Preferences help
enabled [disable] Abstract
Number of results
2008 | 55 | 3 | 457-471
Article title

Recent advances in understanding plant response to sulfur-deficiency stress

Title variants
Languages of publication
Sulfur is an essential macronutrient for all living organisms. Plants are able to assimilate inorganic sulfur and incorporate it into organic compounds, while animals rely entirely on organic sources of sulfur. In the last decades sulfate availability in soils has become the major limiting factor for plant production in many countries due to significant reduction of anthropogenic sulfur emission forced by introducing stringent environmental legislation. The sulfur flux after transferring plants from optimal conditions to sulfur deficiency is regulated on multiple levels including transcription, translation and activity of enzymes needed for sulfate assimilation and synthesis of sulfur-containing metabolites. Most of these regulatory steps are not yet fully characterized. Plant responses to sulfur limitation are complex and can be divided into phases depending on the degree of sulfur shortage. The initial responses are limited to adaptations within sulfur metabolic pathway, while multiple metabolic pathways and developmental process are affected when sulfur shortage becomes more severe. The major aim of this work is a comprehensive review of recent progress in understanding the regulation of plant adaptations to sulfur deficit.
Physical description
  • Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warszawa, Poland
  • Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warszawa, Poland
  • Adai A, Johnson C, Mlotshwa S, Archer-Evans S, Manocha V, Vance V, Sundaresan V (2005) Computational prediction of miRNAs in Arabidopsis thaliana. Genome Res 15: 78-91.
  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221.
  • Bick JA, Setterdahl AT, Knaff DB, Chen Y, Pitcher LH, Zilinskas BA, Leustek T (2001) Regulation of the plant-type 5'-adenylyl sulfate reductase by oxidative stress. Biochemistry 40: 9040-9048.
  • Blaszczyk A, Brodzik R, Sirko A (1999) Increased resistance to oxidative stress in transgenic tobacco plants overexpressing bacterial serine acetyltransferase. Plant J 20: 237-243.
  • Bolchi A, Petrucco S, Tenca PL, Foroni C, Ottonello S (1999) Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response to variations in sulfur nutritional status: stereospecific down-regulation by l-cysteine. Plant Mol Biol 39: 527-537.
  • Bonner ER, Cahoon RE, Knapke SM, Jez JM (2005) Molecular basis of cysteine biosynthesis in plants: structural and functional analysis of O-acetylserine sulfhydrylase from Arabidopsis thaliana. J Biol Chem 280: 38803-38813.
  • Bourgis F, Roje S, Nuccio ML, Fisher DB, Tarczynski MC, Li C, Herschbach C, Rennenberg H, Pimenta MJ, Shen TL, Gage DA, 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: 1485-1498.
  • Buchner P, Stuiver CE, 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.
  • Burkhard P, Rao GS, Hohenester E, Schnackerz KD, Cook PF, Jansonius JN (1998) Three-dimensional structure of O-acetylserine sulfhydrylase from Salmonella typhimurium. J Mol Biol 283: 121-133.
  • Campanini B, Raboni S, Vaccari S, Zhang L, Cook PF, Hazlett TL, Mozzarelli A, Bettati S (2003) Surface-exposed tryptophan residues are essential for O-acetylserine sulfhydrylase structure, function, and stability. J Biol Chem 278: 37511-37519.
  • Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79: 331-348.
  • 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.
  • El Kassis E, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian JC (2007) Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 143: 1231-1241.
  • Falkenberg B, Witt I, Zanor MI, Steinhauser D, Mueller-Roeber B, Hesse H, Hoefgen R (2008) Transcription factors relevant to auxin signalling coordinate broad-spectrum metabolic shifts including sulphur metabolism. J Exp Bot 59: 2831-2846.
  • Fontecave M, Atta M, Mulliez E (2004) S-adenosylmethionine: nothing goes to waste. Trends Biochem Sci 29: 243-249.
  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17: 1866-1875.
  • 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.
  • Giordano M, Norici A, Hell R (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166: 371-382.
  • Gonzalez-Ballester D, Pollock SV, Pootakham W, Grossman AR (2008) The central role of a SNRK2 kinase in sulfur deprivation responses. Plant Physiol 147: 216-227.
  • Gorman J, Shapiro L (2004) Structure of serine acetyltransferase from Haemophilus influenzae Rd. Acta Crystallogr D Biol Crystallogr 60: 1600-1605.
  • Granvogl M, Wieser H, Koehler P, Tucher SV, Schieberle P (2007) Influence of sulfur fertilization on the amounts of free amino acids in wheat. correlation with baking properties as well as with 3-aminopropionamide and acrylamide generation during baking. J Agric Food Chem 55: 4271-4277.
  • Grimble RF (1994) Sulphur amino acids and the metabolic response to cytokines. Adv Exp Med Biol 359: 41-49.
  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10: 453-460.
  • Hansch R, Lang C, Rennenberg H, Mendel RR (2007) Significance of plant sulfite oxidase. Plant Biol 9: 589-595.
  • Harms K, von Ballmoos P, Brunold C, Hofgen R, Hesse H (2000) Expression of a bacterial serine acetyltransferase in transgenic potato plants leads to increased levels of cysteine and glutathione. Plant J 22: 335-343.
  • 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.
  • Hawkesford MJ (2003) Transporter gene families in plants: the sulphate transporter gene family - redundancy or specialization? Physiol Plant 117: 155-163.
  • Hawkesford MJ, De Kok LJ (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29: 382-395.
  • Heeg C, Kruse C, Jost R, Gutensohn M, Ruppert T, Wirtz M, Hell R (2008) Analysis of the Arabidopsis O-acetylserine(thiol)lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. Plant Cell 20: 168-185.
  • Hell R, Hillebrand H (2001) Plant concepts for mineral acquisition and allocation. Curr Opin Biotechnol 12: 161-168.
  • Herschbach C, van Der Zalm E, Schneider A, Jouanin L, De Kok LJ, Rennenberg H (2000) Regulation of sulfur nutrition in wild-type and transgenic poplar over-expressing gamma-glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. Plant Physiol 124: 461-473.
  • Hesse H, Nikiforova V, Gakiere B, Hoefgen R (2004) Molecular analysis and control of cysteine biosynthesis: integration of nitrogen and sulphur metabolism. J Exp Bot 55: 1283-1292.
  • Hicks LM, Cahoon RE, Bonner ER, Rivard RS, Sheffield J, Jez JM (2007) Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. Plant Cell 19: 2653-2661.
  • Hindson VJ, Shaw WV (2003) Random-order ternary complex reaction mechanism of serine acetyltransferase from Escherichia coli. Biochemistry 42: 3113-3119.
  • Hirai MY, Saito K (2004) Post-genomics approaches for the elucidation of plant adaptive mechanisms to sulphur deficiency. J Exp Bot 55: 1871-1879.
  • Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33: 651-663.
  • Hirai MY, Klein M, Fujikawa Y, Yano M, Goodenowe DB, Yamazaki Y, Kanaya S, Nakamura Y, Kitayama M, Suzuki H, Sakurai N, Shibata D, Tokuhisa J, Reichelt M, Gershenzon J, Papenbrock J, Saito K (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem 280: 25590-25595.
  • 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 USA 104: 6478-6483.
  • Hoefgen R, Nikiforova VJ (2008) Metabolomics integrated with transcriptomics: assessing systems response to sulfur-deficiency stress. Physiol Plant 132: 190-198.
  • 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.
  • Huang B, Vetting MW, Roderick SL (2005) The active site of O-acetylserine sulfhydrylase is the anchor point for bienzyme complex formation with serine acetyltransferase. J Bacteriol 187: 3201-3205.
  • Hunter EA, Grimble RF (1997) Dietary sulphur amino acid adequacy influences glutathione synthesis and glutathione-dependent enzymes during the inflammatory response to endotoxin and tumour necrosis factor-alpha in rats. Clin Sci (Lond) 92: 297-305.
  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787-799.
  • Kasajima I, Ohkama-Ohtsu N, Ide Y, Hayashi H, Yoneyama T, Suzuki Y, Naito S, Fujiwara T (2007) The BIG gene is involved in regulation of sulfur deficiency-responsive genes in Arabidopsis thaliana. Physiol Plant 129: 351-363.
  • Kimura T, Shibagaki N, Ohkama-Ohtsu N, Hayashi H, Yoneyama T, Davies JP, Fujiwara T (2006) Arabidopsis SNRK2.3 protein kinase is involved in the regulation of sulfur-responsive gene expression and O-acetyl-l-serine accumulation under limited sulfur supply. Soil Sci Plant Nutr 52: 211-220.
  • Klein M, Papenbrock J (2004) The multi-protein family of Arabidopsis sulphotransferases and their relatives in other plant species. J Exp Bot 55: 1809-1820.
  • Knop M, Pacyna S, Voloshchuk N, Kant S, Mullenborn C, Steiner U, Kirchmair M, Scherer HW, Schulz M (2007) Zea mays: benzoxazolinone detoxification under sulfur deficiency conditions - a complex allelopathic alliance including endophytic Fusarium verticillioides. J Chem Ecol 33: 225-237.
  • Komarnisky LA, Christopherson RJ, Basu TK (2003) Sulfur: its clinical and toxicologic aspects. Nutrition 19: 54-61.
  • Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97: 479-495.
  • Kopriva S, Koprivova A (2003) Sulphate assimilation: a pathway which likes to surprise. In Sulphur in Higher Plants. Abrol YP, Ahmad A, eds, pp 87-112. Kluwer Academic Publishers, Dordrecht.
  • Kopriva S, Wiedemann G, Reski R (2007) Sulfate assimilation in basal land plants - what does genomic sequencing tell us? Plant Biol 9: 556-564.
  • Koprivova A, Suter M, den Camp RO, Brunold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122: 737-746.
  • Koprivova A, Meyer AJ, Schween G, Herschbach C, Reski R, Kopriva S (2002) Functional knockout of the adenosine 5'-phosphosulfate reductase gene in Physcomitrella patens revives an old route of sulfate assimilation. J Biol Chem 277: 32195-32201.
  • 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 (1996) Biosynthesis of cysteine. In Escherichia coli and Salmonell typhimurium. Neidhardt FC, Curtiss R, Ingraham JL, Linn ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umberger M, eds. Cellular and Molecular Biology, pp 514-752. ASM Press, Washington DC.
  • Kruse C, Jost R, Lipschis M, Kopp B, Hartmann M, Hell R (2007) Sulfur-enhanced defence: effects of sulfur metabolism, nitrogen supply, and pathogen lifestyle. Plant Biol 9: 608-619.
  • Lang C, Popko J, Wirtz M, Hell R, Herschbach C, Kreuzwieser J, Rennenberg H, Mendel RR, Hansch R (2007) Sulphite oxidase as key enzyme for protecting plants against sulphur dioxide. Plant Cell Environ 30: 447-455.
  • Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO42- uptake in intact canola (the role of phloem-translocated glutathione). Plant Physiol 111: 147-157.
  • Lappartient AG, Vidmar JJ, Leustek T, Glass AD, 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.
  • Leustek T (2002) Sulfate metabolism. In The Arabidopsis Book. Somerville CR, Meyerowitz EM, eds, American Society of Plant Biologists, Rockville, MD, doi: 10.1199/tab.0009,
  • Lewandowska M, Wawrzynska A, Kaminska J, Liszewska F, Sirko A (2005) Identification of novel proteins of Nicotiana tabacum regulated by short term sulfur starvation. In Sulfur Transport and Assimilation in Plants in the Postgenomic Era. Saito K, De Kok LJ, Stuhlen I, Hawkesford MJ, Schnug E, Sirko A, Rennenberg H, eds, pp 153-156. Backhuys Publishers, Leiden, The Netherlands
  • Liu F, Yoo BC, Lee JY, Pan W, Harmon AC (2006) Calcium-regulated phosphorylation of soybean serine acetyltransferase in response to oxidative stress. J Biol Chem 281: 27405-27415.
  • Marshner H (2005) Mineral Nutrition of Higher Plants. Second edition. Elsevier Academic Press, London, UK.
  • 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.
  • 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.
  • 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.
  • Migge A, Bork C, Hell R, Becker TW (2000) Negative regulation of nitrate reductase gene expression by glutamine or asparagine accumulating in leaves of sulfur-deprived tobacco. Planta 211: 587-595.
  • Muttucumaru N, Halford NG, Elmore JS, Dodson AT, Parry M, Shewry PR, Mottram DS (2006) Formation of high levels of acrylamide during the processing of flour derived from sulfate-deprived wheat. J Agric Food Chem 54: 8951-8955.
  • Neuenschwander U, Suter M, Brunold C (1991) Regulation of sulfate assimilation by light and O-acetyl-l-serine in Lemna minor L. Plant Physiol 97: 253-258.
  • 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.
  • Nikiforova VJ, Gakiere B, Kempa S, Adamik M, Willmitzer L, Hesse H, Hoefgen R (2004) Towards dissecting nutrient metabolism in plants: a systems biology case study on sulphur metabolism. J Exp Bot 55: 1861-1870.
  • Nikiforova VJ, Daub CO, Hesse H, Willmitzer L, Hoefgen R (2005a) Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. J Exp Bot 56: 1887-1896.
  • Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005b) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138: 304-318.
  • Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141: 1138-1148.
  • Noctor G (2006) Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ 29: 409-425.
  • 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.
  • Norici A, Hell R, Giordano M (2005) Sulfur and primary production in aquatic environments: an ecological perspective. Photosynth Res 86: 409-417.
  • 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.
  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants - from the field to the test tube and back. Plant Biol 9: 582-588.
  • 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.
  • Pye VE, Tingey AP, Robson RL, Moody PC (2004) The structure and mechanism of serine acetyltransferase from Escherichia coli. J Biol Chem 279: 40729-40736.
  • Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10: 503-509.
  • Rennenberg H, Schmitz K, Bergmann L (1979) Long-distance transport of sulfur in Nicotiana tabacum. Planta 147: 57-62.
  • Riemenschneider A, Riedel K, Hoefgen R, Papenbrock J, Hesse H (2005a) Impact of reduced O-acetylserine(thiol)lyase isoform contents on potato plant metabolism. Plant Physiol 137: 892-900.
  • Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005b) Isolation and characterization of a d-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J 272: 1291-1304.
  • Roje S (2006) S-Adenosyl-l-methionine: beyond the universal methyl group donor. Phytochemistry 67: 1686-1698.
  • Rouached H, Berthomieu P, El Kassis E, Cathala N, Catherinot V, Labesse G, Davidian JC, 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.
  • Rouached H, Wirtz M, Alary R, Hell R, Arpat AB, Davidian JC, 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.
  • Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136: 2443-2450.
  • Scherer HW (2001) Sulphur in crop production - invited paper. Eur J Agron 14: 81-111.
  • Sekine K, Fujiwara M, Nakayama M, Takao T, Hase T, Sato N (2007) DNA binding and partial nucleoid localization of the chloroplast stromal enzyme ferredoxin:sulfite reductase. FEBS J 274: 2054-2069.
  • Shibagaki N, Grossman AR (2004) Probing the function of STAS domains of the Arabidopsis sulfate transporters. J Biol Chem 279: 30791-30799.
  • Shibagaki N, Grossman AR (2006) The role of the STAS domain in the function and biogenesis of a sulfate transporter as probed by random mutagenesis. J Biol Chem 281: 22964-22973.
  • Sirko A, Blaszczyk A, Liszewska F (2004) Overproduction of SAT and/or OASTL in transgenic plants: a survey of effects. J Exp Bot 55: 1881-1888.
  • 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.
  • Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12: 301-309.
  • Tai CH, Burkhard P, Gani D, Jenn T, Johnson C, Cook PF (2001) Characterization of the allosteric anion-binding site of O-acetylserine sulfhydrylase. Biochemistry 40: 7446-7452.
  • Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JA, 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.
  • 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.
  • 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.
  • Vestreng V, Myhre G, Fagerli H, Reis S, Tarrason L (2007) Twenty-five years of continuous sulphur dioxide emission reduction in Europe. Atmosph Chem Phys 7: 3663-3681.
  • Vidmar JJ, Schjoerring JK, Touraine B, Glass AD (1999) Regulation of the hvst1 gene encoding a high-affinity sulfate transporter from Hordeum vulgare. Plant Mol Biol 40: 883-892.
  • 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. FEBS Lett 475: 65-69.
  • Wawrzynska A, Lewandowska M, Hawkesford MJ, Sirko A (2005) Using a suppression subtractive library-based approach to identify tobacco genes regulated in response to short-term sulphur deficit. J Exp Bot 56: 1575-1590.
  • Wawrzynski A, Kopera E, Wawrzynska A, Kaminska J, Bal W, Sirko A (2006) Effects of simultaneous expression of heterologous genes involved in phytochelatin biosynthesis on thiol content and cadmium accumulation in tobacco plants. J Exp Bot 57: 2173-2182.
  • Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth Res 86: 345-362.
  • Wirtz M, Hell R (2007) Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19: 625-639.
  • Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10: 1539-1550.
  • Yamahuchi Y, Nakamura T, Harada E, Koizumi N, Sano H (1997) Isolation and characterization of a cDNA encoding sulfate transporter from Arabidopsis thaliana. Plant Physiol 113: 1463.
  • Yan X, Chen S (2007) Regulation of plant glucosinolate metabolism. Planta 226: 1343-1352.
  • 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.
  • 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.
  • Zhao FJ, Hawkesford MJ, McGrath SP (1999) Sulphur assimilation and effects on yield and quality of wheat. J Cereal Sci 30: 1-17.
  • Zhao FJ, Fortune S, Barbosa VL, McGrath SP, Stobart R, Bilsborrow PE, Booth EJ, Brown A, Robson P (2006) Effects of sulphur on yield and malting quality of barley. J Cereal Sci 43: 369-377.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.