Stable isotopes of Cu and Zn in higher plants: Evidence for Cu reduction at the root surface and two conceptual models for isotopic fractionation processes

Environmental Science and Technology

Volumn 46, Issue 5, 2012, Pages 2652-2660

  Jouvin, D ^a,e,g   Weiss, D J ^b   Mason, T F M ^b   Bravin, M N ^c,d   Louvat, P ^e   Zhao, F ^f   Ferec, F ^a   Hinsinger, P ^c   Benedetti, M F ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^c UMR ECO SOLS   (France)

^d Dept Performance of Tropical Production and Processing Systems   (France)

^e INSTITUT DE PHYSIQUE DU GLOBE DE PARIS   (France)

^f ROTHAMSTED RESEARCH   (United Kingdom)

^g UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOGEOCHEMICAL CYCLING; CONCEPTUAL MODEL; CONTROLLED CONDITIONS; DURUM WHEATS; FRACTIONATION PATTERNS; HIGHER PLANTS; ISOTOPE FRACTIONATION; ISOTOPIC FRACTIONATIONS; METAL SPECIATION; NUTRIENT SOLUTION; PLANT SPECIES; PLANT UPTAKE; PRELIMINARY MODEL; ROOT CELLS; ROOT SURFACES; STABLE ISOTOPES; STABLE METALS;

CELL MEMBRANES; ISOTOPES; NUTRIENTS; TRACE ELEMENTS; ZINC;

COPPER;

COPPER; IRON; TRACE ELEMENT; ZINC;

BIOACCUMULATION; BIOGEOCHEMICAL CYCLE; BIOLOGICAL UPTAKE; COPPER; CROP PLANT; ISOTOPIC FRACTIONATION; NUMERICAL MODEL; REDUCTION; ROOT SYSTEM; SPECIATION (CHEMISTRY); STABLE ISOTOPE; ZINC;

ARTICLE; CELL MEMBRANE; FRACTIONATION; LETTUCE; NONHUMAN; PLANT ROOT; RICE; TOMATO; TRITICUM DURUM; VASCULAR PLANT;

ADSORPTION; BIODEGRADATION, ENVIRONMENTAL; BIOLOGICAL TRANSPORT; BIOMASS; CELL MEMBRANE; CHEMICAL FRACTIONATION; COPPER; DIFFUSION; IONS; IRON; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PLANT ROOTS; PLANT SHOOTS; PLANTS; SOLUTIONS; SURFACE PROPERTIES; ZINC; ZINC ISOTOPES;

EMBRYOPHYTA; LACTUCA; LYCOPERSICON ESCULENTUM; TRITICUM TURGIDUM SUBSP. DURUM;

EID: 84857855314     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es202587m     Document Type: Article

References (58)

1. Navarrete, J. U.; Borrok, D. M.; Viveros, M.; Ellzey, J. T. Copper isotope fractionation during surface adsorption and intracellular incorporation by bacteria Geochim. Cosmochim. Acta 2011, 75, 784-799
2. von Blanckenburg, F.; von wirén, N.; Guelke, M.; Weiss, D. J.; Bullen, T. D. Fractionation of metal stable isotopes by higher plants Elements 2009, 5, 375-380
3. Peel, K.; Weiss, D. J.; Sigg, L. Zinc isotope composition of settling particles as a proxy for biogeochemical processes in lakes: Insights from the eutrophic Lake Greifen, Switzerland Limnol. Oceanogr. 2009, 54, 1699-1708
4. Goia, S.; Weiss, D. J.; Coles, B.; Arnold, T.; Babinski, M. Accurate and precise measurements of Zn isotopes in aerosols Anal. Chem. 2008, 80, 9776-9780
5. Grotz, N.; Guerinot, M. L. Molecular aspects of Cu, Fe, and Zn homeostasis in plants Biochim. Biophys. Acta 2006, 1763, 595-608
6. Clemens, S. Molecular mechanisms of plant metal tolerance and homeostasis Planta 2001, 212, 475-486
7. Michaud, A. M.; Chappellaz, C.; Hinsinger, P. Copper phytotoxicity affects root elongation and iron nutrition in durum wheat (Triticum turgidum durum L.) Plant Soil 2008, 310, 151-165
8. Johnson, C. M.; Skulan, J. L.; Beard, B. L.; Sun, H.; Nealson, K. H.; Braterman, P. S. Isotopic fractionation between Fe(III) and Fe(II) in aqueous solutions Earth Planet. Sc. Lett. 2002, 195, 141-153
9. Michaud, A. M.; Bravin, M. N.; Galleguillos, M.; Hinsinger, P. Copper uptake and phytotoxicity as assessed in situ for durum wheat (Triticum turgidum durum L.) cultivated in Cu-contaminated, former vineyard soils Plant Soil 2007, 298, 99-111
10. Guelke, M.; Von Blanckenburg, F. Fractionation of stable iron isotopes in higher plants Environ. Sci. Technol. 2007, 41, 1896-1901
11. Guerinot, M. L. The ZIP family of metal transporters Biochim. Biophys. Acta 2000, 1465, 190-198
12. Von Wirén, N.; Marschner, H.; Römheld, V. Roots of iron-efficient maize also absorb phytosiderophore-chelated zinc Plant Physiol. 1996, 111, 1119-1125
13. Hacisalihoglu, G.; Hart, J. J.; Kochian, L. V. High- and low-affinity zinc transport systems and their possible role in zinc efficiency in bread wheat Plant Physiol. 2001, 125, 456-463
14. Broadley, M. R.; White, P. J.; Hammond, J. P.; Zelko, I.; Lux, A. Zinc in plants New Phytol. 2007, 173, 677-702
15. Grotz, N.; Fox, T.; Connolly, E.; Park, W.; Guerinot, M. L.; Eide, D. Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 220-224
16. Arnold, T.; Kirk, G. J. D.; Wissuwa, M.; Frei, M.; Zhao, F.-J.; Mason, F. D. T.; Weiss, D. J. Evidence for the mechanisms of zinc uptake by rice using isotope fractionation Plant Cell Environ. 2010, 33, 370-381
17. Sancenon, V.; Puig, S.; Mateu-Andrés, I.; Dorcey, E.; Thiele, D. J.; Penarrubia, L. The Arabidopsis copper transporter COPT1 functions in root elongation and pollen developpement J. Biol. Chem. 2004, 279 (15) 15348-15355
18. Cakmak, I.; Sari, N.; Marschner, H.; Ekiz, H.; Kalayci, M.; Yilmaz, A.; Braun, H. J. Phytosiderophore release in bread and durum wheat genotypes differing in zinc efficiency Plant Soil 1996, 180, 183-189
19. Suzuki, M.; Takahashi, M.; Tsukamoto, T.; Watanabe, S.; Matsuhashi, S.; Yazaki, J.; Kishimoto, N.; Kikuchi, S.; Nakanishi, H.; Mori, S.; Nishizawa, N. K. Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley The Plant J. 2006, 48, 85-97
20. Zheng, S. J.; He, Y. F.; Arakawa, Y.; Masaoka, Y.; Tang, C. A copper-deficiency-induced root reductase is different from the iron-deficiency-induced one in red clover (Trifolium pratense L.) Plant Soil 2005, 273, 69-76
21. Puig, S.; Andrès-Colas, N.; Garcia-Molina, A.; Penarrubia, L. Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications Plant Cell Environ. 2007, 30, 271-290
22. Wintz, H.; Fox, T.; Wu, Y.-Y.; Feng, V.; Chen, W.; Chang, H.-S.; Zhu, T.; Vulpe, C. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis J. Biol. Chem. 2003, 278, 47644-47653
23. Chaignon, V.; Di Malta, D.; Hinsinger, P. Fe-deficiency increases Cu acquisition by wheat cropped in a Cu-contaminated vineyard soil New Phytol. 2002, 154, 121-130
24. Roberts, L. A.; Pierson, A. J.; Panaviene, Z.; Walker, E. L. Yellow Stripe 1. Expanded roles for the maize iron-phytosiderophore transporter Plant Physiol. 2004, 135, 112-120
25. Schaaf, G.; Ludewig, U.; Erenoglu, B.; Mori, S.; Kitahara, T.; Von Wirén, N. ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals J. Biol. Chem. 2004, 279, 9091-9096
26. Weiss, D. J.; Mason, T. F. D.; Zhao, F. J.; Kirk, G. J. D.; Coles, B. J.; Horstwood, M. S. A. Isotopic discrimination of zinc in higher plants New Phytol. 2005, 165, 703-710
27. Black, J. R.; Yin, Q.-Z.; Casey, W. H. An experimental study of magnesium-isotope fractionation in chlorophyll-a photosynthesis Geochim. Cosmochim. Acta 2006, 70, 4072-4079
28. Black, J. R.; Epstein, E.; Rains, W. D.; Yin, Q.-Z.; Casey, W. H. Magnesium-isotope fractionation during plant growth Environ. Sci. Technol. 2008, 42, 7831-7836
29. Pokrovsky, O. S.; Viers, J.; Emnova, E. E.; Kompantseva, E. I.; Freydier, R. Copper isotope fractionation during its interaction with soil and aquatic microorganisms and metal oxy(hydr)oxides: Possible structural control Geochim. Cosmochim. Acta 2008, 72, 1742-1757
30. Kimball, B. E.; Mathur, R.; Dohnalkova, A. C.; Wall, A. J.; Runkel, R. L.; Brantley, S. L. Copper isotope fractionation in acid mine drainage Geochim. Cosmochim. Acta 2009, 73 (5) 1247-1263
31. Mathur, R.; Ruiz, J.; Titley, S.; Liermann, L.; Buss, H.; Brantley, S. Cu isotopic fractionation in the supergene environnement with and without bacteria Geochim. Cosmochim. Acta 2005, 69, 5233-5246
32. Weinstein, C.; Moynier, F.; Wang, K.; Paniello, R.; Foriel, J.; Catalano, J.; Pichat, S. Isotopic fractionation of Cu in plants Chem. Geol. 2011, 286, 266-271
33. Jouvin, D.; Louvat, P.; Maréchal, C. N.; Juillot, F.; Benedetti, M. F. Zn isotopic fractionation: why organic matters Environ. Sci. Technol. 2009, 43, 5747-5754
34. Ehrlich, S.; Butler, I.; Halicz, L.; Rickard, D.; Oldroyd, A.; Matthews, A. Experimental study of the copper isotope fractionation between aqueous Cu(II) and covellite, CuS Chem. Geol. 2004, 209, 259-269
35. Burkhead, J. L.; Gogolin, K. A.; Abdel-Ghany, S.; Cohu, C. M.; Pilon, M. Copper homeostasis New Phytol. 2009, 182, 799-816
36. Mukherjee, I.; Campbell, N. H.; Ash, J. S.; Connolly, E. L. Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper Planta 2006, 223, 1178-1190
37. Moynier, F.; Pichat, S.; Pons, M.-L.; Fike, D.; Balter, V.; Albarède, F. Isotopic fractionation and transport mechanisms of Zn in plants Chem. Geol. 2009, 267, 125-130
38. Mason, T. F. D.; Weiss, D.; Horstwood, M.; Parrish, R. R.; Russell, S. S.; Mullane, E.; Coles, B. J. High-precision Cu and Zn isotope analysis by plasma source mass spectrometry. Part 2. Correcting for mass discrimination effects J. Anal. Atom. Spectrom. 2004, 19, 218-226
39. Mason, T. F. D.; Weiss, D. J.; Horstwood, M.; Parrish, R. R.; Russell, S. S.; Mullane, E.; Coles, B. J. High-precision Cu and Zn isotope analysis by plasma source mass spectrometry. Part 1. Spectral interferences and their correction J. Anal. Atom. Spectrom. 2004, 19, 209-217
40. Urey, H. C. The thermodynamics properties of isotopic substances J. Chem. Soc. 1947, 562-581
41. Schauble, E. A. Applying stable isotope fractionation theory to new systems. In Geochemistry of Non-traditional Stable Isotopes; Johnson, C. M.; Beard, B. L.; Albarède, F., Eds.; Reviews in Mineralogy and Geochemistry; Mineralogical Society of America: Washington, DC, 2004; Vol. 55, pp 65-111.
42. Field, T. B.; McBryde, W. A.E. Apparent stability constants of proton and metal ion complexes of glycine, iminodiacetic acid, nitrilotriacetic acid, and triethylenetetramine in aqueous methanol Can. J. Chem. 1981, 59, 555-558
43. Smith, R. M.; Martell, A. E., Critical Stability Constants; Plenum Press: 1989.
44. Cornu, J.-Y.; Staunton, S.; Hinsinger, P. Copper concentration in plants and in the rhizosphere as influenced by the iron status of tomato (Lycopersicon esculentum L.) Plant Soil 2007, 292, 63-77
45. Straczek, A.; Sarret, G.; Manceau, A.; Hinsinger, P.; Geoffroy, N.; Jaillard, B. Zinc distribution and speciation in roots of various genotypes of tobacco exposed to Zn Environ. Exp. Bot. 2008, 63, 80-90
46. Juillot, F.; Maréchal, C.; Ponthieu, M.; Cacaly, S.; Morin, G.; Benedetti, M.; Hazemann, J. L.; Proux, O.; Guyot, F. Zn isotopic fractionation caused by sorption on goethite and 2-Lines ferrihydrite Geochim. Cosmochim. Acta 2008, 72, 4886-4900
47. Pokrovsky, O. S.; Viers, J.; Freydier, R. Zinc stable isotope fractionation during its adsorption on oxides and hydroxides J. Colloid Interface Sci. 2005, 291, 192-200
48. Wang, P.; Zhou, D. M.; Luo, X. S.; Li, L. Z. Effects of Zn-complexes on zinc uptake by wheat (Triticum aestivum) roots: A comprehensive consideration of physical, chemical and biological processes on biouptake Plant Soil 2009, 316, 177-192
49. John, S. G.; Geis, R. W.; Saito, M. A.; Boyle, E. A. Zinc isotope fractionation during high-affinity and low-affinity zinc transport by the marine diatom Thalassiosira oceanica Limnol. Oceanogr. 2007, 52, 2710-2714
50. Sancenon, V.; Puig, S.; Mira, H.; Thiele, D. J.; Penarrubia, L. Identification of a copper transporter family in Arabidopsis thaliana Plant Mol. Biol. 2003, 51, 577-587
51. Fernandez, A.; Borrok, D. M. Fractionation of Cu, Fe, and Zn isotopes during the oxidative weathering of sulfide-rich rocks Chem. Geol. 2009, 264, 1-12
52. Clark, C. J.; Holland, P. T.; Smith, G. S. Chemical composition of bleeding xylem sap from kiwifruit vines Ann. Bot-London 1986, 58, 353-362
53. Schmidke, I.; Stephan, U. W. Transport of metal micronutrients in the phloem of castor bean (Ricinus communis) seedlings Physiol. Plantarum 1995, 95, 147-153
54. Von Wirén, N.; Klair, S.; Bansal, S.; Briat, J.-F.; Khodr, H.; Shiori, T.; Leigh, R. A.; Hider, R. C. Nicotianamine chelates both Fe(III) and Fe(II). Implications for metal transport in plants Plant Physiol. 1999, 119, 1107-1114
55. Maréchal, C. N.; Albarède, F. Ion-exchange fractionation of copper and zinc isotopes Geochim. Cosmochim. Acta 2002, 66 (9) 1499-1509
56. Rodushkin, I.; Stenberg, A.; Andrén, H.; Malinovsky, D.; Baxter, D. C. Isotopic fractionation during diffusion of transition metal ions in solution Anal. Chem. 2004, 76, 2148-2151
57. Yruela, I. Copper in plants: Acquisition, transport and interactions Funct. Plant Biol. 2009, 36, 409-430
58. Bigalke, M.; Weyer, S.; Wilcke, W. Copper isotope fractionation during complexation with insolubilized humic acid Environ. Sci. Technol. 2010, 44, 5496-5502