SpringerLink
Log in

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

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 288:7351–7362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alves S, Trancoso MA, Gonçalves MDLS, Correia dos Santos MM (2011) A nickel availability study in serpentinised areas of Portugal. Geoderma 164:155–163

    Article  CAS  Google Scholar 

  • Anjum NA, Hasanuzzaman M, Hossain MA et al (2015) Jacks of metal/metalloid chelation trade in plants—an overview. Front Plant Sci 6:192

    PubMed  PubMed Central  Google Scholar 

  • 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 166:270–277

    Article  CAS  PubMed  Google Scholar 

  • 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 38:437–448

    Article  CAS  PubMed  Google Scholar 

  • Baker a JM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    Google Scholar 

  • 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 265:225–242

    Article  CAS  Google Scholar 

  • 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 314:35–48

    Article  CAS  Google Scholar 

  • 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 249–269

    Chapter  Google Scholar 

  • 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 191–248

    Chapter  Google Scholar 

  • Brooks RR, Shaw S, Asensi Marfil A (1981) The chemical form and physiological function of nickel in some Iberian Alyssum species. Physiol Plant 51:167–170

    Article  CAS  Google Scholar 

  • Callahan DL, Roessner U, Dumontet V et al (2012) Elemental and metabolite profiling of nickel hyperaccumulators from New Caledonia. Phytochemistry 81:80–89

    Article  CAS  PubMed  Google Scholar 

  • Cappa JJ, Pilon-Smits E a H (2014) Evolutionary aspects of elemental hyperaccumulation. Planta 239:267–275

    Article  CAS  PubMed  Google Scholar 

  • 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 44:2904–2910

    Article  CAS  PubMed  Google Scholar 

  • 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 402:3287–3298

    Article  CAS  PubMed  Google Scholar 

  • 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 4:319

    Article  PubMed  PubMed Central  Google Scholar 

  • Frey B, Keller C, Zierold K (2000) Distribution of Zn in functionally different leaf epidermal cells of the hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 23:675–687

    Article  CAS  Google Scholar 

  • 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 23:1068

    Article  CAS  Google Scholar 

  • 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 51:848–853

    Article  CAS  PubMed  Google Scholar 

  • 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 3:1340

    Article  CAS  PubMed  Google Scholar 

  • 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, 135–189

    Chapter  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Cal Agric Exp Stn Circ 347:1–32

    Google Scholar 

  • Jalilehvand F (2006) Sulfur: not a “silent” element any more. Chem Soc Rev 35:1256–1268

    Article  CAS  PubMed  Google Scholar 

  • Kawashima CG, Noji M, Nakamura M et al (2004) Heavy metal tolerance of transgenic tobacco plants over-expressing cysteine synthase. Biotechnol Lett 26:153–157

    Article  CAS  PubMed  Google Scholar 

  • Koptsik GN (2014) Problems and prospects concerning the phytoremediation of heavy metal polluted soils: a review. Eurasian Soil Sci 47:923–939

    Article  CAS  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    Article  CAS  PubMed  Google Scholar 

  • Krämer U, Cotter-Howells JD, Charnock JM et al (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638

    Article  Google Scholar 

  • Kubota M, McGonigle TP, Hyakumachi M (2001) Clethra barbinervis, a member of the order Ericales, forms arbuscular mycorrhizae. Can J Bot 79:300–306

    Google Scholar 

  • Küpper H (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300

    Article  PubMed  Google Scholar 

  • Küpper H, Jie Zhao F, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–312

    Article  PubMed Central  Google Scholar 

  • Kutrowska A, Szelag M (2014) Low-molecular weight organic acids and peptides involved in the long-distance transport of trace metals. Acta Physiol Plant 36:1957–1968

    Article  CAS  Google Scholar 

  • Leitenmaier B, Küpper H (2013) Compartmentation and complexation of metals in hyperaccumulator plants. Front Plant Sci 4:1–13

    Article  Google Scholar 

  • 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 34:1131–1148

    Article  CAS  PubMed  Google Scholar 

  • Macnair MR (2003) The hyperaccumulation of metals by plants. Adv Bot Res 40:63–105

    Article  CAS  Google Scholar 

  • Mattarozzi M, Visioli G, Sanangelantoni AM, Careri M (2015) ESEM-EDS: in vivo characterization of the Ni hyperaccumulator Noccaea caerulescens. Micron 75:18–26

    Article  CAS  PubMed  Google Scholar 

  • McNear DH, Kupper JV (2014) Mechanisms of trichome-specific Mn accumulation and toxicity in the Ni hyperaccumulator Alyssum murale. Plant Soil 377:407–422

    Article  CAS  Google Scholar 

  • 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 71:188–200

    Article  CAS  PubMed  Google Scholar 

  • Na G, Salt DE (2011) The role of sulfur assimilation and sulfur-containing compounds in trace element homeostasis in plants. Environ Exp Bot 72:18–25

    Article  CAS  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S et al (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • Noji M (2001) Cysteine synthase overexpression in tobacco confers tolerance to sulfur-containing environmental pollutants. Plant Physiol 126:973–980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okamoto K, Yamamoto Y, Fuwa K (1978) Accumulation of manganese, zinc, cobalt, nickel and cadmium by Clethra barbinervis. Agric Biol Chem 42:663–664

    CAS  Google Scholar 

  • 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 60:467–474

    Article  CAS  PubMed  Google Scholar 

  • Page V, Feller U (2015) Heavy metals in crop plants: transport and redistribution processes on the whole plant level. Agronomy 5:447–463

    Article  CAS  Google Scholar 

  • Palit S, Sharma A, Talukder G (1994) Effects of cobalt on plants. Bot Rev 60:149–181

    Article  Google Scholar 

  • 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

  • Rennenberg H, Herschbach C, Haberer K, Kopriva S (2007) Sulfur metabolism in plants: are trees different? Plant Biol 9:620–627

    Article  CAS  PubMed  Google Scholar 

  • Sagner S, Kneer R, Wanner G et al (1998) Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry 47:339–347

    Article  CAS  PubMed  Google Scholar 

  • 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 125:441–453

    CAS  Google Scholar 

  • Sharma SS, Dietz KJ, Mimura T (2016) Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant Cell Environ 39:1112–1126

    Article  CAS  PubMed  Google Scholar 

  • 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 20:898–906

    Article  CAS  Google Scholar 

  • Sytar O, Kumar A, Latowski D et al (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999

    Article  CAS  Google Scholar 

  • Tabuchi M, Asakura H, Morimoto H et al (2016) Hard X-ray XAFS beamline, BL5S1, at AichiSR. J Phys Conf Ser 712:012027

    Article  CAS  Google Scholar 

  • 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 62:157–184

    Article  CAS  PubMed  Google Scholar 

  • 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 175:641–654

    Article  CAS  PubMed  Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD et al (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334

    Article  CAS  Google Scholar 

  • Vatansever R, Ozyigit II, Filiz E (2016) Essential and beneficial trace elements in plants, and their transport in roots: a review. Appl Biochem Biotechnol 181:1–19

    Google Scholar 

  • 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 36:1064–1066

    Article  CAS  Google Scholar 

  • Yamaguchi T, Tomioka R, Takenaka C (2015) Can Clethra barbinervis distinguish nickel and cobalt in uptake and translocation? Int J Mol Sci 16:21378–21391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 57:2353–2366

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Tomioka R, Takenaka C (2017) Accumulation of cobalt and nickel in tissues of Clethra barbinervis in a metal dosing trial. Plant Soil 421:273–283

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601, Japan

    Tsuyoshi Yamaguchi, Rie Tomioka & Chisato Takenaka

  2. Synchrotron Radiation Research Center, Nagoya University, Nagoya, 464-8603, Japan

    Chie Tsukada & Kentaro Takahama

  3. SPring-8 Service Co., Ltd., Tatsuno, Japan

    Toshiki Hirotomo

Authors
  1. Tsuyoshi Yamaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chie Tsukada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kentaro Takahama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Toshiki Hirotomo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rie Tomioka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chisato Takenaka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tsuyoshi Yamaguchi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by R. Guy.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yamaguchi, T., Tsukada, C., Takahama, K. et al. Localization and speciation of cobalt and nickel in the leaves of the cobalt-hyperaccumulating tree Clethra barbinervis. Trees 33, 521–532 (2019). https://doi.org/10.1007/s00468-018-1797-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-018-1797-6

Keywords

Search

Navigation