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Localization and speciation of cobalt and nickel in the leaves of the cobalt-hyperaccumulating tree Clethra barbinervis

  • Tsuyoshi YamaguchiEmail author
  • Chie Tsukada
  • Kentaro Takahama
  • Toshiki Hirotomo
  • Rie Tomioka
  • Chisato Takenaka
Original Article
  • 36 Downloads

Abstract

Key message

The accumulation and tolerance mechanisms for Co are clearly different from those for Ni in the leaves of C. barbinervis in terms of both the distribution and speciation.

Abstract

Clethra barbinervis is a Co-hyperaccumulating tree and also accumulates Ni at high concentrations. The mechanism and role of accumulation in tree physiology remains unclear. The aim of this study was to determine the localization and speciation of Co and Ni in the leaves of C. barbinervis to reveal the mechanisms behind its tolerance to high concentrations of these elements. C. barbinervis seedlings were grown for 3 years under treatments with Co or Ni in the rhizosphere. X-ray fluorescence (XRF) and X-ray absorption near edge structure (XANES) analyses were then used to evaluate the distribution and chemical states of Co, Ni, and S in the adaxial leaf epidermis. In addition, the treated leaves were cut into several parts according to the XRF imaging results on Co or Ni, and the concentrations of elements, sulfate, and organic acids were determined in each part by chemical analyses. XRF images showed that Co was present at the tip of the leaf at a high concentration, whereas Ni was mainly distributed around the leaf edge. Results of chemical analyses on leaf parts containing Co or Ni indicated that sulfate acts as a counter ion for Co and that Ni combined with succinic and/or oxalic acid. In addition, XANES analysis showed that sulfate tended to be reduced and glutathione was generated in the tip of the leaf. Our results indicate that C. barbinervis distinguishes Co and Ni and translocates them to different parts of the leaf.

Keywords

Cobalt (Co) Nickel (Ni) Sulfur (S) Hyperaccumulator X-ray absorption near edge structure (XANES) X-ray fluorescence (XRF) 

Notes

Acknowledgements

We thank Dr. Hirozumi Azuma and Mr. Takaaki Murai of the Aichi Synchrotron Radiation Center, Aichi Science & Technology Foundation and Prof. Masao Tabuchi of the Synchrotron Radiation Research Center at Nagoya University for coordination and technical support at synchrotron X-ray measurements. We thank Prof. Shinya Yagi of the Institute of Materials and Systems for Sustainability at Nagoya University for technical support with collecting the data of S K-edge XANES spectra. The synchrotron X-ray experiments were conducted at the BL5S1 and 6N1 of Aichi Synchrotron Radiation Center, Aichi Science & Technology Foundation, Aichi, Japan (Proposal No. 201702073 and 201704079). This work was supported by JSPS KAKENHI Grant number 17J04296.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Agrawal B, Czymmek KJ, Sparks DL, Bais HP (2013) Transient influx of nickel in root mitochondria modulates organic acid and reactive oxygen species production in nickel hyperaccumulator Alyssum murale. J Biol Chem 288:7351–7362CrossRefGoogle Scholar
  2. Alves S, Trancoso MA, Gonçalves MDLS, Correia dos Santos MM (2011) A nickel availability study in serpentinised areas of Portugal. Geoderma 164:155–163CrossRefGoogle Scholar
  3. Anjum NA, Hasanuzzaman M, Hossain MA et al (2015) Jacks of metal/metalloid chelation trade in plants—an overview. Front Plant Sci 6:192PubMedPubMedCentralGoogle Scholar
  4. Araújo GCL, Lemos SG, Nabais C (2009) Nickel sorption capacity of ground xylem of Quercus ilex trees and effects of selected ligands present in the xylem sap. J Plant Physiol 166:270–277CrossRefGoogle Scholar
  5. Azuma AK, Tomioka R, Takenaka C (2015) Evaluation of microelement contents in Clethra barbinervis as food for human and animals in contrasting geological areas. Environ Geochem Health 38:437–448CrossRefGoogle Scholar
  6. Baker a JM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126Google Scholar
  7. Broadhurst CL, Chaney RL, Angle JS et al (2004) Nickel localization and response to increasing Ni soil levels in leaves of the Ni hyperaccumulator Alyssum murale. Plant Soil 265:225–242CrossRefGoogle Scholar
  8. Broadhurst CL, Tappero RV, Maugel TK et al (2009) Interaction of nickel and manganese in accumulation and localization in leaves of the Ni hyperaccumulators Alyssum murale and Alyssum corsicum. Plant Soil 314:35–48CrossRefGoogle Scholar
  9. Broadley M, Brown P, Cakmak I, Ma JF, Rengel Z, Zhao F (2012a) Beneficial elements. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Elsevier, London, pp 249–269CrossRefGoogle Scholar
  10. Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012b) Function of nutrients: micronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Elsevier, London, pp 191–248CrossRefGoogle Scholar
  11. Brooks RR, Shaw S, Asensi Marfil A (1981) The chemical form and physiological function of nickel in some Iberian Alyssum species. Physiol Plant 51:167–170CrossRefGoogle Scholar
  12. Callahan DL, Roessner U, Dumontet V et al (2012) Elemental and metabolite profiling of nickel hyperaccumulators from New Caledonia. Phytochemistry 81:80–89CrossRefGoogle Scholar
  13. Cappa JJ, Pilon-Smits E a H (2014) Evolutionary aspects of elemental hyperaccumulation. Planta 239:267–275CrossRefGoogle Scholar
  14. Collins RN, Bakkaus E, Carrière M et al (2010) Uptake, localization, and speciation of cobalt in Triticum aestivum L. (Wheat) and Lycopersicon esculentum M. (Tomato). Environ Sci Technol 44:2904–2910CrossRefGoogle Scholar
  15. Donner E, Punshon T, Guerinot ML, Lombi E (2012) Functional characterisation of metal(loid) processes in planta through the integration of synchrotron techniques and plant molecular biology. Anal Bioanal Chem 402:3287–3298CrossRefGoogle Scholar
  16. Fernando DR, Marshall A, Baker AJM, Mizuno T (2013) Microbeam methodologies as powerful tools in manganese hyperaccumulation research: present status and future directions. Front Plant Sci 4:319CrossRefGoogle Scholar
  17. Frey B, Keller C, Zierold K (2000) Distribution of Zn in functionally different leaf epidermal cells of the hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 23:675–687CrossRefGoogle Scholar
  18. Fukuda N, Hokura A, Kitajima N et al (2008) Micro X-ray fluorescence imaging and micro X-ray absorption spectroscopy of cadmium hyper-accumulating plant, Arabidopsis halleri ssp. gemmifera, using high-energy synchrotron radiation. J Anal At Spectrom 23:1068CrossRefGoogle Scholar
  19. Harada E, Hokura A, Takada S et al (2010) Characterization of cadmium accumulation in willow as a woody metal accumulator using synchrotron radiation-based X-ray microanalyses. Plant Cell Physiol 51:848–853CrossRefGoogle Scholar
  20. Harada E, Hokura A, Nakai I et al (2011) Assessment of willow (Salix sp.) as a woody heavy metal accumulator: field survey and in vivo X-ray analyses. Metallomics 3:1340CrossRefGoogle Scholar
  21. Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Møller IS, White P (2012) Functions of Macronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn, Elsevier, London, pp, 135–189CrossRefGoogle Scholar
  22. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Cal Agric Exp Stn Circ 347:1–32Google Scholar
  23. Jalilehvand F (2006) Sulfur: not a “silent” element any more. Chem Soc Rev 35:1256–1268CrossRefGoogle Scholar
  24. Kawashima CG, Noji M, Nakamura M et al (2004) Heavy metal tolerance of transgenic tobacco plants over-expressing cysteine synthase. Biotechnol Lett 26:153–157CrossRefGoogle Scholar
  25. Koptsik GN (2014) Problems and prospects concerning the phytoremediation of heavy metal polluted soils: a review. Eurasian Soil Sci 47:923–939CrossRefGoogle Scholar
  26. Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534CrossRefGoogle Scholar
  27. Krämer U, Cotter-Howells JD, Charnock JM et al (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638CrossRefGoogle Scholar
  28. Kubota M, McGonigle TP, Hyakumachi M (2001) Clethra barbinervis, a member of the order Ericales, forms arbuscular mycorrhizae. Can J Bot 79:300–306Google Scholar
  29. Küpper H (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300CrossRefGoogle Scholar
  30. Küpper H, Jie Zhao F, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–312CrossRefGoogle Scholar
  31. Kutrowska A, Szelag M (2014) Low-molecular weight organic acids and peptides involved in the long-distance transport of trace metals. Acta Physiol Plant 36:1957–1968CrossRefGoogle Scholar
  32. Leitenmaier B, Küpper H (2013) Compartmentation and complexation of metals in hyperaccumulator plants. Front Plant Sci 4:1–13CrossRefGoogle Scholar
  33. Luo Z, He J, Polle A, Rennenberg H (2016) Heavy metal accumulation and signal transduction in herbaceous and woody plants: paving the way for enhancing phytoremediation efficiency. Biotechnol Adv 34:1131–1148CrossRefGoogle Scholar
  34. Macnair MR (2003) The hyperaccumulation of metals by plants. Adv Bot Res 40:63–105CrossRefGoogle Scholar
  35. Mattarozzi M, Visioli G, Sanangelantoni AM, Careri M (2015) ESEM-EDS: in vivo characterization of the Ni hyperaccumulator Noccaea caerulescens. Micron 75:18–26CrossRefGoogle Scholar
  36. McNear DH, Kupper JV (2014) Mechanisms of trichome-specific Mn accumulation and toxicity in the Ni hyperaccumulator Alyssum murale. Plant Soil 377:407–422CrossRefGoogle Scholar
  37. McNear DH, Chaney RL, Sparks DL (2010) The hyperaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage. Phytochemistry 71:188–200CrossRefGoogle Scholar
  38. Na G, Salt DE (2011) The role of sulfur assimilation and sulfur-containing compounds in trace element homeostasis in plants. Environ Exp Bot 72:18–25CrossRefGoogle Scholar
  39. Noctor G, Mhamdi A, Chaouch S et al (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484CrossRefGoogle Scholar
  40. Noji M (2001) Cysteine synthase overexpression in tobacco confers tolerance to sulfur-containing environmental pollutants. Plant Physiol 126:973–980CrossRefGoogle Scholar
  41. Okamoto K, Yamamoto Y, Fuwa K (1978) Accumulation of manganese, zinc, cobalt, nickel and cadmium by Clethra barbinervis. Agric Biol Chem 42:663–664Google Scholar
  42. Oven M, Grill E, Golan-Goldhirsh A et al (2002) Increase of free cysteine and citric acid in plant cells exposed to cobalt ions. Phytochemistry 60:467–474CrossRefGoogle Scholar
  43. Page V, Feller U (2015) Heavy metals in crop plants: transport and redistribution processes on the whole plant level. Agronomy 5:447–463CrossRefGoogle Scholar
  44. Palit S, Sharma A, Talukder G (1994) Effects of cobalt on plants. Bot Rev 60:149–181CrossRefGoogle Scholar
  45. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org. Accessed 28 Sept 2017
  46. Rennenberg H, Herschbach C, Haberer K, Kopriva S (2007) Sulfur metabolism in plants: are trees different? Plant Biol 9:620–627CrossRefGoogle Scholar
  47. Sagner S, Kneer R, Wanner G et al (1998) Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry 47:339–347CrossRefGoogle Scholar
  48. Saito A, Higuchi K, Hirai M et al (2005) Selection and characterization of a nickel-tolerant cell line from tobacco (Nicotiana tabacum cv. bright yellow-2) suspension culture. Physiol Plant 125:441–453Google Scholar
  49. Sharma SS, Dietz KJ, Mimura T (2016) Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant Cell Environ 39:1112–1126CrossRefGoogle Scholar
  50. Shen ZG, Zhao FJ, McGrath SP (1997) Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum. Plant Cell Environ 20:898–906CrossRefGoogle Scholar
  51. Sytar O, Kumar A, Latowski D et al (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999CrossRefGoogle Scholar
  52. Tabuchi M, Asakura H, Morimoto H et al (2016) Hard X-ray XAFS beamline, BL5S1, at AichiSR. J Phys Conf Ser 712:012027CrossRefGoogle Scholar
  53. Takahashi H, Kopriva S, Giordano M et al (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184CrossRefGoogle Scholar
  54. Tappero R, Peltier E, Gräfe M et al (2007) Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel. New Phytol 175:641–654CrossRefGoogle Scholar
  55. van der Ent A, Baker AJM, Reeves RD et al (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334CrossRefGoogle Scholar
  56. Vatansever R, Ozyigit II, Filiz E (2016) Essential and beneficial trace elements in plants, and their transport in roots: a review. Appl Biochem Biotechnol 181:1–19Google Scholar
  57. Yagi S, Matsumura Y, Soda K et al (2004) Interface study for liquid-solid state surface by means of the S K-edge NEXAFS method. Surf Interface Anal 36:1064–1066CrossRefGoogle Scholar
  58. Yamaguchi T, Tomioka R, Takenaka C (2015) Can Clethra barbinervis distinguish nickel and cobalt in uptake and translocation? Int J Mol Sci 16:21378–21391CrossRefGoogle Scholar
  59. Yamaguchi C, Takimoto Y, Ohkama-Ohtsu N et al (2016) Effects of cadmium treatment on the uptake and translocation of sulfate in Arabidopsis thaliana. Plant Cell Physiol 57:2353–2366CrossRefGoogle Scholar
  60. Yamaguchi T, Tomioka R, Takenaka C (2017) Accumulation of cobalt and nickel in tissues of Clethra barbinervis in a metal dosing trial. Plant Soil 421:273–283CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Graduate School of Bioagricultural SciencesNagoya UniversityNagoyaJapan
  2. 2.Synchrotron Radiation Research CenterNagoya UniversityNagoyaJapan
  3. 3.SPring-8 Service Co., Ltd.TatsunoJapan

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