Biogeochemistry

, Volume 104, Issue 1–3, pp 237–249 | Cite as

Subcellular localization of silicon and germanium in grass root and leaf tissues by SIMS: evidence for differential and active transport

  • Jed P. Sparks
  • Subhash Chandra
  • Louis A. Derry
  • Mandayam V. Parthasarathy
  • Carole S. Daugherty
  • Rory Griffin
Article

Abstract

Silicon transport and incorporation into plant tissue is important to both plant physiological function and to the influence plants have on ecosystem silica cycling. However, the mechanisms controlling this transport have only begun to be explored. In this study, we used secondary ion mass spectrometry (SIMS) to image concentrations of Si in root and shoot tissues of annual blue grass (Poa annua L.) and orchard grass (Dactylis glomerata L.) with the goal of identifying control points in the plant silica uptake pathway. In addition, we used SIMS to describe the distributions of germanium (Ge); the element used to trace Si in biogeochemical studies. Within root tissue, Si and Ge were localized in the suberized thick-walled region of endodermal cells, i.e. the proximal side of endodermal cells which is in close association to the casparian strip. In leaves, Si was present in the cell walls, but Ge was barely detectable. The selective localization of Si and Ge in the proximal side of endodermal cell walls of roots suggests transport control is exerted upon Si and Ge by the plant. The absence of Si in most root cell walls and its presence in the cell walls of leaves (in areas outside of the transpiration terminus) suggests modifications in the chemical form of Si to a form that favors Si complexation in the cell walls of leaf tissue. The low abundance of Ge in leaf tissue is consistent with previous studies that suggest preferential transport of Si relative to Ge.

Keywords

Silicon Germanium Casparian strip Secondary ion mass spectrometry (SIMS) High pressure freezing Freeze-substitution 

References

  1. Alexandre A, Meunier J-D, Colin F, Koud J-M (1997) Plant impact on the biogeochemical cycle of silicon and related weathering processes. Geochim Cosmochim Acta 61:677–682. doi:10.1016/S0016-7037(97)00001-X CrossRefGoogle Scholar
  2. Azam F, Volcani BE (1981) Germanium-silicon interactions in biological systems. In: Simpson TL, Volcani BE (eds) Silicon and siliceous structures in biological systems. Springer-Verlag, New York, pp 43–67Google Scholar
  3. Berner EK, Berner RA (1996) Global environment: water, air, and geochemical cycles. Prentice Hall, Upper Saddle River, NJ, 376 pGoogle Scholar
  4. Blecker SW, King SL, Derry LA, Chadwick OA, Ippolito JA, Kelly EF (2007) The ratio of germanium to silicon in plant phytoliths: quantification of biological discrimination under controlled experimental conditions. Biogeochemistry 86(2):189–199. doi:10.1007/s10533-007-9154-7 CrossRefGoogle Scholar
  5. Bondi A (1964) van der Waals volumes and radii. J Phys Chem 68:441–451CrossRefGoogle Scholar
  6. Capobianco C, Navrotsky A (1982) Calorimetric evidence for ideal mixing of silicon and germanium in glasses and crystals of sodium feldspar composition. Am Mineral 67:718–724Google Scholar
  7. Carnelli AL, Madella M, Theurillat JP (2001) Biogenic silica production in selected alpine plant species and plant communities. Ann Bot 87(4):425–434CrossRefGoogle Scholar
  8. Casey WH, Phillips BL, Furrer G (2001) Aqueous aluminum polynuclear complexes and nanoclusters: a review. Nanoparticles and the environment. Rev Mineral Geochem 44:167–190CrossRefGoogle Scholar
  9. Castaing R, Slodzian G (1962) Microanalyse par emission ionique secondarie. J Microsc (Paris) 1:395–410Google Scholar
  10. Chandra S (2005) Quantitative imaging of subcellular calcium stores in mammalian LLC-PK1 epithelial cells undergoing mitosis by SIMS ion microscopy. Eur J Cell Biol 84:783–797CrossRefGoogle Scholar
  11. Chandra S (2008) Subcellular imaging of RNA distribution and DNA replication in single mammalian cells with SIMS: the localization of heat shock induced RNA in relation to the distribution of intranuclear bound calcium. J Microsc 232:27–35CrossRefGoogle Scholar
  12. Chandra S, Smith DR, Morrison GH (2000) Subcellular imaging by dynamic SIMS ion microscopy. Anal Chem 72:104A–114ACrossRefGoogle Scholar
  13. Chandra S, Kabalka GW, Lorey D R II, Smith DR, Coderre JA (2002) Imaging of fluorine and boron from fluorinated-boronophenylalanine in the same cell at organelle resolution by correlative SIMS ion microscopy and confocal laser scanning microscopy. Clin Cancer Res 8:2675–2683Google Scholar
  14. Conley DJ (2002) Terrestrial ecosystems and the global biogeochemical silica cycle. Global Biogeochem Cycles 16:68(1)–68(8). doi:10.1029/2002GB001894
  15. Cussler EL (1997) Diffusion: mass transfer in fluid systems. Cambridge University Press, Cambridge, p 580Google Scholar
  16. Dahl R, Staehelin LA (1989) High-pressure freezing for the preservation of biological structures: theory and practice. J Electron Microsc Tech 13:165–174CrossRefGoogle Scholar
  17. Delvigne C, Opfergelt S, Cardinal D, Delvaux B, Andre L (2009) Distinct silicon and germanium pathways in the soil-plant system: evidence from banana and horsetail. J Geophys Res 114:G02013. doi:10.1029/2008JG000899 CrossRefGoogle Scholar
  18. Derry LA, Kurtz AC, Ziegler K, Chadwick OA (2005) Biological control of terrestrial silica cycling and export fluxes to watersheds. Nature 433:728–731. doi:10.1038/nature03299 CrossRefGoogle Scholar
  19. Derue C, Gibouin D, Demarty M, Verdus M-C, Lefbre F, Thellier M, Ripoll C (2006) Dynamic-SIMS imaging and quantification of inorganic ions in frozen-hydrate plant samples. Microsc Res Technol 69:53–63CrossRefGoogle Scholar
  20. Edwards JT (1970) Molecular volumes and the Stokes-Einstein equation. J Chem Educ 47:261–270CrossRefGoogle Scholar
  21. Epstein E (1999) Silicon. Annu Rev Plant Physiol Plant Mol Biol 50:641–664CrossRefGoogle Scholar
  22. Evans MJ, Derry LA (2002) Quartz control of high germanium/silicon ratios in geothermal waters. Geology 30:1019–1022CrossRefGoogle Scholar
  23. Fauteux F, Remus-Borel W, Menzies JG, Belanger RR (2005) Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiol Lett 249:1–6CrossRefGoogle Scholar
  24. Froelich PN, Hambrick GA, Andreae MO, Mortlock RA, Edmond JM (1985) The geochemistry of germanium in natural waters. J Geophys Res 90:1133–1141CrossRefGoogle Scholar
  25. Froelich PN, Blanc V, Mortlock RA, Chillrud SN, Dunstan W, Udomkit A, Peng T-H (1992) River fluxes of dissolved silica to the ocean were higher during the glacials: Ge/Si in diatoms, rivers, and oceans. Paleoceanography 7:739–768CrossRefGoogle Scholar
  26. Garvin CJ (2006) An exploratory study of the terrestrial silicon cycle at a small watershed in Northern Vermont. MS thesis, Cornell, Ithaca, New York, USAGoogle Scholar
  27. Gibbs GV, Downs JV, Boisen MB Jr (1994) The elusive SiO bond. Rev Mineral 29:331–368Google Scholar
  28. Grignon N, Halpern S, Jeusset J, Briancon C, Fragu P (1996) Localization of chemical elements and isotopes in the leaf of soybean (Glycine max) by secondary ion mass spectrometry microscopy: critical choice of sample preparation procedure. J Microsc 186:51–66CrossRefGoogle Scholar
  29. Harvey DMR, Hall JL, Flowers TJ, Kent B (1981) Quantitative ion localization within Suaeda meritima leaf mesophyll cells. Planta 151:555–560CrossRefGoogle Scholar
  30. Hildebrand M, Volcani BE, Gassmann W, Schroeder JI (1997) A gene family of silicon transporters. Nature 385:688–689CrossRefGoogle Scholar
  31. Kroger N, Lorenz S, Brunner E, Sumper M (2002) Self-assembly of highly phosphorylated silaffins and their function in biosilica morphogenesis. Science 298:584–586CrossRefGoogle Scholar
  32. Kurtz AC, Derry LA, Chadwick OA (2002) Germanium-silicon fractionation in the weathering environment. Geochim Cosmochim Acta 66:1525–1537CrossRefGoogle Scholar
  33. Lazof DB, Goldsmith JG, Rufty TW, Linton RW (1996) The early entry of Al into cells of intact soybean roots: a comparison of three developmental root regions using secondary ion mass spectrometry imaging. Plant Physiol 112:1289–1300Google Scholar
  34. Linton RW, Goldsmith JG (1992) The role of secondary ion mass spectrometry (SIMS) in biological microanalysis: technique comparisons and prospects. Biol Cell 74:147–160CrossRefGoogle Scholar
  35. Lucas Y (2001) The role of plants in controlling rates and products of weathering: importance of biological pumping. Annu Rev Earth Planet Sci 29:135–163CrossRefGoogle Scholar
  36. Lucas Y, Luizao FJ, Chauvel A, Rouiller J, Nahon D (1993) The relation between biological activity of the rain forest and mineral composition of soils. Science 260:521–523CrossRefGoogle Scholar
  37. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691. doi:10.1038/nature04590 CrossRefGoogle Scholar
  38. Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M (2007) An efflux transporter of silicon in rice. Nature 448:209–212. doi:10.1038/nature05964 CrossRefGoogle Scholar
  39. Martin F et al (1996) Random distribution of Ge and Si in synthetic talc: an EXAFS and FTIR study. Eur J Mineral 8:289–299Google Scholar
  40. Meunier JD, Colin F, Alarcon C (1999) Biogenic silica storage in soils. Geology 27:835–838CrossRefGoogle Scholar
  41. Mitani N, Ma JF, Iwashita T (2005) Identification of the silicon form in xylem sap of rice (Oryza sativa L.). Plant Cell Physiol 46:279–283CrossRefGoogle Scholar
  42. Mortlock RN, Froelich PE (1987) Continental weathering of germanium: Ge/Si in the global river discharge. Geochim Cosmochim Acta 51:2075–2082CrossRefGoogle Scholar
  43. Murnane RJ, Stallard RF (1990) Germanium and silicon in rivers of the Orinoco drainage basin. Nature 344:749–752CrossRefGoogle Scholar
  44. Nikolic M, Nikolic N, Liang YC, Kirkby EA, Romheld V (2007) Germanium-68 as an adequate tracer for silicon transport in plants. Characterization of silicon uptake in different crop species. Plant Physiol 143:495–503CrossRefGoogle Scholar
  45. Perry C (2003) Silicification: the processes by which organisms capture and mineralize silica. In: Riebe P (ed)Reviews in mineralogy and geochemistry, vol 54. Mineral Society America, Washington, DC, pp 291–327Google Scholar
  46. Pokrovski GS, Schott J (1998) Thermodynamic properties of aqueous Ge(IV) hydroxide complexes from 25 to 350 degrees C: implications for the behavior of germanium and the Ge/Si ratio in hydrothermal fluids. Geochim Cosmochim Acta 62(9):1631–1642CrossRefGoogle Scholar
  47. Rafi MM, Epstein E, Falk RH (1994) Silicon deprivation causes physical abnormalities in wheat (Triticum aestivum L.). J Plant Physiol 151:497–501Google Scholar
  48. Rains DW, Epstein E, Zasoski RJ, Aslam M (2006) Active silicon uptake by wheat. Plant Soil 280:223–228CrossRefGoogle Scholar
  49. Ramseyer GO, Morrison GH (1983) Relative sensitivity factors of elements in quantitative secondary ion mass spectrometry analysis of biological reference materials. Anal Chem 55:1963–1970CrossRefGoogle Scholar
  50. Raven JA (2003) Cycling silicon—the role of accumulation in plants. New Phytol 158(3):419–421CrossRefGoogle Scholar
  51. Richmond KE, Sussmman M (2003) Got silicon? The non-essential beneficial plant nutrient. Curr Opin Plant Biol 6:268–272CrossRefGoogle Scholar
  52. Shannon RD (1976) Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Crystallogr A A32:751–767CrossRefGoogle Scholar
  53. Shannon RD, Prewitt CT (1969) Effective ionic radii in oxides and fluorides. Acta Crystallogr A B25:925–946Google Scholar
  54. Tamai K, Ma JF (2003) Characterization of silicon uptake by rice roots. Plant Cell Physiol 44:43–48Google Scholar
  55. Tanaka T, Homma Y, Kurosawa S (1988) Secondary ion mass spectrometric ion yields and detection limits of impurities in indium phosphide. Anal Chem 60:58–61CrossRefGoogle Scholar
  56. Treguer P, Nelson DM, Van Bennekom AJ, DeMaster DJ, Leynaert A, Queguiner B (1995) The silica balance in the world ocean: a reestimate. Science 268:375–379CrossRefGoogle Scholar
  57. White AF, Brantley SL (eds) (1995) Chemical weathering rates of silicate minerals. In: Reviews in mineralogy, vol 31. Mineralogical Society of America, Washington, DCGoogle Scholar
  58. Wilson RG (1995) SIMS quantification in Si, GaAs, diamond—an update. Int J Mass Spectrometry 143:43–49CrossRefGoogle Scholar
  59. Yoshida S, Navasero SA, Ramirez EA (1969) Effects of silica and nitrogen supply on some leaf characters of rice plant. Plant Soil 31(1):48–56CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Jed P. Sparks
    • 1
  • Subhash Chandra
    • 2
  • Louis A. Derry
    • 3
  • Mandayam V. Parthasarathy
    • 4
  • Carole S. Daugherty
    • 4
  • Rory Griffin
    • 3
  1. 1.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA
  2. 2.Cornell SIMS Laboratory, Department of Earth and Atmospheric SciencesCornell UniversityIthacaUSA
  3. 3.Department of Earth and Atmospheric SciencesCornell UniversityIthacaUSA
  4. 4.Plant Biology and Cornell Integrated Microscopy CenterCornell UniversityIthacaUSA

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