva S, Hawkesford MJ, De Kok LJ (2008) Regulation of sulfate uptake, expression of the sulfate transporters Sultr1;1 and Sultr1;2, and APS reductase in Chinese cabbage (Brassica pekinensis) as affected by atmospheric H2S nutrition and sulfate deprivation. Funct Plant Biol 35:318–327

    Article  CAS  Google Scholar 

  • Krusell L, Krause K, Ott T, Desbrosses G, Kramer U, Sato S, Nakamura Y, Tabata S, James EK, Sandal N, Stougaard J, Kawaguchi M, Miyamoto A, Suganuma N, Udvardi MK (2005) The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell 17:1625–1636

    Article  PubMed  CAS  Google Scholar 

  • Lass B, Ullrich-Eberius CI (1984) Evidence for proton/sulfate cotransport and its kinetics in Lemna gibba G1. Planta 161:53–60

    Article  CAS  Google Scholar 

  • Lee RB (1982) Selectivity and kinetics of ion uptake by barley plants following nutrient deficiency. Ann Bot 50:429–449

    CAS  Google Scholar 

  • Leggett JE, Epstein E (1956) Kinetics of sulfate absorption by barley roots. Plant Physiol 31:222–226

    Article  PubMed  CAS  Google Scholar 

  • Leves FP, Tierney ML, Howitt SM (2008) Polar residues in a conserved motif spanning helices 1 and 2 are functionally important in the SulP transporter family. Int J Biochem Cell Biol 40:2596–2605

    Article  PubMed  CAS  Google Scholar 

  • Markovich D (2001) Physiological roles and regulation of mammalian sulfate transporters. Physiol Rev 81:1499–1533

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101:18228–18233

    Article  PubMed  CAS  Google Scholar 

  • Rennenberg H, Kemper O, Thoene B (1989) Recovery of sulfate transport into heterotrophic tobacco cells from inhibition by reduced glutathione. Physiol Plant 76:271–276

    CAS  Google Scholar 

  • Rouached H, Berthomieu P, El Kassis E, Cathala N, Catherinot V, Labesse G, Davidian J-C, Fourcroy P (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

    Article  PubMed  CAS  Google Scholar 

  • Saier MH, Eng BH, Fard S, Garg J, Haggerty DA, Hutchinson WJ, Jack DL, Lai EC, Liu HJ, Nusinew DP, Omar AM, Pao SS, Paulsen IT, Quan JA, Sliwinski M, Tseng TT, Wachi S, Young GB (1999) Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim Biophys Acta 1422:1–56

    Article  PubMed  CAS  Google Scholar 

  • Schweinfest CW, Henderson KW, Suster S, Kondoh N, Papas TS (1993) Identification of a colon mucosa gene that is down-regulated in colon adenomas and adenocarcinomas. Proc Natl Acad Sci USA 90:4166–4170

    Article  PubMed  CAS  Google Scholar 

  • Shelden MC, Loughlin P, Tierney ML, Howitt SM (2001) Proline residues in two tightly coupled helices of the sulphate transporter, SHST1, are important for sulphate transport. Biochem J 356:589–594

    Article  PubMed  CAS  Google Scholar 

  • Shelden MC, Loughlin P, Tierney ML, Howitt SM (2003) Interactions between charged amino acid residues within transmembrane helices in the sulfate transporter SHST1. Biochemistry 42:12941–12949

    Article  PubMed  CAS  Google Scholar 

  • Shibagaki N, Grossman AR (2004) Probing the function of STAS domains of the Arabidopsis sulfate transporters. J Biol Chem 279:30791–30799

    Article  PubMed  CAS  Google Scholar 

  • Shinmachi F, Buchner P, Stroud JL, Parmar S, Zhao FJ, McGrath SP, Hawkesford MJ (2010) Influence of sulfur deficiency on the expression of specific sulfate transporters and the distribution of sulfur, selenium and molybdenum in wheat. Plant Physiol 153:327–336

    Article  PubMed  CAS  Google Scholar 

  • Smith IK (1976) Characterization of sulfate transport in cultured tobacco cells. Plant Physiol 58:358–362

    Article  PubMed  CAS  Google Scholar 

  • Smith FW, Ealing PM, Hawkesford MJ, Clarkson DT (1995a) Plant members of a family of sulfate transporters reveal functional subtypes. Proc Natl Acad Sci USA 92:9373–9377

    Article  PubMed  CAS  Google Scholar 

  • Smith FW, Hawkesford MJ, Prosser IM, Clarkson DT (1995b) Isolation of a cDNA from Saccharomyces cerevisiae that encodes a high-affinity sulfate transporter at the plasma-membrane. Mol Gen Genet 247:709–715

    Article  PubMed  CAS  Google Scholar 

  • Smith FW, Hawkesford MJ, Ealing PM, Clarkson DT, Vanden Berg PJ, Belcher AR, Warrilow AGS (1997) Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J 12:875–884

    Article  PubMed  CAS  Google Scholar 

  • Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, De Almeida EJ, Engler G, Van Montagu M, 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

    Article  PubMed  CAS  Google Scholar 

  • Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, 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

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vidmar JJ, Tagmount A, Cathala N, Touraine B, Davidian J-C (2000) Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. FEBS Lett 475:65–69

    Article  PubMed  CAS  Google Scholar 

  • Yoshimoto N, Takahashi H, Smith FW, 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H (2007) Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 145:378–388

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council (BBSRC) of the UK.

Author information

Authors and Affiliations

  1. Plant Science Department, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK

    Malcolm J. Hawkesford

Authors
  1. Malcolm J. Hawkesford
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Malcolm J. Hawkesford .

Editor information

Editors and Affiliations

  1. Purdue University, Agriculture Mall Drive 625, West Lafayette, 47907, Indiana, USA

    Angus S. Murphy

  2. Department of Horticulture, Purdue University, Agriculture Mall Drive 625, West Lafayette, 47907, Indiana, USA

    Burkhard Schulz

  3. Department of Horticulture, Purdue University, Agriculture Mall Drive 625, West Lafayette, 47907, Indiana, USA

    Wendy Peer

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Hawkesford, M.J. (2011). Sulfate Transport. In: Murphy, A., Schulz, B., Peer, W. (eds) The Plant Plasma Membrane. Plant Cell Monographs, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-13431-9_13

Download citation

Publish with us

Policies and ethics

Search

Navigation