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Significance of Phloem-Translocated Organic Sulfur Compounds for the Regulation of Sulfur Nutrition

  • Cornelia Herschbach
  • Heinz Rennenberg
Part of the Progress in Botany book series (BOTANY, volume 62)

Abstract

Sulfur is an essential nutrient of all living organisms. In plants, it is fifth or sixth in order of elemental abundance, after hydrogen, oxygen, carbon, nitrogen and phosphorus (Pitman and Cram 1977; Raven 1980; Cram 1990). Reduced-sulfur, i.e. sulfur in the oxidation state -2, is the most important form of sulfur in living cells. It supports the specific conformations and functions of enzymes and structural proteins via reactive sulfide moieties and disulfide bonds. Sulfur is available for plants mainly as sulfate at the roots (Rennenberg 1984). Therefore, sulfate has to be activated, reduced to sulfide and incorporated into carbohydrate skeletons by assimilatory sulfate reduction before it can be used in protein synthesis (Brunold 1990, 1993). The final product of assimilatory sulfate reduction in plants is cysteine. From this amino acid, all other reduced-sulfur compounds, including methionine (Giovanelli 1990), glutathione (Bergmann and Rennenberg 1993), the S-alkylcysteine sulfoxides of Liliacea., the isothiocyanates of Brassicacea. (Schnug 1990) and phytochelatins (Rauser 1995), are synthesized in a whole set of metabolic pathways. In most plant species, a specific sulfur/nitrogen (S/N) ratio of approximately 1/20 reflects the relationship of these macro-nutrients in protein (Dijkshoorn and Van Wijk 1967).

Keywords

Sulfate Transporter Sulfate Uptake Transgenic Poplar Phloem Exudate Assimilatory Sulfate Reduction 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Alosi MC, Melroy DL, Park RB (1988) The regulation of gelation of phloem exudate from Cucurbit. fruit by dilution, glutathione, and glutathione reductase. Plant Physiol 86:1089–1094PubMedCrossRefGoogle Scholar
  2. Bell CI, Cram WJ, Clarkson DT (1994) Compartmental analysis of 35SO4 2- exchange kinetics in roots and leaves of a tropical legume Macroptilium atropurpureu. cv. Sirato. J Exp Bot 45:879–886CrossRefGoogle Scholar
  3. Bell CI, Clarkson DT, Cram WJ (1995) Sulfate supply and its regulation of transport in roots of a tropical legume Macroptilium atropurpureu. cv. Sirato. J Exp Bot 46:65–71CrossRefGoogle Scholar
  4. Bergmann L, Rennenberg H (1993) Glutathione metabolism in plants. In: De Kok LJ, Stulen I, Rennenberg H, Brunold C, Rauser WE (eds) Sulfur nutrition and assimilation in higher plants. SPB Academic Publishing, The Hague, pp 109–123Google Scholar
  5. Biddulph O, Cory R, Biddulph S (1956) The absorption and translocation of sulfur in red kidney bean. Plant Physiol 31:28–33PubMedCrossRefGoogle Scholar
  6. Biddulph O, Biddulph S, Cory R, Koontz H (1958) Circulation patterns for phosphorus, sulfur and calcium in the bean plant. Plant Physiol 33:293–300PubMedCrossRefGoogle Scholar
  7. Bohlmann H (1993) Significance of sulfur-rich proteins in seeds and leaves. In: DeKok LJ, Stulen I, Rennenberg H, Brunold C, Rauser WE (eds) Sulfur nutrition and assimilation in higher plants. SPB Academic Publishing, The Hague, pp 211–219Google Scholar
  8. 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 39:527–537PubMedCrossRefGoogle Scholar
  9. Bonas U, Schmitz K, Rennenberg H, Bergmann L (1982) Phloem transport of sulfur in Ricinus. Planta 155:82–88CrossRefGoogle Scholar
  10. Bourgis F, Roje S, Nuccio ML, Fisher DB, Tarczynski MC, Herschbach C, Rennenberg H, Pimenta MJ, Shen T-L, Gage DA, Hanson AD (1999) S-Methylmethionine has a major role in phloem sulfur transport, and is synthesised by a novel type of methyltrans-ferase. Plant Cell 11:1485–1497PubMedGoogle Scholar
  11. Brunold C (1990) Reduction of sulfate to sulfide. In: Rennenberg H, Brunold C, De Kok LJ, Stulen I (eds) Sulfur nutrition and sulfur assimilation in higher plants. SPB Academic Publishing, The Hague, pp 13–31Google Scholar
  12. Brunold C (1993) Regulatory interactions between sulfate and nitrate assimilation. In: DeKok LJ, Stulen I, Rennenberg H, Brunold C, Rauser WE (eds) Sulfur nutrition and assimilation in higher plants. SPB Academic Publishing, The Hague, pp 61–75Google Scholar
  13. Brunold C, Suter M (1989) Localisation of enzymes of assimilatory sulfate reduction in pea roots. Planta 179:228–234CrossRefGoogle Scholar
  14. Cacco G, Ferrari G, Saccomani M (1980) Pattern of sulfate uptake during root elongation in maize: its correlation with productivity. Physiol Plant 48:375–378CrossRefGoogle Scholar
  15. Clarkson DT, Smith FW, Vanden Berg PJ (1983) Regulation of sulfate transport in a tropical legume, Macroptilium atropurpureu., cv. siratro. J Exp Bot 34:1463–1483CrossRefGoogle Scholar
  16. Clarkson DT, Saker LR, Purves JV (1989) Depression of nitrate and ammonium transport in barley plants with diminished sulfate status. Evidence of co-regulation of nitrogen and sulfate intake. J Exp Bot 40:953–963CrossRefGoogle Scholar
  17. Clarkson DT, Hawkesford MJ, Davidian J-C, Grignon C (1992) Contrasting responses of sulfate and phosphate transport in barley (Hordeum vulgar. L.) roots to protein-modifying reagents and inhibition of protein synthesis. Planta 187:306–314CrossRefGoogle Scholar
  18. Clarkson DT, Hawkesford MJ, Davidian J-C (1993) Membrane and long-distance transport of sulfate. In: De Kok LJ, Stulen I, Rennenberg H, Brunold C, Rauser WE (eds) Sulfur nutrient and sulfur assimilation in higher plants. SPB Academic Publishing, The Hague, pp 3–19Google Scholar
  19. Clarkson DT, Diogo E, Amâncio S (1999) Uptake and assimilation of sulfate by sulfur deficient Zea may. cells: the role of O-acetyl-L-serine in the interaction between nitrogen and sulfur assimilation pathways. Plant Physiol Biochem 37:283–290CrossRefGoogle Scholar
  20. Cram WJ (1983a) Characteristics of sulfate transport across plasmalemma and tonoplasts of carrot root cells. Plant Physiol 72:204–211PubMedCrossRefGoogle Scholar
  21. Cram WJ (1983b) Sulfate accumulation is regulated at the tonoplast. Plant Sci Lett 31:329–338CrossRefGoogle Scholar
  22. Cram WJ (1990) Uptake and transport of sulfate. In: Rennenberg H, Brunold C, De Kok LJ, Stulen I (eds) Sulfur nutrient and sulfur assimilation in higher plants. SPB Academic Publishing, The Hague, pp 3–11Google Scholar
  23. Datko AH, Mudd SH (1984a) Sulfate uptake and its regulation in Lemna paucicostat. Hegelm. 6746. Plant Physiol 75:466–473PubMedCrossRefGoogle Scholar
  24. Datko AH, Mudd SH (1984b) Responses of sulfur-containing compounds in Lemna paucicostat. Hegelm. 6746 to changes in availability of sulfur sources. Plant Physiol 75:474–479PubMedCrossRefGoogle Scholar
  25. De Kok LJ (1990) Sulfur metabolism in plants exposed to atmospheric sulfur. In: Rennenberg H, Brunold C, De Kok LJ, Stulen I (eds) Sulfur nutrition and sulfur assimilation in higher plants. SPB Academic Publishing, The Hague, pp 111–130Google Scholar
  26. Deane-Drummond CE (1987) The regulation of sulfate uptake following growth of Pisum sativu. L. seedlings in S nutrient limiting conditions. Interaction between nitrate and sulfate transport. Plant Sci 50:27–35CrossRefGoogle Scholar
  27. Dijkshoorn W, Van Wijk AL (1967) The sulfur requirements of plants as evidenced by the sulfur-nitrogen ratio in the organic matter. A review of published data. Plant Soil 26:129–157CrossRefGoogle Scholar
  28. Evans LT (1975) Sulfur in agriculture. In: McLachlan KD (ed) Sulfur in Australian agriculture. Sydney University Press, Sydney, pp 3–9Google Scholar
  29. Ferrari G, Renosto F (1972) Regulation of sulfate uptake by excised barley roots in the presence of selenate. Plant Physiol 49:114–116PubMedCrossRefGoogle Scholar
  30. Gessler A, Schulte M, Schrempp S, Rennenberg H (1998) Interaction of phloem-translocated amino compounds with nitrate net uptake by the roots of beech (Fagus sylvatic.) seedlings. J Exp Bot 49:1529–1537CrossRefGoogle Scholar
  31. Giovanelli J (1990) Regulatory aspects of cysteine and methionine synthesis. In: Rennenberg H, Brunold C, De Kok LJ, Stulen I (eds) Sulfur nutrition and sulfur assimilation in higher plants. SPB Academic Publishing, The Hague, pp 33–48Google Scholar
  32. Hart JW, Filner P (1969) Regulation of sulfate uptake by amino acids in cultured tobacco cells. Plant Physiol 44:1253–1259PubMedCrossRefGoogle Scholar
  33. Hartmann T, Mult S, Suter M, Rennenberg H, Herschbach C (2000a) Leaf age-dependent differences in sulfur assimilation and allocation in poplar (Populus tremul. x P. alb.). J Exp Bot 51 51:1077–1088PubMedCrossRefGoogle Scholar
  34. Hartmann T, Kopriva S, Von Ballmoos P, Suter M, Jouanin L, Rennenberg H (2000b) Interaction of overexpressing of γ-glutamylcysteine synthetase with the regulation of assimilatory sulfate reduction in poplar (Populus tremul. x P. alb.) leaves. J Exp Bot (submitted)Google Scholar
  35. Hatzfeld Y, Cathala N, Grignon C, Davidian J-C (1998) Effect of ATP sulfurylase overex-pression in bright yellow 2 tobacco cells. Plant Physiol 116:1307–1313PubMedCrossRefGoogle Scholar
  36. Hawkesford MJ, Belcher AR (1991) Differential protein synthesis in response to sulfate and phosphate deprivation. Planta 185:323–329CrossRefGoogle Scholar
  37. Hawkesford MJ, Smith FW (1997) Molecular biology of higher plant sulfate transportes. In: Cram WJ, De Kok LJ, Stulen I, Brunold C, Rennenberg H (eds) Sulfur metabolism in higher plants molecular, ecophysiological and nutritional aspects. Backhuys, Leiden, pp 13–25Google Scholar
  38. Hawkesford MJ, Davidian J-C, Grignion C (1993) Sulfate/proton cotransport in plasma-membrane vesicles isolated from roots of Brassica napu. L.: increased transport in membranes isolated from sulfur-starved plants. Planta 190:297–304CrossRefGoogle Scholar
  39. Heiss S, Schäfer HJ, Haag-Kerwer A, Rausch T (1999) Cloning sulfur assimilation genes of Brassica junce. L.: cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase. Plant Mol Biol 39:847–857PubMedCrossRefGoogle Scholar
  40. Herschbach C, Rennenberg H (1991) Influence of glutathione (GSH) on sulfate influx, xylem loading and exudation in excised tobacco roots. J Exp Bot 42:1021–1029CrossRefGoogle Scholar
  41. Herschbach C, Rennenberg H (1994) Influence of glutathione (GSH) on net uptake of sulfate and sulfate transport in tobacco plants. J Exp Bot 45:1069–1076CrossRefGoogle Scholar
  42. Herschbach C, Rennenberg H (1995) Long-distance transport of 35S-sulfur in 3-year-old beech trees (Fagus sylvatic.). Physiol Plant 95:379–386CrossRefGoogle Scholar
  43. Herschbach C, Rennenberg H (1996) Storage and re-mobilisation of sulfur in beech trees (Fagus sylvatic.). Physiol Plant 98:125–132CrossRefGoogle Scholar
  44. Herschbach C, Rennenberg H (1997) Sulfur nutrition in conifers and deciduous trees. In: Rennenberg H, Eschrisch W, Ziegler H (eds) Trees: contributions to modern tree physiology. Backhuys, Leiden, pp 293–311Google Scholar
  45. Herschbach C, De Kok LJ, Rennenberg H (1995a) Net uptake of sulfate and its transport to the shoot in spinach plants fumigated with H2S or SO2: does atmospheric sulfur affect the ‘inter-organ’ regulation of sulfur nutrition. Bot Acta 108:41–46Google Scholar
  46. Herschbach C, De Kok LJ, Rennenberg H (1995b) Net uptake of sulfate and its transport to the shoot in tobacco plants fumigated with H2S or SO2. Plant Soil 175:75–84CrossRefGoogle Scholar
  47. Herschbach C, Jouanin L, Rennenberg H (1998) Overexpression of γ-glutamylcysteine synthetase, but not of glutathione synthetase elevates glutathione allocation in the phloem of transgenic poplar (Populus tremul. x Populus alb.) trees. Plant Cell Physiol 39:447–451CrossRefGoogle Scholar
  48. Herschbach C, Van der Zalm E, Schneider A, Jouanin L, De Kok L, Rennenberg H (2000) Regulation of sulfur nutrition in wild-type and transgenic poplar over-expressing γ-glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. Plant Physiol (in press)Google Scholar
  49. Hocking PJ (1980) The composition of phloem exudate and xylem sap from tree tobacco (Nicotiana glauc. Grah.). Ann Bot 45:633–643Google Scholar
  50. Jeanjean R, Broda E (1977) Dependence of sulfate uptake by Anacystis nidulan. on energy, on osmotic shock and on sulfate starvation. Arch Microbiol 114:19–23PubMedCrossRefGoogle Scholar
  51. Jensén P, König T (1982) Development of regulation mechanisms for SO4 2- influx in spring wheat roots. Physiol Plant 55:459–464CrossRefGoogle Scholar
  52. Karmoker JL, Clarkson DT, Saker LR, Rooney JM, Purves JV (1991) Sulfate deprivation depresses the transport of nitrogen to the xylem and the hydraulic conductivity of barley (Hordeum vulgar. L.) roots. Planta 185:269–278CrossRefGoogle Scholar
  53. Kreuzwieser J (1997) Sulfat- und Nitrattransport bei mykorrhizierten und nicht-mykor-rhizierten Buchen (Fagus sylvatic. L.). Dissertation. Albert-Ludwigs-Universität Freiburg i. Br, Wissenschafts-Verlag, FrankfurtGoogle Scholar
  54. Kreuzwieser J, Rennenberg H (1998) Sulfate uptake and xylem loading of mycorrhizal beech roots. New Phytol 140:319–329CrossRefGoogle Scholar
  55. Kreuzwieser J, Herschbach C, Rennenberg H (1996) Sulfate uptake and xylem loading of non-mycorrhizal excised roots of young Fagus sylvatic. trees. Plant Physiol Biochem 34:409–416Google Scholar
  56. Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO4 2- uptake in intact canola. The role of phloem-translocated glutathione. Plant Physiol 111:147–157PubMedGoogle Scholar
  57. Lappartient AG, Vidmar JJ, Leustek T, Glass ADM, Touraine B (1999) Inter-organ signalling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compounds. Plant J 18:89–95PubMedCrossRefGoogle Scholar
  58. Lass B, Ullrich-Eberius CI (1984) Evidence for proton/sulfate cotransport and its kinetics in Lemna gibb. Gl. Planta 161:53–60CrossRefGoogle Scholar
  59. Lee RB (1982) Selectivity and kinetics of ion uptake by barley plants following nutrient deficiency. Ann Bot 50:429–449Google Scholar
  60. Lee S, Leustek T (1999) The affect of cadmium on sulfate assimilation enzymes in Brassica juncea. Plant Sci 141:201–207CrossRefGoogle Scholar
  61. Macnicol PK, Bergmann L (1984) A role for homoglutathione in organic sulfur transport to the developing mung bean seed. Plant Sci Lett 36:219–223CrossRefGoogle Scholar
  62. Maggioni A, Renosto F (1977) Cysteine and methionine regulation of sulfate uptake in potato tuber discs (Solanum tuberosu.). Physiol Plant 39:143–147CrossRefGoogle Scholar
  63. Matsuda Y, Colman B (1995) Characterisation of sulfate transport in the green alga Chlorella ellipsoidea. Plant Cell Physiol 36:1291–1296Google Scholar
  64. Müntz K, Christov V, Jung R, Saalbach G, Saalbach I, Waddell D, Pickardt T, Schieder O (1997) Genetic engineering of high methionine proteins in grain legumes. In: Cram WJ, De Kok LJ, Stulen I, Brunold C, Rennenberg H (eds) Sulfur metabolism in higher plants molecular, ecophysiological and nutritional aspects. Backhuys, Leiden, pp 71–86Google Scholar
  65. Pitman MG, Cram WJ (1977) Regulation of ion content in whole plants. Symp Soc Exp Biol 31:391–424PubMedGoogle Scholar
  66. Rauser WE (1995) Phytochelatins and related peptides. Plant Physiol 109:1141–1149PubMedCrossRefGoogle Scholar
  67. Raven JA (1980) Nutrient transport in microalgae. Adv Microbiol Physiol 21:47–226CrossRefGoogle Scholar
  68. Rennenberg H (1984) The fate of excess sulfur in higher plants. Annu Rev Plant Physiol 35:121–153CrossRefGoogle Scholar
  69. Rennenberg H (1995) Processes involved in glutathione metabolism. In: Wallsgrove RM (ed) Amino acids and their derivatives in higher plants: biosynthesis and metabolism. Cambridge University Press, Cambridge, pp 155–171CrossRefGoogle Scholar
  70. Rennenberg H (1999) The significance of ectomycorrhizal fungi for sulfur nutrition of trees. Plant Soil 215:115–122CrossRefGoogle Scholar
  71. Rennenberg H, Herschbach C (1996) Responses of plants to atmospheric sulfur. In: Iqbal M, Yunus M (eds) Plant responses to air pollution. Wiley, New York, pp 285–293Google Scholar
  72. Rennenberg H, Lamoureux GL (1990) Physiological processes that modulate the concentration of glutathione in plant cells. In: Rennenberg H, Brunold C, De Kok LJ, Stulen I (eds) Sulfur nutrition and sulfur assimilation in higher plants. SPB Academic Publishing, The Hague, pp 53–65Google Scholar
  73. Rennenberg H, Schmitz K, Bergmann L (1979) Long-distance transport of sulfur in Nico-tiana tabacum. Planta 147:57–62CrossRefGoogle Scholar
  74. Rennenberg H, Polie A, Martini N, Thoene B (1988) Interaction of sulfate and glutathione transport in cultured tobacco cells. Planta 176:68–74CrossRefGoogle Scholar
  75. Rennenberg H, Kemper O, Thoene B (1989) Recovery of sulfate transport into het-erotropic tobacco cells from inhibition by reduced glutathione. Physiol Plant 76:271–276Google Scholar
  76. Schnug E (1990) Glucosinolates — fundamental, environmental and agricultural aspects. In: Rennenberg H, Brunold C, De Kok LJ, Stulen I (eds) Sulfur nutrition and sulfur assimilation in higher plants, fundamental environmental and agricultural aspects. SPB Academic Publishing, The Hague, pp 97–106Google Scholar
  77. Schulte M, Herschbach C, Rennenberg H (1998) Interactive effects of CO2, mycorrhization and drought stress on long-distance transport of reduced-sulfur in young pedunculate oak trees. Plant Cell Environ 21:917–926CrossRefGoogle Scholar
  78. Seegmüller S, Schulte M, Herschbach C, Rennenberg H (1996) Interactive effects of mycorrhization and elevated atmospheric CO2 on sulfur nutrition of young pedunculate oak (Quercus robu. L.) trees. Plant Cell Environ 19:418–426CrossRefGoogle Scholar
  79. Smith FW, Ealing PM, Hawkesford MJ, Clarkson DT (1995) Plant members of a family of sulfate transports reveal functional subtypes. Proc Natl Acad Sci USA 92:9373–9377PubMedCrossRefGoogle Scholar
  80. Smith FW, Hawkesford MJ, Ealing PM, Clarkson DT, Van den Berg PJ, Belcher AR, Warrilow AGS (1997) Regulation of expression of a cDNA from barley roots encoding a high affinity sulfate transporter. Plant J 12:875–884PubMedCrossRefGoogle Scholar
  81. Smith IK (1980) Regulation of sulfate assimilation in tobacco cells. Effect of nitrogen and sulfur nutrition on sulfate permease and O-acetylserine sulfhydrylase. Plant Physiol 66:877–883PubMedCrossRefGoogle Scholar
  82. Strohm M, Jouanin L, Kunert KJ, Pruvost C, Polle A, Foyer HC, Rennenberg H (1995) Regulation of glutathione synthesis in leaves of transgenic poplar (Populus tremul. × P. alb.) overexpressing glutathione synthetase. Plant J 7:141–145CrossRefGoogle Scholar
  83. Tabe L, Molvig L, Khan R, Schroeder H, Gollasch S, Wardley-Richardson T, Moore A, Craig S, Spencer D, Eggum B, Higgins TJV (1997) Modifying the sulfur amino acid content of protein in transgenic legumes. In: Cram WJ, De Kok LJ, Stulen I, Brunold C, Rennenberg H (eds) Sulfur metabolism in higher plants molecular, ecophysiological and nutritional aspects. Backhuys, Leiden, pp 87–93Google Scholar
  84. Takahashi H, Sasakura N, Noji M, Saito K (1996) Isolation and characterisation of a cDNA encoding a sulfate transporter. FEBS Lett 392:95–99PubMedCrossRefGoogle Scholar
  85. Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, De Almeida-Engler J, Engler G, Van Montagu M, Saito K (1997) Regulation of cysteine biosynthesis in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:11102–11107PubMedCrossRefGoogle Scholar
  86. Yildiz FH, Davies JP, Grossman AR (1994) Characterization of sulfate transport in Chlamydomonas reinhardti. during sulfur-limited and sulfur-sufficient growth. Plant Physiol 104:981–987PubMedGoogle Scholar
  87. Yildiz FH, Davies JP, Grossman A (1996) Sulfur availability and the SAC. gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii. Plant Physiol 112:669–675PubMedCrossRefGoogle Scholar
  88. Ziegler H (1975) Nature of transported substances. In: Zimmermann MH, Milburn JA (eds) Encyclopedia of plant physiology, vol 1. Springer, Berlin Heidelberg New York, pp 59–100Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2001

Authors and Affiliations

  • Cornelia Herschbach
    • 1
  • Heinz Rennenberg
    • 1
  1. 1.Institut für Forstbotanik und BaumphysiologieAlbert-Ludwigs-Universität FreiburgFreiburgGermany

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