Skip to main content
Log in

Iron and zinc complexation in wild-type and ferritin-expressing wheat grain: implications for mineral transport into developing grain

  • Original Paper
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

We have used synchrotron-based X-ray fluorescence and absorption techniques to establish both metal distribution and complexation in mature wheat grains. In planta, extended X-ray absorption fine structure (EXAFS) spectroscopy reveals iron phytate and zinc phytate structures in aleurone cells and in modified aleurone cells in the transfer region of the grain: iron is coordinated octahedrally by six oxygen atoms and fewer than two phosphorous atoms. Zinc is coordinated tetrahedrally by four oxygen atoms and approximately 1.5 phosphorus atoms in an asymmetric coordination shell. We also present evidence of modified complexation of both metals in transgenic grain overexpressing wheat ferritin. For zinc, there is a consistent doubling of the number of complexing phosphorus atoms. Although there is some EXAFS evidence for iron phytate in ferritin-expressing grain, there is also evidence of a structure lacking phosphorus. This change may lead to an excess of phosphorus within the storage regions of grain, and in turn to the demonstrated increased association of phosphorus with zinc in ferritin-expressing grains. Derivative X-ray absorption spectra also suggest that mineral complexation in the transfer region of ferritin-expressing grains is quite different from that in wild-type grain. This may explain why the raised levels of minerals transported to the developing grain accumulate within the crease region of the transgenic grain.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  1. Manton MJ (2010) Curr Opin Environ Sustain 2:151–155

    Article  Google Scholar 

  2. Newton AC, Johnson SN, Gregory PJ (2011) Euphytica 179:3–18

    Article  Google Scholar 

  3. Jaggard KW, Qi AM, Ober ES (2010) Philos Trans R Soc B 365:2835–2851

    Article  Google Scholar 

  4. Brinch-Pedersen H, Borg S, Tauris B, Holm PB (2007) J Cereal Sci 46:308–326

    Article  CAS  Google Scholar 

  5. Xu YF, An DG, Li HJ, Xu HX (2011) Can J Plant Sci 91:231–237

    Article  CAS  Google Scholar 

  6. World Health Organization (2002) World health report 2002. World Health Organization, Geneva

    Google Scholar 

  7. Monasterio I, Graham RD (2000) Food Nutr Bull 21:392–396

    Google Scholar 

  8. Zhao FJ, Su YH, Dunham SJ, Rakszegi M, Bedo Z, McGrath SP, Shewry PR (2009) J Cereal Sci 49:290–295

    Article  CAS  Google Scholar 

  9. Black R, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Rivera J (2008) Lancet 371:243–260

    Article  PubMed  Google Scholar 

  10. Borg S, Brinch-Pedersen H, Tauris B, Holm PB (2009) Plant Soil 325:15–24

    Article  CAS  Google Scholar 

  11. Regvar M, Eichert D, Kaulich B, Gianoncelli A, Pongrac P, Vogel-Mikus K, Kreft I (2011) J Exp Bot 62:3929–3939

    Article  PubMed  CAS  Google Scholar 

  12. O’Dell BL, DeBoland AR, Koirtyohann SR (1972) J Agric Food Chem 20:178–185

    Google Scholar 

  13. Heard PJ, Feeney KA, Allen GC, Shewry PR (2001) Plant J 30:237–245

    Article  Google Scholar 

  14. Ockenden I, Dorsch JA, Reid MM, Lin L, Grant LK, Raboy V, Lott JNA (2004) Plant Sci 167:1131–1142

    Article  CAS  Google Scholar 

  15. Mazzolini AP, Pallaghy CK, Legge GJF (1985) New Phytol 100:483–509

    Article  CAS  Google Scholar 

  16. Cramer SP, Hodgson KO (1979) Prog Inorg Chem 25:1–39

    Article  CAS  Google Scholar 

  17. Scott RA (1985) Methods Enzymol 117:414–459

    Article  CAS  Google Scholar 

  18. Borg S, Brinch-Pedersen H, Tauris B, Madsen LH, Darbani B, Noeparvar S, Holm PB (2012) J Cereal Sci 56:204–213

    Article  CAS  Google Scholar 

  19. Lamacchia C, Shewry PR, Di Fonzo N, Forsyth J, Harris N, Lazzeri PA, Napier JA, Halford NG, Barcelo P (2001) J Exp Bot 55:243–250

    Article  Google Scholar 

  20. Brinch-Pedersen H, Olesen A, Rasmussen SK, Holm PB (2000) Mol Breed 6:195–206

    Article  CAS  Google Scholar 

  21. Dionisio G, Madsen CK, Holm PB, Welinder KG, Jørgensen M, Stoger E, Arcalis E, Brinch-Pedersen H (2011) Plant Physiol 156:1087–1100

    Article  PubMed  CAS  Google Scholar 

  22. Solé VA, Papillon E, Cotte M, Walter P, Susini J (2007) Spectrochim Acta Part B 62:63–68

    Article  Google Scholar 

  23. Girardeau T, Mimault J, Jaouen M, Chartier P, Tourillon G (1992) Phys Rev B 46:7144–7152

    Article  Google Scholar 

  24. Ravel B, Newville M (2005) J Synchrotron Radiat 12:537–540

    Article  CAS  Google Scholar 

  25. Tenderholt A, Hedman B, Hodgson KO (2006) AIP Conf Proc 882:105–107

    Google Scholar 

  26. Tomić S, Searle BG, Wander A, Harrison NM, Dent AJ, Mosselmans JFW, Inglesfield JE (2005) New tools for the analysis of EXAFS: the DL EXCURVE package. CCLRC technical report DL-TR-2005-001

  27. Lombi E, Smith E, Hansen TH, Paterson D, de Jonge MD, Howard DL, Persson DP, Husted S, Ryan C, Schjoerring JK (2011) J Exp Bot 62:273–282

    Article  PubMed  CAS  Google Scholar 

  28. Wang YX, Specht A, Horst WJ (2011) New Phytol 189:428–437

    Article  PubMed  CAS  Google Scholar 

  29. Persson DP, Hansen TH, Laursen KH, Schjoerring JK, Husted S (2009) Metallomics 1:418–426

    Article  PubMed  CAS  Google Scholar 

  30. Hasnain SS, Wardell EM, Garner CD, Schlösser M, Beyersmann D (1985) Biochem J 230:625–633

    PubMed  CAS  Google Scholar 

  31. Zdanowski K, Doughty P, Jakimowicz P, O’Hara L, Buttner MJ, Paget MSB, Kleanthous C (2006) Biochemistry 45:8294–8300

    Article  PubMed  CAS  Google Scholar 

  32. Sarret G, Manceau A, Spadini L, Roux J-C, Hazeman J-L, Soldo Y, Eybert-Bérard L, Menthonnex J-J (1998) Environ Sci Technol 32:1648–1655

    Article  CAS  Google Scholar 

  33. Sarret G, Saumitou-Laprade P, Bert V, Proux O, Hazemann J-L, Traverse A, Marcus MA, Manceau A (2002) Plant Physiol 130:1815–1826

    Article  PubMed  CAS  Google Scholar 

  34. Sarret G, van Gronsveld J, Manceau A, Musso M, D’Haen J, Menthonnex J-J, Hazeman J-L (2001) Environ Sci Technol 35:2854–2859

    Article  PubMed  CAS  Google Scholar 

  35. von Wiren N, Klair S, Bansal S, Briat JF, Khodr H, Shioiri T, Leigh RA, Hider RC (1999) Plant Physiol 119:1107–1114

    Article  Google Scholar 

  36. Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wiren N (2004) J Biol Chem 279:9091–9096

    Article  PubMed  CAS  Google Scholar 

  37. Casaravilla C, Brearley C, Soulé S, Fontana C, Veiga N, Bessio MI, Ferreira F, Kremer C, Diaz A (2006) FEBS J 273:3192–3203

    Article  PubMed  CAS  Google Scholar 

  38. Morris ER, Ellis R (1976) J Nutr 106:753–760

    PubMed  CAS  Google Scholar 

  39. Tauris B, Borg S, Gregersen PL, Holm PB (2009) J Exp Bot 60:1333–1347

    Article  PubMed  CAS  Google Scholar 

  40. Waters BM, Uauy C, Dubcovsky J, Grusak MA (2009) J Exp Bot 60:4263–4274

    Article  PubMed  CAS  Google Scholar 

  41. Troll W (1937) Vergleichende Morphologie der höheren Pflanzen. Bornträger, Berlin

    Google Scholar 

  42. Sachs J (1887) Vorlesungen über Pflanzen-Physiologie. Engelmann, Leipzig

    Google Scholar 

  43. Dornez E et al (2011) J Cereal Sci 54:363–373

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by HarvestPlus (Washington, DC, USA). Rothamsted Research receives strategic support from the Biotechnology and Biological Science Research Council of the UK. Access to the Diamond Light Source synchrotron facility was made available by the Science and Technology Facilities Council of the UK. The authors are grateful for two anonymous reviews which helped improve the manuscript considerably. We are also grateful to Gerhard Leubner for allowing us to use the images in Fig. 1.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrew L. Neal.

Electronic supplementary material

Below is the link to the electronic supplementary material.

775_2013_1000_MOESM1_ESM.pdf

Comparison of single-shell and asymmetric-shell zinc phytate models to EXAFS data collected from Bobwhite aleurone cells. The asymmetric model not only provides a lower reduced χ 2 (χ 2 red.), indicating a better fit to the experimental data, but also provides a visually better description of the second-shell feature at approximately 3.5 Å in the Fourier transform. Details of the models are provided in the text (PDF 73 kb)

Supplementary material 2 (PDF 141 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Neal, A.L., Geraki, K., Borg, S. et al. Iron and zinc complexation in wild-type and ferritin-expressing wheat grain: implications for mineral transport into developing grain. J Biol Inorg Chem 18, 557–570 (2013). https://doi.org/10.1007/s00775-013-1000-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-013-1000-x

Keywords

Navigation