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Nutrient Use Efficiency in Plants pp 51–91Cite as

Macronutrient Use Efficiency – Sulfur in Arabidopsis thaliana

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Part of the book series: Plant Ecophysiology ((KLEC,volume 10))

Abstract

Sulfur is an essential macronutrient required for proper growth of not only plants but also fungi and prokaryotes. It is present in a wide variety of metabolites such as amino acids: cysteine and methionine, coenzymes, vitamins and many others having distinctive biological functions. Plants take up sulfur from the soil in the form of sulfate via sulfate transporters. It is then reduced and assimilated in bioorganic compounds where cysteine is the first stable product. This process is very well described on both biochemical and molecular levels. Both reduction and assimilation are tightly regulated in demand-driven manner. The pathway has been extensively studied over last years because of important functions of sulfur in plant metabolism and stress defence. Here we summarise the up-to-date knowledge about the pathway and its regulation based mainly on the study on model plant Arabidopsis thaliana. We also emphasize areas in which little is known including the interconnection of sulfate metabolism with other nutrients.

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References

  • Abdallah M, Dubousset L, Meuriot F, Etienne P, Avice JC, Ourry A (2010) Effect of mineral sulphur availability on nitrogen and sulphur uptake and remobilization during the vegetative growth of Brassica napus L. J Exp Bot 61:2635–2646

    CAS  PubMed Central  PubMed  Google Scholar 

  • Alonso-Blanco C, Aarts MG, Bentsink L, Keurentjes JJ, Reymond M, Vreugdenhil D, Koornneef M (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21:1877–1896

    CAS  PubMed Central  PubMed  Google Scholar 

  • Alvarez C, Garcia I, Romero LC, Gotor C (2012) Mitochondrial sulfide detoxification requires a functional isoform O-acetylserine(thiol)lyase C in Arabidopsis thaliana. Mol Plant 5:1217–1226

    CAS  PubMed  Google Scholar 

  • Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y (2007) Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci U S A 104:18333–18338

    CAS  PubMed Central  PubMed  Google Scholar 

  • Amir R, Hacham Y, Galili G (2002) Cystathionine gamma-synthase and threonine synthase operate in concert to regulate carbon flow towards methionine in plants. Trends Plant Sci 7:153–156

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I, Brachi B, Chory J, Dean C, Debieu M, de Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JD, Michael T, Nemri A, Roux F, Salt DE, Tang C, Todesco M, Traw MB, Weigel D, Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631

    CAS  PubMed Central  PubMed  Google Scholar 

  • Awazuhara M, Kim H, Goto DB, Matsui A, Hayashi H, Chino M, Kim S-G, Naito S, Fujiwara T (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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Barberon M, Berthomieu P, Clairotte M, Shibagaki N, Davidian JC, 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

    CAS  PubMed  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    CAS  PubMed  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(2):e1000004. doi:10.1371/journal.pgen.1000004

    PubMed Central  PubMed  Google Scholar 

  • Benfey PN, Mitchell-Olds T (2008) From genotype to phenotype: systems biology meets natural variation. Science 320:495–497

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bessey CE (1906) Crop improvement by utilizing wild species. J Hered 2:112–118

    Google Scholar 

  • Bick JA, Aslund F, Chen Y, Leustek T (1998) Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′-adenylylsulfate reductase. Proc Natl Acad Sci U S A 95:8404–8409

    CAS  PubMed Central  PubMed  Google Scholar 

  • Blake-Kalff MM, Harrison KR, Hawkesford MJ, Zhao FJ, McGrath SP (1998) Distribution of sulfur within oilseed rape leaves in response to sulfur deficiency during vegetative growth. Plant Physiol 118:1337–1344

    CAS  PubMed Central  PubMed  Google Scholar 

  • Blake-Kalff MMA, Hawkesford MJ, Zhao FJ, McGrath SP (2000) Diagnosing sulfur deficiency in field-grown oilseed rape (Brassica napus L.) and wheat (Triticum aestivum L.). Plant Soil 225:95–107

    CAS  Google Scholar 

  • Blake-Kalff MMA, Zhao FJ, Hawkesford MJ, McGrath SP (2001) Using plant analysis to predict yield losses caused by sulphur deficiency. Ann Appl Biol 138:123–127

    CAS  Google Scholar 

  • Brader G, Tas E, Palva ET (2001) Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiol 126:849–860

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62:471–481

    CAS  PubMed  Google Scholar 

  • Brunold C, Schiff JA (1976) Studies of sulfate utilization of algae: 15. Enzymes of assimilatory sulfate reduction in euglena and their cellular localization. Plant Physiol 57:430–436

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brunold C, Suter M (1984) Regulation of sulfate assimilation by nitrogen nutrition in the duckweed Lemna minor L. Plant Physiol 76:579–583

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brunold C, Suter M (1989) Localization of enzymes of assimilatory sulfate reduction in pea roots. Planta 179:228–234

    CAS  PubMed  Google Scholar 

  • Brychkova G, Xia Z, Yang G, Yesbergenova Z, Zhang Z, Davydov O, Fluhr R, Sagi M (2007) Sulfite oxidase protects plants against sulfur dioxide toxicity. Plant J 50:696–709

    CAS  PubMed  Google Scholar 

  • Buchner P, Prosser IM, Hawkesford MJ (2004a) Phylogeny and expression of paralogous and orthologous sulphate transporter genes in diploid and hexaploid wheats. [Research Support, Non-U S Gov’t]. Genome 47:526–534

    CAS  PubMed  Google Scholar 

  • Buchner P, Takahashi H, Hawkesford MJ (2004b) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 55:1765–1773

    CAS  PubMed  Google Scholar 

  • Buescher E, Achberger T, Amusan I, Giannini A, Ochsenfeld C, Rus A, Lahner B, Hoekenga O, Yakubova E, Harper JF, Guerinot ML, Zhang M, Salt DE, Baxter IR (2010) Natural genetic variation in selected populations of Arabidopsis thaliana is associated with ionomic differences. PLoS One 5:e11081

    PubMed Central  PubMed  Google Scholar 

  • Burstenbinder K, Rzewuski G, Wirtz M, Hell R, Sauter M (2007) The role of methionine recycling for ethylene synthesis in Arabidopsis. Plant J 49:238–249

    PubMed  Google Scholar 

  • Cao MJ, Wang Z, Wirtz M, Hell R, Oliver DJ, Xiang CB (2013) SULTR3;1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana. Plant J 73:607–616

    CAS  PubMed  Google Scholar 

  • Chen YF, Matsubayashi Y, Sakagami Y (2000) Peptide growth factor phytosulfokine-alpha contributes to the pollen population effect. Planta 211:752–755

    CAS  PubMed  Google Scholar 

  • Chiba Y, Ishikawa M, Kijima F, Tyson RH, Kim J, Yamamoto A, Nambara E, Leustek T, Wallsgrove RM, Naito S (1999) Evidence for autoregulation of cystathionine gamma-synthase mRNA stability in Arabidopsis. Science 286:1371–1374

    CAS  PubMed  Google Scholar 

  • Chiba Y, Sakurai R, Yoshino M, Ominato K, Ishikawa M, Onouchi H, Naito S (2003) S-adenosyl-L-methionine is an effector in the posttranscriptional autoregulation of the cystathionine gamma-synthase gene in Arabidopsis. Proc Natl Acad Sci U S A 100:10225–10230

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18:412–421

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Curien G, Dumas R, Ravanel S, Douce R (1996) Characterization of an Arabidopsis thaliana cDNA encoding an S-adenosylmethionine-sensitive threonine synthase. Threonine synthase from higher plants. FEBS Lett 390:85–90

    CAS  PubMed  Google Scholar 

  • Curtis TY, Powers SJ, Balagiannis D, Elmore JS, Mottram DS, Parry MAJ, Rakszegi M, Bedö Z, Shewry PR, Halford NG (2010) Free amino acids and sugars in rye grain: implications for acrylamide formation. J Agric Food Chem 58:1959–1969

    CAS  PubMed  Google Scholar 

  • Doughty KJ, Kiddle GA, Pye BJ, Wallsgrove RM, Pickett JA (1995) Selective induction of glucosinolates in oilseed rape leaves by methyl jasmonate. Phytochemistry 38:347–350

    CAS  Google Scholar 

  • Droux M, Ruffet ML, 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

    CAS  PubMed  Google Scholar 

  • Eilers T, Schwarz G, Brinkmann H, Witt C, Richter T, Nieder J, Koch B, Hille R, Hansch R, Mendel RR (2001) Identification and biochemical characterization of Arabidopsis thaliana sulfite oxidase. A new player in plant sulfur metabolism. J Biol Chem 276:46989–46994

    CAS  PubMed  Google Scholar 

  • Essigmann B, Guler S, Narang RA, Linke D, Benning C (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 95:1950–1955

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51

    CAS  PubMed  Google Scholar 

  • Fernie AR, Tadmor Y, Zamir D (2006) Natural genetic variation for improving crop quality. Curr Opin Plant Biol 9:196–202

    PubMed  Google Scholar 

  • Fismes J, Vong PC, Guckert A, Frossard E (2000) Influence of sulfur on apparent N-use efficiency, yield and quality of oilseed rape (Brassica napus L.) grown on a calcareous soil. Eur J Agron 12:127–141

    CAS  Google Scholar 

  • Flæte NES, Hollung K, Ruud L, Sogn T, Færgestad EM, Skarpeid HJ, Magnus EM, Uhlen AK (2005) Combined nitrogen and sulphur fertilisation and its effect on wheat quality and protein composition measured by SE-FPLC and proteomics. J Cereal Sci 41:357–369

    Google Scholar 

  • Francois JA, Kumaran S, Jez JM (2006) Structural basis for interaction of O-acetylserine sulfhydrylase and serine acetyltransferase in the Arabidopsis cysteine synthase complex. Plant Cell 18:3647–3655

    CAS  PubMed Central  PubMed  Google Scholar 

  • Friedman M (2003) Chemistry, biochemistry, and safety of acrylamide, a review. J Agric Food Chem 51:4504–4526

    CAS  PubMed  Google Scholar 

  • Fujii H, Chiou T-J, Lin S-I, Aung K, Zhu J-K (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043

    CAS  PubMed  Google Scholar 

  • Garcia I, Castellano JM, Vioque B, Solano R, Gotor C, Romero LC (2010) Mitochondrial beta-cyanoalanine synthase is essential for root hair formation in Arabidopsis thaliana. Plant Cell 22:3268–3279

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gasber A, Klaumann S, Trentmann O, Trampczynska A, Clemens S, Schneider S, Sauer N, Feifer I, Bittner F, Mendel RR, Neuhaus HE (2011) Identification of an Arabidopsis solute carrier critical for intracellular transport and inter-organ allocation of molybdate. Plant Biol 13:710–718

    CAS  PubMed  Google Scholar 

  • Ghandilyan A, Ilk N, Hanhart C, Mbengue M, Barboza L, Schat H, Koornneef M, El-Lithy M, Vreugdenhil D, Reymond M, Aarts MG (2009) A strong effect of growth medium and organ type on the identification of QTLs for phytate and mineral concentrations in three Arabidopsis thaliana RIL populations. J Exp Bot 60:1409–1425

    CAS  PubMed  Google Scholar 

  • Gigolashvili T, Berger B, Mock HP, Muller C, Weisshaar B, Flugge UI (2007) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 50:886–901

    CAS  PubMed  Google Scholar 

  • Gigolashvili T, Engqvist M, Yatusevich R, Muller C, Flugge UI (2008) HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytol 177:627–642

    CAS  PubMed  Google Scholar 

  • Gilbert SM, Clarkson DT, Cambridge M, Lambers H, Hawkesford MJ (1997) SO4 2− 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Giovanelli J, Mudd SH, Datko AH (1985) Quantitative analysis of pathways of methionine metabolism and their regulation in lemna. Plant Physiol 78:555–560

    CAS  PubMed Central  PubMed  Google Scholar 

  • Haas FH, Heeg C, Queiroz R, Bauer A, Wirtz M, Hell R (2008) Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. Plant Physiol 148:1055–1067

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hacham Y, Schuster G, Amir R (2006) An in vivo internal deletion in the N-terminus region of Arabidopsis cystathionine gamma-synthase results in CGS expression that is insensitive to methionine. Plant J 45:955–967

    CAS  PubMed  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    CAS  PubMed  Google Scholar 

  • Halford NG, Curtis TY, Muttucumaru N, Postles J, Elmore JS, Mottram DS (2012) The acrylamide problem: a plant and agronomic science issue. J Exp Bot 63:2841–2851

    CAS  PubMed  Google Scholar 

  • Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333

    CAS  PubMed  Google Scholar 

  • Hänsch R, Lang C, Riebeseel E, Lindigkeit R, Gessler A, Rennenberg H, Mendel RR (2006) Plant sulfite oxidase as novel producer of H2O2: combination of enzyme catalysis with a subsequent non-enzymatic reaction step. J Biol Chem 281:6884–6888

    PubMed  Google Scholar 

  • Hatzfeld Y, Lee S, Lee M, Leustek T, Saito K (2000a) Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248:51–58

    CAS  PubMed  Google Scholar 

  • Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K, Saito K (2000b) beta-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol 123:1163–1171

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Hawkesford M, Davidian J-C, Grignon C (1993) Sulphate/proton cotransport in plasma-membrane vesicles isolated from roots of Brassica napus L.: increased transport in membranes isolated from sulphur-starved plants. Planta 190:297–304

    CAS  Google Scholar 

  • Hell R, Hillebrand H (2001) Plant concepts for mineral acquisition and allocation. Curr Opin Biotechnol 12:161–168

    CAS  PubMed  Google Scholar 

  • Hell R, Wirtz M (2008) Metabolism of cysteine in plants and phototrophic bacteria. In: Hell R, Dahl C, Knaff D, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Netherlands, pp 59–91

    Google Scholar 

  • Hell R, Wirtz M (2011) Molecular biology, biochemistry and cellular physiology of cysteine metabolism in Arabidopsis thaliana. The Arabidopsis book. Am Soc Plant Biol 9:e0154

    Google Scholar 

  • Hesse H, Trachsel N, Suter M, Kopriva S, von Ballmoos P, Rennenberg H, Brunold C (2003) Effect of glucose on assimilatory sulphate reduction in Arabidopsis thaliana roots. J Exp Bot 54:1701–1709

    CAS  PubMed  Google Scholar 

  • Hesse H, Kreft O, Maimann S, Zeh M, Hoefgen R (2004a) Current understanding of the regulation of methionine biosynthesis in plants. J Exp Bot 55:1799–1808

    CAS  PubMed  Google Scholar 

  • Hesse H, Nikiforova V, Gakiere B, Hoefgen R (2004b) Molecular analysis and control of cysteine biosynthesis: integration of nitrogen and sulphur metabolism. J Exp Bot 55:1283–1292

    CAS  PubMed  Google Scholar 

  • Hirai MY, Sugiyama K, Sawada Y, Tohge T, Obayashi T, Suzuki A, Araki R, Sakurai N, Suzuki H, Aoki K, Goda H, Nishizawa OI, Shibata D, Saito K (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci U S A 104:6478–6483

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hopkins L, Parmar S, Blaszczyk 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Howarth JR, Fourcroy P, Davidian JC, Smith FW, Hawkesford MJ (2003) Cloning of two contrasting high-affinity sulfate transporters from tomato induced by low sulfate and infection by the vascular pathogen Verticillium dahliae. Planta 218:58–64

    CAS  PubMed  Google Scholar 

  • Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132

    PubMed Central  PubMed  Google Scholar 

  • Hubberten HM, Klie S, Caldana C, Degenkolbe T, Willmitzer L, Hoefgen R (2012) Additional role of O-acetylserine as a sulfur status-independent regulator during plant growth. Plant J 70:666–677

    CAS  PubMed  Google Scholar 

  • Hussain A, Larsson H, Kuktaite R, Prieto-Linde ML, Johansson E (2012) Towards the understanding of bread-making quality in organically grown wheat: dough mixing behaviour, protein polymerisation and structural properties. J Cereal Sci 56:659–666

    CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    CAS  PubMed  Google Scholar 

  • Jost R, Altschmied L, Bloem E, Bogs J, Gershenzon J, Hahnel U, Hansch R, Hartmann T, Kopriva S, Kruse C, Mendel RR, Papenbrock J, Reichelt M, Rennenberg H, Schnug E, Schmidt A, Textor S, Tokuhisa J, Wachter A, Wirtz M, Rausch T, Hell R (2005) Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosynth Res 86:491–508

    CAS  PubMed  Google Scholar 

  • Kandlbinder A, Finkemeier I, Wormuth D, Hanitzsch M, Dietz KJ (2004) The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol Plant 120:63–73

    CAS  PubMed  Google Scholar 

  • Karmoker J, Clarkson D, Saker L, Rooney J, Purves J (1991) Sulphate deprivation depresses the transport of nitrogen to the xylem and the hydraulic conductivity of barley (Hordeum vulgare L.) roots. Planta 185:269–278

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kawashima CG, 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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

  • Kawashima CG, Matthewman CA, Huang S, Lee B-R, Yoshimoto N, Koprivova A, Rubio-Somoza I, Todesco M, Rathjen T, Saito K, Takahashi H, Dalmay T, Kopriva S (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66:863–876

    CAS  PubMed  Google Scholar 

  • Khan MS, Haas FH, Allboje Samami A, Moghaddas Gholami A, Bauer A, Fellenberg K, Reichelt M, Hänsch R, Mendel RR, Meyer AJ, Wirtz M, Hell R (2010) Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana. Plant Cell Online 22:1216–1231

    CAS  Google Scholar 

  • Kim H, Hirai MY, Hayashi H, Chino M, Naito S, Fujiwara T (1999) Role of O-acetyl-L-serine in the coordinated regulation of the expression of a soybean seed storage-protein gene by sulfur and nitrogen nutrition. Planta 209:282–289

    CAS  PubMed  Google Scholar 

  • Kobayashi T, Eun C-H, Hanai H, Matsubayashi Y, Sakagami Y, Kamada H (1999) Phytosulphokine-α, a peptidyl plant growth factor, stimulates somatic embryogenesis in carrot. J Exp Bot 50:1123–1128

    CAS  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Physiol Plant Mol Biol 55:141–172

    CAS  Google Scholar 

  • Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kopriva S, Koprivova A (2004) Plant adenosine 5′-phosphosulphate reductase: the past, the present, and the future. J Exp Bot 55:1775–1783

    CAS  PubMed  Google Scholar 

  • Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55:1831–1842

    CAS  PubMed  Google Scholar 

  • Kopriva S, Muheim R, Koprivova A, Trachsel N, Catalano C, Suter M, Brunold C (1999) Light regulation of assimilatory sulphate reduction in Arabidopsis thaliana. Plant J 20:37–44

    CAS  PubMed  Google Scholar 

  • Kopriva S, Buchert T, Fritz G, Suter M, Weber M, Benda R, Schaller J, Feller U, Schurmann P, Schunemann V, Trautwein AX, Kroneck PM, Brunold C (2001) Plant adenosine 5′-phosphosulfate reductase is a novel iron-sulfur protein. J Biol Chem 276:42881–42886

    CAS  PubMed  Google Scholar 

  • Kopriva S, Suter M, von Ballmoos P, Hesse H, Krähenbühl U, Rennenberg H, Brunold C (2002) Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol 130:1406–1413

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kopriva S, Fritzemeier K, Wiedemann G, Reski R (2007) The putative moss 3′-phosphoadenosine-5′-phosphosulfate reductase is a novel form of adenosine-5′-phosphosulfate reductase without an iron-sulfur cluster. J Biol Chem 282:22930–22938

    CAS  PubMed  Google Scholar 

  • Kopriva S, Mugford S, Matthewman C, Koprivova A (2009) Plant sulfate assimilation genes: redundancy versus specialization. Plant Cell Rep 28:1769–1780

    CAS  PubMed  Google Scholar 

  • Kopriva S, Mugford SG, Baraniecka P, Lee B-R, Matthewman CA, Koprivova A (2012) Control of sulfur partitioning between primary and secondary metabolism in Arabidopsis. Front Plant Sci 3:163. doi:10.3389/fpls.2012.00163

    PubMed Central  PubMed  Google Scholar 

  • Koprivova A, Suter M, Op den Camp R, Brunold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737–746

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koprivova A, North KA, Kopriva S (2008) Complex signaling network in regulation of adenosine 5′-phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol 146:1408–1420

    CAS  PubMed Central  PubMed  Google Scholar 

  • Krueger S, Niehl A, Lopez Martin MC, Steinhauser D, Donath A, Hildebrandt T, Romero LC, Hoefgen R, Gotor C, Hesse H (2009) Analysis of cytosolic and plastidic serine acetyltransferase mutants and subcellular metabolite distributions suggests interplay of the cellular compartments for cysteine biosynthesis in Arabidopsis. Plant Cell Environ 32:349–367

    CAS  PubMed  Google Scholar 

  • Kuktaite R, Larsson H, Johansson E (2004) Variation in protein composition of wheat flour and its relationship to dough mixing behaviour. J Cereal Sci 40:31–39

    CAS  Google Scholar 

  • Kutz A, Muller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J 30:95–106

    CAS  PubMed  Google Scholar 

  • Lambein I, Chiba Y, Onouchi H, Naito S (2003) Decay kinetics of autogenously regulated CGS1 mRNA that codes for cystathionine gamma-synthase in Arabidopsis thaliana. Plant Cell Physiol 44:893–900

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lee B-R, Koprivova A, Kopriva S (2011) The key enzyme of sulfate assimilation, adenosine 5′-phosphosulfate reductase, is regulated by HY5 in Arabidopsis. Plant J 67:1042–1054

    CAS  PubMed  Google Scholar 

  • Lejay L, Gansel X, Cerezo M, Tillard P, Muller C, Krapp A, von Wiren N, Daniel-Vedele F, Gojon A (2003) Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 15:2218–2232

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51:141–165

    CAS  PubMed  Google Scholar 

  • Levy M, Wang Q, Kaspi R, Parrella MP, Abel S (2005) Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense. Plant J 43:79–96

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lin S-I, Chiang S-F, Lin W-Y, Chen J-W, Tseng C-Y, Wu P-C, Chiou T-J (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    CAS  PubMed Central  PubMed  Google Scholar 

  • Logan HM, Cathala N, Grignon C, Davidian JC (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. J Biol Chem 271:12227–12233

    CAS  PubMed  Google Scholar 

  • López-Martín MC, Becana M, Romero LC, Gotor C (2008) Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol 147:562–572

    PubMed Central  PubMed  Google Scholar 

  • Loudet O, Saliba-Colombani V, Camilleri C, Calenge F, Gaudon V, Koprivova A, North KA, Kopriva S, Daniel-Vedele F (2007) Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat Genet 39:896–900

    CAS  PubMed  Google Scholar 

  • Lunn JE, Droux M, Martin J, Douce R (1990) Localization of ATP sulfurylase and O-Acetylserine(thiol)lyase in Spinach leaves. Plant Physiol 94:1345–1352

    CAS  PubMed Central  PubMed  Google Scholar 

  • Malhi SS, Gan Y, Raney JP (2007) Yield, seed quality, and sulfur uptake of Brassica oilseed crops in response to sulfur fertilization. Agron J 99:570–577

    CAS  Google Scholar 

  • Martin MN, Tarczynski MC, Shen B, Leustek T (2005) The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants. Photosynth Res 86:309–323

    CAS  PubMed  Google Scholar 

  • Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol 132:597–605

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matsubayashi Y, Sakagami Y (1999) Characterization of specific binding sites for a mitogenic sulfated peptide, phytosulfokine-alpha, in the plasma-membrane fraction derived from Oryza sativa L. Eur J Biochem 262:666–671

    CAS  PubMed  Google Scholar 

  • Matsubayashi Y, Sakagami Y (2006) Peptide hormones in plants. Annu Rev Plant Biol 57:649–674

    CAS  PubMed  Google Scholar 

  • Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470–1472

    CAS  PubMed  Google Scholar 

  • Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y (2010) Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329:1065–1067

    CAS  PubMed  Google Scholar 

  • Matthewman CA, Kawashima CG, Huska D, Csorba T, Dalmay T, Kopriva S (2012) miR395 is a general component of the sulfate assimilation regulatory network in Arabidopsis. FEBS Lett 586:3242–3248

    CAS  PubMed  Google Scholar 

  • McCouch S (2004) Diversifying selection in plant breeding. PLoS Biol 2:e347

    PubMed Central  PubMed  Google Scholar 

  • McGrath SP, Zhao FJ (1996) Sulphur uptake, yield responses and the interactions between nitrogen and sulphur in winter oilseed rape (Brassica napus). J Agric Sci 126:53–62

    CAS  Google Scholar 

  • McGrath SP, Zhao FJ, Withers PJA (1996) Development of sulphur deficiency in crops and its treatment. Proceedings of the Fertiliser Society

    Google Scholar 

  • Meng L, Buchanan BB, Feldman LJ, Luan S (2012) CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis. Proc Natl Acad Sci U S A 109:1760–1765

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mithen R, Faulkner K, Magrath R, Rose P, Williamson G, Marquez J (2003) Development of isothiocyanate-enriched broccoli, and its enhanced ability to induce phase 2 detoxification enzymes in mammalian cells. Theor Appl Genet 106:727–734

    CAS  PubMed  Google Scholar 

  • Moss H, Wrigley C, MacRichie R, Randall P (1981) Sulfur and nitrogen fertilizer effects on wheat. II. Influence on grain quality. Aust J Agric Res 32:213–226

    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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mugford SG, Matthewman CA, Hill L, Kopriva S (2010) Adenosine-5′-phosphosulfate kinase is essential for Arabidopsis viability. FEBS Lett 584:119–123

    CAS  PubMed  Google Scholar 

  • Murillo M, Leustek T (1995) Adenosine-5′-triphosphate-sulfurylase from Arabidopsis thaliana and Escherichia coli are functionally equivalent but structurally and kinetically divergent: nucleotide sequence of two adenosine-5′-triphosphate-sulfurylase cDNAs from Arabidopsis thaliana and analysis of a recombinant enzyme. Arch Biochem Biophys 323:195–204

    CAS  PubMed  Google Scholar 

  • Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21:2194–2202

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakayama M, Akashi T, Hase T (2000) Plant sulfite reductase: molecular structure, catalytic function and interaction with ferredoxin. J Inorg Biochem 82:27–32

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Nowak K, Luniak N, Witt C, Wustefeld Y, Wachter A, Mendel RR, Hansch R (2004) Peroxisomal localization of sulfite oxidase separates it from chloroplast-based sulfur assimilation. Plant Cell Physiol 45:1889–1894

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ohkama-Ohtsu N, Oikawa A, Zhao P, Xiang C, Saito K, Oliver DJ (2008) A gamma-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol 148:1603–1613

    CAS  PubMed Central  PubMed  Google Scholar 

  • Olsen LR, Huang B, Vetting MW, Roderick SL (2004) Structure of serine acetyltransferase in complexes with CoA and its cysteine feedback inhibitor. Biochemistry 43:6013–6019

    CAS  PubMed  Google Scholar 

  • Prosser IM, Purves JV, Saker LR, Clarkson DT (2001) Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. J Exp Bot 52:113–121

    CAS  PubMed  Google Scholar 

  • Rae A, Smith F (2002) Localisation of expression of a high-affinity sulfate transporter in barley roots. Planta 215:565–568

    CAS  PubMed  Google Scholar 

  • Ravanel S, Gakière B, Job D, Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci U S A 95:7805–7812

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ravanel S, Block MA, Rippert P, Jabrin S, Curien G, Rébeillé F, Douce R (2004) Methionine metabolism in plants: chloroplasts are autonomous for de novo methionine synthesis and can import s-adenosylmethionine from the cytosol. J Biol Chem 279:22548–22557

    CAS  PubMed  Google Scholar 

  • Renosto F, Patel HC, Martin RL, Thomassian C, Zimmerman G, Segel IH (1993) ATP sulfurylase from higher plants: kinetic and structural characterization of the chloroplast and cytosol enzymes from spinach leaf. Arch Biochem Biophys 307:272–285

    CAS  PubMed  Google Scholar 

  • Renwick JA (2001) Variable diets and changing taste in plant-insect relationships. J Chem Ecol 27:1063–1076

    CAS  PubMed  Google Scholar 

  • Rotte C, Leustek T (2000) Differential subcellular localization and expression of ATP sulfurylase and 5′-adenylylsulfate reductase during ontogenesis of Arabidopsis leaves indicates that cytosolic and plastid forms of ATP sulfurylase may have specialized functions. Plant Physiol 124:715–724

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rouached H (2011) Multilevel coordination of phosphate and sulfate homeostasis in plants. Plant Signal Behav 6:952–955

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

  • Rouached H, Wirtz M, Alary R, Hell R, Arpat AB, Davidian J-C, Fourcroy P, Berthomieu P (2008) Differential regulation of the expression of two high-affinity sulfate transporters, SULTR1.1 and SULTR1.2, in Arabidopsis. Plant Physiol 147:897–911

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rouached H, Secco D, Arpat B, Poirier Y (2011) The transcription factor PHR1 plays a key role in the regulation of sulfate shoot-to-root flux upon phosphate starvation in Arabidopsis. BMC Plant Biol 11:19

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saito K (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr Opin Plant Biol 3:188–195

    CAS  PubMed  Google Scholar 

  • Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443–2450

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shahsavani S, Gholami A (2008) Effect of sulphur fertilization on breadmaking quality of three winter wheat varieties. Pak J Biol Sci 11:2134–2138

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Shibagaki N, Grossman AR (2010) Binding of cysteine synthase to the STAS domain of sulfate transporter and its regulatory consequences. J Biol Chem 285:25094–25102

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Skirycz A, Reichelt M, Burow M, Birkemeyer C, Rolcik J, Kopka J, Zanor MI, Gershenzon J, Strnad M, Szopa J, Mueller-Roeber B, Witt I (2006) DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J 47:10–24

    CAS  PubMed  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 U S A 92:9373–9377

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smith FW, Hawkesford MJ, Prosser IM, 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sønderby IE, Hansen BG, Bjarnholt N, Ticconi C, Halkier BA, Kliebenstein DJ (2007) A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS One 2:e1322

    PubMed Central  PubMed  Google Scholar 

  • Suzuki A, Shirata Y, Ishida H, Chiba Y, Onouchi H, Naito S (2001) The first exon coding region of cystathionine gamma-synthase gene is necessary and sufficient for downregulation of its own mRNA accumulation in transgenic Arabidopsis thaliana. Plant Cell Physiol 42:1174–1180

    CAS  PubMed  Google Scholar 

  • Takahashi H, Saito K (1996) Subcellular localization of spinach cysteine synthase isoforms and regulation of their gene expression by nitrogen and sulfur. Plant Physiol 112:273–280

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takahashi H, Saito K (2008) Molecular biology and functional genomics for identification of regulatory networks of plant sulfate uptake and assimilatory metabolism. In: Hell R, Dahl C, Knaff D, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Netherlands, pp 149–159

    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

    CAS  PubMed  Google Scholar 

  • Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184

    CAS  PubMed  Google Scholar 

  • Tareke E, Rydberg P, Karlsson P, Eriksson S, Tornqvist M (2002) Analysis of acrylamide, a carcinogen formed in heated foodstuffs. J Agric Food Chem 50:4998–5006

    CAS  PubMed  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 U S A 104:18807–18812

    CAS  PubMed Central  PubMed  Google Scholar 

  • Varadarajan DK, Karthikeyan AS, Matilda PD, Raghothama KG (2002) Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol 129:1232–1240

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krahenbuhl 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

    CAS  PubMed  Google Scholar 

  • Vidmar JJ, Tagmount A, Cathala N, Touraine B, Davidian JE (2000) Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. [Research Support, Non-U S Gov’t]. FEBS Lett 475:65–69

    CAS  PubMed  Google Scholar 

  • Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–567

    CAS  PubMed Central  PubMed  Google Scholar 

  • Watanabe M, Mochida K, Kato T, Tabata S, Yoshimoto N, Noji M, Saito K (2008) Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyltransferase gene family in Arabidopsis. Plant Cell 20:2484–2496

    CAS  PubMed Central  PubMed  Google Scholar 

  • White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wirtz M, Berkowitz O, Droux M, Hell R (2001) The cysteine synthase complex from plants. Mitochondrial serine acetyltransferase from Arabidopsis thaliana carries a bifunctional domain for catalysis and protein-protein interaction. Eur J Biochem 268:686–693

    CAS  PubMed  Google Scholar 

  • Wirtz M, Droux M, Hell R (2004) O-acetylserine (thiol) lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J Exp Bot 55:1785–1798

    CAS  PubMed  Google Scholar 

  • Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell Online 10:1539–1550

    CAS  Google Scholar 

  • Yamaguchi Y, Nakamura T, Harada E, Koizumi N, Sano H (1999) Differential accumulation of transcripts encoding sulfur assimilation enzymes upon sulfur and/or nitrogen deprivation in Arabidopsis thaliana. Biosci Biotechnol Biochem 63:762–766

    CAS  PubMed  Google Scholar 

  • Yamakawa S, Sakuta C, Matsubayashi Y, Sakagami Y, Kamada H, Satoh S (1998) The promotive effects of a peptidyl plant growth factor, phytosulfokine-α, on the formation of adventitious roots and expression of a gene for a root-specific cystatin in cucumber hypocotyls. J Plant Res 111:453–458

    CAS  Google Scholar 

  • Yang H, Matsubayashi Y, Nakamura K, Sakagami Y (1999) Oryza sativa PSK gene encodes a precursor of phytosulfokine-alpha, a sulfated peptide growth factor found in plants. Proc Natl Acad Sci U S A 96:13560–13565

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang H, Matsubayashi Y, Hanai H, Sakagami Y (2000) Phytosulfokine-alpha, a peptide growth factor found in higher plants: its structure, functions, precursor and receptors. Plant Cell Physiol 41:825–830

    CAS  PubMed  Google Scholar 

  • Yang H, Matsubayashi Y, Nakamura K, Sakagami Y (2001) Diversity of Arabidopsis genes encoding precursors for phytosulfokine, a peptide growth factor. Plant Physiol 127:842–851

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yatusevich R, Mugford SG, Matthewman C, Gigolashvili T, Frerigmann H, Delaney S, Koprivova A, Flugge UI, Kopriva S (2010) Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J 62:1–11

    CAS  PubMed  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

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zamir D (2001) Improving plant breeding with exotic genetic libraries. Nat Rev Genet 2:983–989

    CAS  PubMed  Google Scholar 

  • Zhao F, McGrath SP (1994) Extractable sulphate and organic sulphur in soils and their availability to plants. Plant Soil 164:243–250

    CAS  Google Scholar 

  • Zhao FJ, Hawkesford MJ, Warrilow AGS, McGrath SP, Clarkson DT (1996) Responses of two wheat varieties to sulphur addition and diagnosis of sulphur deficiency. Plant Soil 181:317–327

    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

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Metabolic Biology, John Innes Centre, Norwich, UK

    Patrycja Baraniecka

  2. Botanical Institute, University of Cologne, Cologne, Germany

    Stanislav Kopriva

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  1. Patrycja Baraniecka
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  2. Stanislav Kopriva
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  1. Rothamsted Research, Harpenden, Hertfordshire, United Kingdom

    Malcolm J. Hawkesford

  2. Botanical Institute, University of Cologne, Cologne, Germany

    Stanislav Kopriva

  3. Laboratory of Plant Physiology, University of Groningen, Groningen, The Netherlands

    Luit J. De Kok

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Baraniecka, P., Kopriva, S. (2014). Macronutrient Use Efficiency – Sulfur in Arabidopsis thaliana . In: Hawkesford, M., Kopriva, S., De Kok, L. (eds) Nutrient Use Efficiency in Plants. Plant Ecophysiology, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-319-10635-9_3

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