Skip to main content

Sulfate Uptake and Assimilation – Whole Plant Regulation

  • Conference paper
  • First Online:
Sulfur Metabolism in Plants

Part of the book series: Proceedings of the International Plant Sulfur Workshop ((PIPSW,volume 1))

Abstract

Sulfur remains an important issue on the agenda for crop plant nutrition. In addition to avoidance of sulfur deficiency, which will impact on yield and quality, there are requirements for adequate fertilization of crops for resistance to biotic and abiotic stresses. Equally importantly, there are clear consequences for efficient nitrogen utilization and there are interactions with micronutrient acquisition (selenium and molybdenum). Substantial advances have been made at the cellular level, dissecting the signal transduction pathways linking cellular nutritional status with expression of sulfur regulated genes and pathways. However cellular processes need to be placed in the context of whole plant regulation of sulfur uptake and assimilation, which encompasses developmental, spatial and environmental factors, and which facilitates optimum growth and fecundity (and yield in the case of crops) with available sulfur supply. During development, adequate sulfur must be acquired for optimum growth, ideally with any excess being sequestered into re-mobilizable temporary stores. As the plant develops, efficient utilization of sulfur will require organ to organ transfer, and additionally degradation pathways, metabolic inter-conversions and multiple trans-membrane and vascular tissue mediated transport steps for both inorganic and organic sulfur compounds. For crops, efficient transfer of sulfur to harvested sink tissues and its incorporation into protein are important agronomic traits. Insufficient sulfur to meet the demand for growth results in a number of plant responses, targeted at optimising uptake and use of available sulfur. Notable early and specific responses are the up-regulation of transporters and key steps of the assimilatory pathways in sulfur-deficient tissues, and the allocation of resources to stimulate growth of root tissues compared to the shoots. These responses involving root proliferation and transporter functionality are adaptations to improve pedospheric sulfur acquisition. A long standing question has concerned the existence and nature of inter-organ signals of nutrient status. It is possible that local sulfur availability, coupled with intrinsic cell specific programmed function, is sufficient to mediate local gene and pathway expression, influence organ responses and effect whole plant sulfur management without inter organ signals. Developmental cues will influence organ specific pathways, most clearly demonstrated in processes of leaf senescence and associated nutrient remobilization. Conversely, the recognition of possibly mobile phloem located miRNAs may be indicative of long distance regulatory mechanisms. Similarly, root proliferation will almost certainly have a hormonal basis.

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

Access this chapter

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 

  • Breton A, Surdin-Kerjan Y (1977) Sulfate uptake in Saccharomyces cerevisiae: biochemical and genetic study. J Bacteriol 132:224–232

    PubMed  CAS  Google Scholar 

  • Buchner P, Stuiver CEE, Westerman S, Wirtz M, Hell R, Hawkesford MJ, De Kok LJ (2004) 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 sulfate transporter family in wheat: tissue-specific gene expression in relation to nutrition. Mol Plant 3:374–389

    Article  PubMed  CAS  Google Scholar 

  • Dubousset L, Abdallah M, Desfeux AS, Etienne P, Meuriot F, Hawkesford MJ, Gombert J, Segura R, Bataille MP, Reze S, Bonnefoy J, Ameline AF, Ourry A, Le Dily F, Avice JC (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

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick KL, Tyerman SD, Kaiser BN (2008) Molybdate transport through the plant sulfate transporter SHST1. FEBS Lett 582:1508–1513

    Article  PubMed  CAS  Google Scholar 

  • Gilbert SM, Clarkson DT, Cambridge M, Lambers H, Hawkesford MJ (1997) SO 2−4 deprivation has an early effect on the content of ribulose-1,5-bisphosphate carboxylase/oxygenase and photosynthesis in young leaves of wheat. Plant Physiol 115:1231–1239

    PubMed  CAS  Google Scholar 

  • Godfrey D, Hawkesford MJ, Powers SJ, Millar S, Shewry PR (2010) Effects of crop nutrition on wheat grain composition and end use quality. J Agric Food Chem 58:3012–3021

    Article  PubMed  CAS  Google Scholar 

  • Hawkesford MJ (2000) Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S-utilization efficiency. J Exp Bot 51:131–138

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

    Article  CAS  Google Scholar 

  • Hawkesford MJ, Howarth JR, Buchner P (2006) Control of sulfur uptake, assimilation and metabolism. In: Paxton W, McManus MT (eds) Control of primary metabolism in plants. Blackwell, Oxford, pp 348–372

    Chapter  Google Scholar 

  • Hell R, Jost R, Berkowitz O, Wirtz M (2002) Molecular and biochemical analysis of the enzymes of cysteine biosynthesis in the plant Arabidopsis thaliana. Amino Acids 22:245–257

    Article  PubMed  CAS  Google Scholar 

  • Hopkins L, Parmar S, Baszczyk 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 

  • Howarth JR, Parmar S, Jones J, Shepherd CE, Corol DI, Galster AM, Hawkins ND, Miller SJ, Baker JM, Verrier PJ, Ward JL, Beale MH, Barraclough PB, Hawkesford MJ (2008) Co-ordinated expression of amino acid metabolism in response to N and S deficiency during wheat grain filling. J Exp Bot 59:3675–3689

    Article  PubMed  CAS  Google Scholar 

  • Kataoka T, Takahashi H (2005) Sulfate transporters involved in redistribution and translocation of sulfate in root vasculature of Arabidopsis thaliana. In: Saito K, De Kok LJ, Stulen I, Hawkesford MJ, Schnug E, Sirko A, Rennenberg H (eds) Sulfur transport and assimilation in plants in the post genomic era. Backhuys Publishers, Leiden, pp 45–47

    Google Scholar 

  • Kataoka T, Hayashi N, Takahashi-Watanabe A, Inoue E, Saito K, Yamaya T, Takahashi H (2003) Functional analysis of sulfate transporters expressed in pericycles of Arabidopsis root. Plant Cell Physiol 44:S173

    Article  Google Scholar 

  • Kataoka T, Hayashi N, Takahashi-Watanabe A, Inoue E, Yamaya T, Takahashi H (2004a) Functional analysis of sulfate transporters SULTR2;1 and SULTR3;5 in Arabidopsis. Plant Cell Physiol 45:S174

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (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

    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 

  • Koralewska A, Buchner P, Stuiver CEE, Posthumus FS, Kopriva S, Hawkesford MJ, De Kok LJ (2009) Expression and activity of sulfate transporters and APS reductase in curly kale in response to sulfate deprivation and re-supply. J Plant Physiol 166:168–179

    Article  PubMed  CAS  Google Scholar 

  • Kredich NM (1993) Gene-regulation of sulfur assimilation. In: De Kok LJ, Stulen I, Rennenberg H, Brunold C, Rauser WE (eds) Sulfur nutrition and assimilation in higher plants – regulatory agricultural and environmental aspects. SPB Academic Publishing, The Hague, pp 37–47

    Google Scholar 

  • Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO 2−4 uptake in intact canola. The role of phloem-translocated glutathione. Plant Physiol 111:147–157

    PubMed  CAS  Google Scholar 

  • Lappartient AG, Vidmar JJ, Leustek T, Glass ADM, Touraine B (1999) Inter-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

    Article  PubMed  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 

  • Liang G, Yang FX, Yu DQ (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62:1046–1057

    PubMed  CAS  Google Scholar 

  • Molvig L, Tabe LM, Eggum BO, Moore AE, Craig S, Spencer D, Higgins TJV (1997) Enhanced methionine levels and increased nutritive value of seeds of transgenic lupins (Lupinus angustifolius L) expressing a sunflower seed albumin gene. Proc Natl Acad Sci USA 94:8393–8398

    Article  PubMed  CAS  Google Scholar 

  • Mugford SG, Yoshimoto N, Reichelt M, Wirtz M, Hill L, Mugford ST, Nakazato Y, Noji M, Takahashi H, Kramell R, Gigolashvili T, Flugge UI, Wasternack C, Gershenzon J, Hell R, Saito K, Kopriva S (2009) Disruption of adenosine-5′-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21:910–927

    Article  PubMed  CAS  Google Scholar 

  • Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138:304–318

    Article  PubMed  CAS  Google Scholar 

  • Parmar S, Buchner P, Hawkesford MJ (2007) Leaf developmental stage affects sulfate depletion and specific sulfate transporter expression during sulfur deprivation in Brassica napus L. Plant Biol 9:647–653

    Article  PubMed  CAS  Google Scholar 

  • Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci USA 97:12356–12360

    Article  PubMed  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 

  • Shahbaz M, Tseng MH, Stuiver CEE, Koralewska A, Posthumus FS, Venema JH, Parmar S, Schat H, Hawkesford MJ, De Kok LJ (2010) Copper exposure interferes with the regulation of the uptake, distribution and metabolism of sulfate in Chinese cabbage. J Plant Physiol 167:438–446

    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 

  • Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (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

    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 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 

  • Stroud JL, Li HF, Lopez-Bellido FJ, Broadley MR, Foot I, Fairweather-Tait SJ, Hart DJ, Hurst R, Knott P, Mowat H, Norman K, Scott P, Tucker M, White PJ, McGrath SP, Zhao FJ (2010) Impact of sulphur fertilisation on crop response to selenium fertilisation. Plant Soil 332:31–40

    Article  CAS  Google Scholar 

  • Tabe L, Higgins TJV (1998) Engineering plant protein composition for improved nutrition. Trends Plant Sci 3:282–286

    Article  Google Scholar 

  • Tan QM, Zhang LZ, Grant J, Cooper P, Tegeder M (2010) Increased phloem transport of s-methylmethionine positively affects sulfur and nitrogen metabolism and seed development in pea plants. Plant Physiol 154:1886–1896

    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 

  • Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krähenbühl U, den Camp RO, Brunold C (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

    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, 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 

  • Zhao FJ, Hawkesford MJ, McGrath SP (1999) Sulphur assimilation and effects on yield and quality of wheat. J Cereal Sci 30:1–17

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council (BBSRC), U.K.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Malcolm J. Hawkesford .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media Dordrecht

About this paper

Cite this paper

Hawkesford, M.J. (2012). Sulfate Uptake and Assimilation – Whole Plant Regulation. In: De Kok, L., et al. Sulfur Metabolism in Plants. Proceedings of the International Plant Sulfur Workshop, vol 1. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4450-9_2

Download citation

Publish with us

Policies and ethics