32S/34S isotope fractionation in plant sulphur metabolism

New Phytologist

Volumn 200, Issue 1, 2013, Pages 44-53

  Tcherkez, Guillaume ^a,b   Tea, Illa ^c  

^a INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^b INSTITUT UNIVERSITAIRE DE FRANCE   (France)

^c UNIVERSITÉ DE NANTES   (France)

Author keywords

34S abundance; Fractionation; Isotope effect; S metabolism; Sulfur; Sulphate; Sulphur

Indexed keywords

EID: 84878004270     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12314     Document Type: Review

References (71)

1. n aqueous solution. Inorganic Chemistry 45: 1427–1429.
2. Amrani A, Ma Q, Ahmad WS, Aizenshtat Z, Tang Y. 2008. Sulfur isotope fractionation during incorporation of sulfur nucleophiles into organic compounds. Chemical Communications 2008: 1356–1358.
3. 34S analysis of volatile organics by coupled GC/Multicollector-ICPMS. Analytical Chemistry 81: 9027–9034.
4. 34S of dimethyl sulphide in the surface ocean. Proceedings of the Goldschmidt Conference 2012, Montreal, Canada.
5. Aneja VP. 1990. Natural sulfur emissions into the atmosphere. Journal of the Air & Waste Management Association 40: 469–476.
6. Aneja VP, Overton JH, Cupitt LT, Durham JL, Wilson WE. 1979. Carbon disulphide and carbonyl sulphide from biogenic sources and their contributions to the global sulphur cycle. Nature 282: 493–496.
7. Baliga BT, Bourns AN. 1966. Kinetic sulfur isotope effects in aromatic bromodesulfonation. Canadian Journal of Chemistry 44: 363–378.
8. Bell CI, Clarkson DT, Cram WJ. 1995. Partitioning and redistribution of sulphur during S-stress in Macroptilium atropurpureum cv. Siratro. Journal of Experimental Botany 46: 73–81.
9. Benkovic SJ, Hevey RC. 1970. Studies in sulfate esters. V. The mechanism of hydrolysis of phenyl phosphosulfate, a model system for 3’ -phosphoadenosine 5’-phosphosulfate. Journal of the American Chemical Society 92: 4971–4977.
10. Bourgis F, Roje S, Nuccio ML, Fisher DB, Tarczynski MC, Li C, Herschbach C, Rennerberg H, Pimenta MJ, Shen TL et al. 1999. S-methylmethionine plays a major role in phloem sulfur transport and is synthesised by a novel type of methyltransferase. Plant Cell 11: 1485–1497.
11. Brody MS, Hille R. 1999. The kinetic behaviour of chicken liver sulphite oxidase. Biochemistry 38: 6668–6677.
12. Brunner B, Bernasconi SM, Kleikemper J, Schroth MH.2005. A model for oxygen and sulphur isotope fractionation in sulphate during bacterial sulphate reduction processes. Geochimica et Cosmochimica Acta 69: 4773–4785.
13. 34S isotope effect on sulphate ester hydrolysis: mechanistic implications. Journal of the American Chemical Society 125: 13036–13037.
14. Cleland WW, Hengge AC. 2006. Enzymatic mechanisms of phosphate and sulphate transfer. Chemical Reviews 106: 3252–3278.
15. Cooper HD, Clarkson DT. 1989. Cycling of amino-nitrogen and other nutrients betweenshootsandrootsincereals–apossiblemechanismintegratingshootandroot in the regulation of nutrient uptake. Journal of Experimental Botany 40: 753–762.
16. Cram WJ. 1983. Characteristics of sulphate transport across plasmalemma and tonoplast of carrot root cells. Plant Physiology 72: 204–211.
17. Crane BR, Siegel LM, Getzoff ED. 1995. Sulfite reductase structure at 1.6 Å: evolution and catalysis for reduction of inorganic anions. Science 270: 59–67.
18. Crane BR, Siegel LM, Getzoff ED. 1997. Probing the catalytic mechanism of sulphite reductase by X-ray crystallography: structures of the Escherichia coli hemoprotein in complex with substrates, inhibitors, intermediates and products. Biochemistry 36: 12120–12137.
19. Cumming M, Leung S, McCallum J, McManus MT. 2007. Complex formation between recombinant ATP sulfurylase and APS reductase of Allium cepa (L.). FEBS Letters 581: 4139–4147.
20. Detmers J, Brüchert V, Habicht KS, Kuever J. 2001. Diversity of sulfur isotope fractionations by sulfate-reducing prokaryotes. Applied and Environmental Microbiology 67: 888–894.
21. Dörmann P, Hölzl G. 2009. The role of glycolipids in photosynthesis. In: Wada H, Murata N, eds. Lipids in photosynthesis: essential and regulatory functions. Advances in Photosynthesis and Respiration 30: 265–282.
22. 2 on stable isotope fractionation during bacterial sulphate reduction. Environmental Science and Technology 43: 82–87.
23. 2. Acta Chemica Scandinavica 26: 581–584.
24. Fismes J, Vong PC, Guckert A. 1999. Use of labelled sulphur-35 for tracing sulphur transfers in developing pods of field-grown oilseed rape. Communications in Soil Science and Plant Analysis 30: 221–234.
25. Frentzen M. 2004. Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Current Opinion in Plant Biology 7: 270–276.
26. Friedberger MP, Thornton ER. 1976. Solvolysis mechanisms: sulfur kinetic isotope effects in the hydrolysis of substituted benzyldimethylsulfoniumtosylates. Journal of the American Chemical Society 98: 2861–2865.
27. Gebauer G, Giesemann A, Schultze ED, Jäger HJ. 1994. Isotope ratios and concentrations of sulfur and nitrogen in needles and soils of Picea abies stands as influenced by atmospheric deposition of sulfur and nitrogen compounds. Plant and Soil 164: 267–281.
28. Graham DE, Xu H, White RH. 2002. Identification of coenzyme M biosynthetic phosphosulfolactate synthase. Journal of Biological Chemistry 277: 13421–13429.
29. Grassineau NV, Mattey DP, Lowry D. 1998. Measurement of sulphur isotopic compositions of sulphide minerals using new continuous He-flow EA-MS technology. Mineralogical Magazine 62: 537–538.
30. Habicht KS, Canfield DE, Rethmeier J. 1998. Sulfur isotope fractionation during bacterial reduction and disproportionation of thiosulfate and sulfite. Geochimica et Cosmochimica Acta 62: 2585–2595.
31. Hanson AD, Roje S. 2001. One-carbon metabolism in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 52: 119–137.
32. Hargreaves RT, Katz AM, Saunders WH. 1976. Sulfur isotope effects in substitution reactions of trimethylsulfonium ion. Journal of the American Chemical Society 98: 2614–2617.
33. 3(P). Journal of Physical Chemistry A 116: 3521–3526.
34. Hawkesford MJ, De Kok LJ. 2006. Managing sulphur metabolism in plants. Plant, Cell & Environment 29: 382–395.
35. Hemann C, Hood BL, Fulton M, Hänsch R, Schwarz G, Mendel RR, Kirk ML, Hille R. 2005. Spectroscopic and kinetic studies of Arabidopsis thaliana sulphite oxidase: nature of the redox-active orbital and electronic structure contributions to catalysis. Journal of the American Chemical Society 127: 16567–16577.
36. 33S nuclear magnetic resonance spectroscopy of biological samples obtained with a laboratory model 33S cryogenic probe. Review of Scientific Instruments 81: 54302–54309.
37. Hoefgen R, Hesse H. 2008. Sulfur and cysteine metabolism. In: Jez J, ed. Sulfur: a missing link between soils, crops, and nutrition. Agronomy Monographs. Madison, USA, 50: 83–104.
38. Ivanov MV. 1981. The biogeochemical sulphur cycle. In: Likens G, ed. Some perspectives of the major biogeochemical cycles. SCOPE, New York, USA, 61–78.
39. Kaplan IR, Rittenberg SC. 1964. Microbiological fractionation of sulphur isotopes. Journal of General Microbiology 34: 195–212.
40. Kepplinger-Sparace KF, Mudd JB. 1989. Biosynthesis of sulfoquinovosyldiacylglycerol in higher plants. Plant Physiology 93: 256–263.
41. 3– by plants. Plant Physiology 66: 51–56.
42. 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 Journal 20: 37–44.
43. Kwart H, Stanulonis J. 1976. Assessment of the thioallylic rearrangement by a simplified technique for high-precision measurement of isotope effects. Journal of the American Chemical Society 98: 4009–4010.
44. Larsson CM, Larsson M, Purves JV, Clarkson DT. 2006. Translocation and cycling through roots of recently absorbed nitrogen and sulfur in wheat (Triticum aestivum) during vegetative and generative growth. Physiologia Plantarum 82: 345–352.
45. Loudet O, Saliba-Colombani V, Camilleri C, Calenge F, Gaudon V, Koprivova A, North KA, Kopriva S, Daniel-Vedele F. 2007. Natural variation for sulphate content in Arabidopsis thaliana is highly controlled by APR2. Nature Genetics 39: 896–900.
46. 3 by Pearl Millet. Plant Physiology 69: 880–884.
47. Markham GD, Parkin DW, Mentch F, Schramm VL. 1987.Akinetic isotope effect study and transition state analysis of the S-adenosylmethionine synthetase reaction. Journal of Biological Chemistry 262: 5609–5615.
48. Monaghan JM, Scrimgeour CM, Stein WM, Zhao FJ, Evans EJ. 1999. Sulphur accumulation and redistribution in wheat (Triticum aestivum): a study using stable sulphur isotope ratios as a tracer. Plant, Cell & Environment 22: 831–839.
49. Mudd SH, Datko AH. 1990. The S-methylmethionine cycle in Lemna paucicostata. Plant Physiology 93: 623–630.
50. Nakayama M, Akashi T, Hase T. 2000. Plant sulphite reductase: molecular structure, catalytic function and interaction with ferredoxin. Journal of Inorganic Biochemistry 82: 27–32.
51. Paris G, Sessions AL, Subhas AV, Adkins JF. 2013. MC-ICP-MS measurement of d34SandD33Sinsmallamountsofdissolvedsulphate.ChemicalGeology 345:50–61.
52. Richards MP, Fuller BT, Hedges REM. 2001. Sulphur isotopic variation in ancient bone collagen from Europe: implications for human palaeodiet, residence mobility and modern pollutant studies. Earth and Planetary Science Letters 191: 185–190.
53. Richards MP, Fuller BT, Sponheimer M, Robinson T, Ayliffe L. 2003. Sulphur isotopes in palaeodietary studies: a review and results from a controlled feeding experiment. International Journal of Osteoarchaeology 13: 37–45.
54. Rodgers J, Femec DA, Schowen RL. 1982. Isotopic mapping of transition state structural features associated with enzymatic catalysis of methyl transfer. Journal of the American Chemical Society 104: 3263–3268.
55. Saunders WH, Asperger S. 1957. Mechanisms of elimination reactions. Sulfur isotope effects in the decomposition of some sulfonium salts. Journal of the American Chemical Society 79: 1612–1615.
56. 2S release from plants. In: Schnug E, De Kok LJ, eds. Proceedings of the 1st Sino-German workshop on aspects of sulfur nutrition of plants. Braunschweig, Germany: Federal Agricultural Research Centre Braunschweig, 121–129.
57. Sekulic N, Dietrich K, Paarmann I, Ort S, Konrad M, Lavie A. 2007. Elucidation of the active conformation of the APS-kinase domain of human PAPS synthetase 1. Journal of Molecular Biology 367: 488–500.
58. Sim MS, Bosak T, Ono S. 2011. Large sulfur isotope fractionation does not require disproportionation. Science 333: 74–77.
59. 2 during leaf gas exchange. New Phytologist 186: 869–878.
60. 35S-methionine incorporates differentially into polypeptides across leaves of spinach (Spinacia oleracea). Plant and Cell Physiology 37: 996–1006.
61. Sun M, Leyh TS. 2006. Channelling in sulphate activating complexes. Biochemistry 45: 11304–11311.
62. 34S-value measurements in food origin assignments and sulfur isotope fractionations in plants and animals. Journal of Agriculture and Food Chemistry 58: 3139–3146.
63. 3 leaves. Journal of Experimental Botany 59: 1685–1693.
64. 13C fractionations in plant primary metabolism. Trends in Plant Science 16: 499–506.
65. Tcherkez G, Ribas-Carbo M. 2012 Interactions between photosynthesis and day respiration. In: Flexas J, Loreto F, Medrano H, eds. Terrestrial photosynthesis in a changing environment. Cambridge, UK: Cambridge University Press, 41–53.
66. Tea I. 2004. Contribution à l’amé lioration de la qualité technologique des farines de blé (Triticum aestivum L.) par l’apport foliaire d’azote et de soufre: implication des protéïnes de réserve et du glutathion. PhD thesis, Institut National Polytechnique de Toulouse, France.
67. Tea I, Genter T, Naulet N, Lummerzheim M, Kleiber D. 2007. Interaction between nitrogen and sulfur by foliar application and its effects on flour bread-making quality. Journal of the Science of Food and Agriculture 87: 2853–2859.
68. Tea I, Genter T, Naulet N, Morvan E, Kleiber D. 2003. Isotopic study of postanthesis foliar incorporation of sulphur and nitrogen in wheat. Isotopes in Environmental and Health Studies 39: 289–300.
69. Thode HG. 1991. Sulphur isotopes in nature and the environment: an overview. In: Krouse HR, Grinenko VA, eds. Stable isotopes in the assessment of natural and anthropogenic sulphur in the environment. Chichester, UK: Wiley and Sons Ltd, 1–26.
70. Trust BA, Fry B. 1992. Stable sulphur isotopes in plants: a review. Plant, Cell & Environment 15: 1105–1110.
71. Wadleigh MA. 2003. Lichens and atmospheric sulphur: what stable isotopes reveal. Environmental Pollution 126: 345–351.