Skip to main content
Log in

Sulfate assimilation and glutathione synthesis in C4 plants

Photosynthesis Research Aims and scope Submit manuscript

Abstract

Sulfate assimilation and glutathione synthesis were traditionally believed to be differentially compartmentalised in C4 plants with the synthesis of cysteine and glutathione restricted to bundle sheath and mesophyll cells, respectively. Recent studies, however, showed that although ATP sulfurylase and adenosine 5′ phosphosulfate reductase, the key enzymes of sulfate assimilation, are localised exclusively in bundle sheath in maize and other C4 monocot species, this is not true for the dicot C4 species of Flaveria. On the other hand, enzymes of glutathione biosynthesis were demonstrated to be active in both types of maize cells. Therefore, in this review the recent findings on compartmentation of sulfate assimilation and glutathione metabolism in C4 plants will be summarised and the consequences for our understanding of sulfate metabolism and C4 photosynthesis will be discussed.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • M Badiani, AR Paolacci, A D'Annibale and GG Sermanni, Antioxidants and photosynthesis in the leaves of Triticum durum L. seedlings acclimated to low, non-chilling temperature. J Plant Physiol 142 (1993) 18-24

    CAS  Google Scholar 

  • B Bassüner, O Keerberg, H Bauwe, T Pyarnik and H Keerberg, Photosynthetic CO2 metabolism in C3–C4 intermediate and C4 species of Flaveria (Asteraceae). Biochem Physiol Pflanzen 179 (1984) 631-634

    Google Scholar 

  • H Bauwe, Photosynthetic enzyme activities and immunofluorescence studies on the localization of ribulose-1, 5-bisphosphate carboxylase/oxygenase in leaves of C3, C4, and C3–C4 intermediate species of Flaveria (Asteraceae). Biochem Phys Pflanzen 179 (1984) 253-268

    CAS  Google Scholar 

  • TW Becker, C Perrot-Rechenmann, A Suzuki and B Hirel, Subcellular and immunocytochemical localization of the enzymes involved in ammonia assimilation in mesophyll and bundle-sheath cells of maize leaves. Planta 191 (1993) 129-136

    Article  CAS  Google Scholar 

  • A Bolchi, S Petrucco, PL Tenca, C Foroni and S Ottonello, 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 (1999) 527-537

    Article  PubMed  CAS  Google Scholar 

  • G Bowes, SK Rao, GM Estavillo and JB Reiskind, C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. Funct Plant Biol 29 (2002) 379-392

    Article  CAS  Google Scholar 

  • RH Brown, A difference in N use efficiency in C3 and C4 plants and its implications in adaptation and evolution. Crop Sci 18 (1978) 93-98

    Article  CAS  Google Scholar 

  • M Brunner, G Kocsy, A Rüegsegger, D Schmutz and C Brunold, Effect of chilling on assimilatory sulfate reduction and glutathione synthesis in maize. J Plant Physiol 146 (1995) 743-747

    CAS  Google Scholar 

  • C Brunold, Regulatory interactions between sulfate and nitrate assimilation. In: LJ De Kok (ed.) Sulfur Nutrition and Sulfur Assimilation in Higher Plants. The Hague: SPB Academic Publishing (1993) pp. 61-75

    Google Scholar 

  • M Burgener, M Suter, S Jones and C Brunold, Cyst(e)ine is the transport metabolite of assimilated sulfur from bundle-sheath to mesophyll cells in maize leaves. Plant Physiol 116 (1998) 1315-1322

    Article  PubMed  CAS  Google Scholar 

  • JN Burnell, Sulfate assimilation in C4 plants. Plant Physiol 75 (1984) 873-875

    PubMed  CAS  Google Scholar 

  • AG Doulis, N Debian, AH Kingston-Smith and CH Foyer, Differential localization of antioxidants in maize leaves. Plant Physiol 114 (1997) 1031-1037

    PubMed  CAS  Google Scholar 

  • M Droux, Plant serine acetyltransferase: new insights for regulation of sulphur metabolism in plant cells. Plant Physiol Biochem 41 (2003) 619-627

    Article  CAS  Google Scholar 

  • GE Edwards, VR Franceschi, MS Ku, EV Voznesenskaya, VI Pyankov and CS Andreo, Compartmentation of photosynthesis in cells and tissues of C4 plants. J Exp Bot 52 (2001) 577-590

    Article  PubMed  CAS  Google Scholar 

  • GE Edwards and SC Huber, The C4 pathway. In: MD Hatch and NK Boardman (eds.) Biochemistry of Plants. New York/London: Academic Press (1981) pp. 238-281

    Google Scholar 

  • GE Edwards and DA Walker, C3, C4: Mechanisms and Cellular and Environmental Regulation of Photosynthesis. Oxford: Blackwell Scientific (1983).

    Google Scholar 

  • CH Foyer and H Rennenberg, Regulation of glutathione synthesis and its role in abiotic and biotic stress defence. In: C Brunold (ed.) Sulfur Nutrition and Sulfur Assimilation in Higher Plants: Molecular, Biochemical and Physiological Aspects. Bern, Switzerland: Paul Haupt (2000) pp. 127-153

    Google Scholar 

  • BC Gerwick and CC Black, Sulfur assimilation in C4 plants. Plant Physiol 64 (1979) 590-593

    PubMed  CAS  Google Scholar 

  • BC Gerwick, SB Ku and CC Black, Initiation of sulfate activation: a variation in C4 photosynthesis plants. Science 209 (1980) 513-515

    Article  PubMed  CAS  Google Scholar 

  • O Ghannoum, JR Evans, WS Chow, TJ Andrews, JP Conroy and S Caemmerer von, Faster Rubisco is the key to superior nitrogen-use efficiency in NADP-malic enzyme relative to NAD-malic enzyme C4 grasses. Plant Physiol 137 (2005) 638-650

    Article  PubMed  CAS  Google Scholar 

  • LD Gómez, H Vanacker, P Buchner, G Noctor and CH Foyer, Intercellular distribution of glutathione synthesis in maize leaves and its response to short-term chilling. Plant Physiol 134 (2004) 1662-1671

    Article  PubMed  CAS  Google Scholar 

  • MD Hatch, C4 photosynthesis: a unique blend of modified biochemistry, anatomy, and ultrastructure. Biochim Biophys Acta 895 (1987) 81-106

    CAS  Google Scholar 

  • MD Hatch and CB Osmond, Compartmentation and transport in C4 photosynthesis. In: CR Stocking and U Heber (eds.) Encyclopedia of Plant Physiology, New Series. Berlin: Springer-Verlag (1976) pp. 144-184

    Google Scholar 

  • R Hell and L Bergmann, γ-glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localisation. Planta 180 (1990) 303-312

    Article  Google Scholar 

  • C Herschbach and H Rennenberg, Significance of phloem-translocated organic sulfur compounds for the regulation of sulfur nutrition. Prog Bot 62 (2001) 177-192

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • L Hopkins, S Parmar, DL Bouranis, JR Howarth and MJ Hawkesford, Coordinated expression of sulfate uptake and components of the sulfate assimilatory pathway in maize. Plant Biol 6 (2004) 408-414

    Article  PubMed  CAS  Google Scholar 

  • CM Hylton, S Rawsthorne, AM Smith, DA Jones and HW Woolhouse, Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C3–C4 intermediate species. Planta 175 (1988) 452-459

    Article  CAS  Google Scholar 

  • D Kast, M Stalder, A Rüegsegger, U Galli and C Brunold, Effects of NO2 and nitrate on sulfate assimilation in maize. J Plant Physiol 147 (1995) 9-14

    CAS  Google Scholar 

  • SL Ketchner and RT Sayre, Characterization of the expression of the Photosystem II-oxygen evolving complex in C4 species of Flaveria. Plant Physiol 98 (1992) 1154-1162

    Article  PubMed  CAS  Google Scholar 

  • G Kocsy, M Brunner, A Rüegsegger, P Stamp and C Brunold, Glutathione synthesis in maize genotypes with different sensitivities to chilling. Planta 198 (1996) 365-370

    Article  CAS  Google Scholar 

  • G Kocsy, G Galiba and C Brunold, Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol Plant 113 (2001) 158-164

    Article  PubMed  CAS  Google Scholar 

  • G Kocsy, G Owttrim, K Brander and C Brunold, Effect of chilling on the diurnal rhythm of enzymes involved in protection against oxidative stress in a chilling-tolerant and a chilling-sensitive maize genotype. Physiol Plant 99 (1997) 249-254

    Article  CAS  Google Scholar 

  • G Kocsy, G Szalai, A Vagujfalvi, L Stehli, G Orosz and G Galiba, Genetic study of glutathione accumulation during cold hardening in wheat. Planta 210 (2000) 295-301

    Article  PubMed  CAS  Google Scholar 

  • G Kocsy, P Ballmoos von, M Suter, A Ruüegsegger, U Galli, G Szalai, G Galiba and C Brunold, Inhibition of glutathione synthesis reduces chilling tolerance in maize. Planta 211 (2000) 528-536

    Article  PubMed  CAS  Google Scholar 

  • S Kopriva, C-C Chu and H Bauwe, Molecular phylogeny of Flaveria as deduced from the analysis of H-protein nucleotide sequences. Plant Cell Environ 19 (1996) 1028-1036

    Article  CAS  Google Scholar 

  • S Kopriva, S Jones, A Koprivova, M Suter, P Ballmoos von, K Brander, J Flückiger and C Brunold, Influence of chilling stress on the intercellular distribution of assimilatory sulfate reduction and thiols in Zea mays. Plant Biol 3 (2001) 24-31

    Article  CAS  Google Scholar 

  • S Kopriva and A Koprivova, Sulphate assimilation: a pathway which likes to surprise. In: YP Abrol and A Ahmad (eds.) Sulphur in Higher Plants. Dordrecht/Boston/London: Kluwer Academic Publishers (2003) pp. 87-112

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • S Kopriva, R Muheim, A Koprivova, N Trachsler, C Catalano, M Suter and C Brunold, Light regulation of assimilatory sulfate reduction in Arabidopsis thaliana. Plant J 20 (1999) 37-44

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • A Koprivova, M Melzer, P Ballmoos von, T Mandel, C Brunold and S Kopriva, Assimilatory sulfate reduction in C3, C3–C4, and C4 species of Flaveria. Plant Physiol 127 (2001) 543-550

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • MSB Ku, JR Wu, ZY Dai, RA Scott, C Chu and GE Edwards, Photosynthetic and photorespiratory characteristics of Flaveria species. Plant Physiol 96 (1991) 518-528

    PubMed  CAS  Google Scholar 

  • WM Laetsch, The C4 syndrome: a structural analysis. Annu Rev Plant Physiol 25 (1974) 27-52

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • T Matsumura, Y Kimata-Ariga, H Sakakibara, T Sugiyama, H Murata, T Takao, Y Shimonishi and T Hase, Complementary DNA cloning and characterization of ferredoxin localized in bundle-sheath cells of maize leaves. Plant Physiol 119 (1999) 481-488

    Article  PubMed  CAS  Google Scholar 

  • MJ May, T Vernoux, C Leaver, M Montagu van and D Inzé, Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49 (1998) 649-667

    Article  CAS  Google Scholar 

  • A Migge, C Bork, R Hell and TW Becker, Negative regulation of nitrate reductase gene expression by glutamine or asparagines accumulating in leaves of sulfur-deprived tobacco. Planta 211 (2000) 587-595

    Article  PubMed  CAS  Google Scholar 

  • RK Monson and BD Moore, On the significance of C3–C4 intermediate photosynthesis to the evolution of C4 photosynthesis. Plant Cell Environ 12 (1989) 689-699

    Article  CAS  Google Scholar 

  • RK Monson, BD Moore, MSB Ku and GE Edwards, Co-function of C3- and C4-photosynthetic pathways in C3, C4 and C3–C4 intermediate Flaveria species. Planta 168 (1986) 493-502

    Article  CAS  Google Scholar 

  • R Moore and CC Black, Nitrogen assimilation pathways in leaf mesophyll and bundle sheath cells of C4 photosynthesis plants formulated from comparative studies with Digitaria sanguinalis (L.) Scop. Plant Physiol 64 (1979) 309-313

    PubMed  CAS  Google Scholar 

  • U Neuenschwander, M Suter and C Brunold, Regulation of sulfate assimilation by light and O-acetyl-L-serine in Lemna minor L. Plant Physiol 97 (1991) 253-258

    Article  PubMed  CAS  Google Scholar 

  • G Noctor, A-CM Arisi, L Jouanin, KJ Kunert, H Rennenberg and CH Foyer, Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49 (1998) 623-647

    Article  CAS  Google Scholar 

  • G Noctor and CH Foyer, Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49 (1998) 249-279

    Article  PubMed  CAS  Google Scholar 

  • M Noji, K Inoue, N Kimura, A Gouda and K Saito, Isoform-dependent differences in feedback regulation and subcellular localization of serine acetyltransferase involved in cysteine biosynthesis from Arabidopsis thaliana. J Biol Chem 273 (1998) 32739-32745

    Article  PubMed  CAS  Google Scholar 

  • S Nussbaum, K Schmutz and C Brunold, Regulation of assimilatory sulfate reduction by cadmium in Zea mays L. Plant Physiol 88 (1988) 1407-1410

    PubMed  CAS  Google Scholar 

  • C Passera and R Ghisi, ATP sulphurylase and O-acetylserine sulphydrylase in isolated mesophyll protoplasts and bundle sheath strands of S-deprived maize leaves. J Exp Bot 33 (1982) 432-438

    Article  CAS  Google Scholar 

  • GM Pastori, PM Mullineaux and CH Foyer, Post-transcriptional regulation prevents accumulation of glutathione reductase protein and activity in the bundle sheath cells of maize. Plant Physiol 122 (2000) 667-675

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • CKM Rathnam and GE Edwards, Distribution of nitrate-assimilating enzymes between mesophyll protoplasts and bundle sheath cells in leaves of three groups of C-4 plants. Plant Physiol 57 (1976) 881-885

    Article  PubMed  CAS  Google Scholar 

  • S Rawsthorne, C3–C4 intermediate photosynthesis – linking physiology to gene expression. Plant J 2 (1992) 267-274

    Article  CAS  Google Scholar 

  • JR Reinfelder, AM Kraepiel and FM Morel, Unicellular C4 photosynthesis in a marine diatom. Nature 407 (2000) 996-999

    Article  PubMed  CAS  Google Scholar 

  • Z Reuveny, DK Dougall and PM Trinity, Regulatory coupling of nitrate and sulfate assimilation pathways in cultured tobacco cells. Proc Natl Acad Sci USA 77 (1980) 6670-6672

    Article  PubMed  CAS  Google Scholar 

  • A Rüegsegger and C Brunold, Effect of cadmium on γ-glutamylcysteine synthesis in maize seedlings. Plant Physiol 99 (1992) 428-433

    PubMed  Google Scholar 

  • M Saccomani, G Cacco and G Ferrari, Efficiency of the first steps of sulfate utilization by maize hybrids in relation to their productivity. Physiol Plant 53 (1984) 101-104

    Article  Google Scholar 

  • D Schmutz and C Brunold, Intercellular localization of assimilatory sulfate reduction in leaves of Zea mays and Triticum aestivum. Plant Physiol 74 (1984) 866-870

    Article  PubMed  CAS  Google Scholar 

  • D Schmutz and C Brunold, Localization of nitrite and sulfite reductase in bundle sheath and mesophyll cells of maize leaves. Physiol Plant 64 (1985) 523-528

    Article  CAS  Google Scholar 

  • J Sheen, C4 gene expression. Annu Rev Plant Physiol Plant Mol Biol 50 (1999) 187-217

    Article  PubMed  CAS  Google Scholar 

  • LM Tabe and M Droux, Limits to sulfur accumulation in transgenic lupin seeds expressing a foreign sulfur-rich protein. Plant Physiol 128 (2002) 1137-1148

    Article  PubMed  CAS  Google Scholar 

  • P Vauclare, S Kopriva, D Fell, M Suter, L Sticher, P Ballmoos von, U Krähenbühl, R Opden Camp and C Brunold, Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible to negative control by thiols than ATP sulphurylase. Plant J 31 (2002) 729-740

    Article  PubMed  CAS  Google Scholar 

  • KC Vaughn and WH Campbell, Immunogold localization of nitrate reductase in maize leaves. Plant Physiol 88 (1988) 1354-1357

    PubMed  CAS  Google Scholar 

  • EV Voznesenskaya, VR Franceschi, O Kiirats, H Freitag and GE Edwards, Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414 (2001) 543-546

    Article  PubMed  CAS  Google Scholar 

  • A Wachter, S Wolf, H Steininger, J Bogs and T Rausch, Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J 41 (2005) 15-30

    Article  PubMed  CAS  Google Scholar 

  • MA Walker and BD McKersie, Role of the ascorbate-glutathione antioxidant system in chilling resistance of tomato. J Plant Physiol 141 (1993) 234-239

    CAS  Google Scholar 

  • S Westerman, I Stulen, M Suter, C Brunold and JL De Kok, Atmospheric H2S as sulphur source for Brassica oleracea: consequences for the activity of the enzymes of the assimilatory sulphate reduction pathway. Plant Physiol Biochem 39 (2001) 425-432

    Article  CAS  Google Scholar 

  • K Yonekura-Sakakibara, Y Onda, T Ashikari, Y Tanaka, T Kusumi and T Hase, Analysis of reductant supply systems for ferredoxin-dependent sulfite reductase in photosynthetic and nonphotosynthetic organs of maize. Plant Physiol 122 (2000) 887-894

    Article  PubMed  CAS  Google Scholar 

  • P Zimmermann, M Hirsch-Hoffmann, L Hennig and W Gruissem, GENEVESTIGATOR. Arabidopsis Microarray Database and Analysis Toolbox. Plant Physiol 136 (2004) 2621-2632

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stanislav Kopriva.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kopriva, S., Koprivova, A. Sulfate assimilation and glutathione synthesis in C4 plants. Photosynth Res 86, 363–372 (2005). https://doi.org/10.1007/s11120-005-3482-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-005-3482-z

Keywords

Navigation