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Cellular and subcellular compartmentation of Ni in the Eurasian serpentine plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome heratensis (Capparaceae)

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Abstract

This study investigated the cellular and subcellular compartmentation of Ni in the Eurasian serpentine species Alyssum murale, Alyssum bracteatum and Cleome heratensis and a non-serpentine population of A. murale (as a control) grown in hydroponic culture. Plant growth responses and Ni uptake clearly revealed the higher Ni tolerance of serpentine plants than the non-serpentine plants. Serpentine A. murale and A. bracteatum grew better at elevated (0.01 mM) Ni in the nutrient solution, supporting the view that the Ni hyperaccumulators have a higher requirement for Ni than normal plants. Low shoot Ni content of C. heratensis in response to the high Ni treatments indicated that this species employs an avoidance strategy for Ni tolerance. Energy-dispersive X-ray microanalysis showed that Ni was highly concentrated in the cell walls and cell lumen, most likely the vacuoles, of leaf epidermis of A. murale and A. bracteatum rather than in the mesophyll cells. EDX spectra from leaves of the non-serpentine A. murale suggested that Ni accumulated in both epidermal and mesophyll cells but not in the epidermal cell walls. Growth reduction and Ni toxicity in plants of the non-serpentine A. murale could be due to accumulation of Ni in the lumen of leaf mesophyll cells. Our data suggest that cellular and subcellular compartmentation are both possible mechanisms for Ni tolerance employed by the serpentine A. murale and A. bracteatum.

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Abbreviations

EDX:

Energy-dispersive X-ray microanalysis

STEM:

Scanning transmission electron microscope

References

  • Assunçao AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003) A cosegregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens. New Phytol 159:383–390

    Article  CAS  Google Scholar 

  • Baker AJM (1981) Accumulators and excluders: strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    CAS  Google Scholar 

  • Baker AJM, Walker PL (1990) Ecophysiology of metal uptake by tolerant plants. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, pp 155–177

    Google Scholar 

  • Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biochemical resource for phytoremediation of metal-polluted soils. In: Terry N, Bañuelos G (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, pp 85–107

    Google Scholar 

  • Bidwell SD, Crawford SA, Sommer-Knudsen J, Woodrow IE, Marshall AT (2004) Sub-cellular localization of Ni in the hyperaccumulator, Hybanthus floribundus (Lindley) F. Muell. Plant Cell Environ 27:705–716

    Article  CAS  Google Scholar 

  • Boyd RS, Martens SN (1998) Nickel hyperaccumulation of Thlaspi montanum var. montanum (Brassicaceae): a constitutive trait. Am J Bot 85:259–265

    Article  CAS  Google Scholar 

  • Brooks RR (1998) Geobotany and hyperaccumulators. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, New York, pp 55–94

    Google Scholar 

  • Brooks RR, Lee J, Reeves RD, Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium species of indicator plants. J Geochem Explor 7:49–57

    Article  CAS  Google Scholar 

  • Brune A, Urbach W, Dietz K-J (1994) Compartmentation and transport of zinc in barley primary leaves as basic mechanisms involved in zinc tolerance. Plant Cell Environ 17:153–162

    Article  CAS  Google Scholar 

  • Brune A, Urbach W, Dietz K-J (1995) Differential toxicity of heavy metals is partly related to a loss of preferential extraplasmatic compartmentation: a comparison of Cd, Mo, Ni, and Zn stress. New Phytol 129:403–409

    Article  CAS  Google Scholar 

  • Clemens S (2001) Molecular mechanism of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  PubMed  CAS  Google Scholar 

  • Condron RJ, Marshall AT (1990) A comparison of three low temperature techniques of specimen preparation for X-ray microanalysis. Scanning Microsc 4:439–447

    Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  PubMed  CAS  Google Scholar 

  • Heath S, Southworth D, d’Allura JA (1997) Localization of nickel in epidermal subsidiary cells of leaves of Thlaspi montanum var. siskiouense (Brassicaceae) using energy-dispersive X-ray microanalysis. Int J Plant Sci 158:184–188

    Article  CAS  Google Scholar 

  • Ingram P, Shelburne JD, LeFurgey A (1999) Principles and instrumentation. In: Ingram P, Shelburne JD, Roggli VL, LeFurgey A (eds) Biomedical applications of microprobe analysis. Academic, San Diego, pp 1–57

    Google Scholar 

  • Krämer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halácsy. Plant Physiol 115:1641–1650

    PubMed  Google Scholar 

  • Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1353

    Article  PubMed  Google Scholar 

  • Küpper H, Lombi E, Zhao F-J, Wieshammer G, McGrath SP (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 

  • Macnair MR, Bert V, Huitson SB, Saumitou-Laprade P, Petit D (1999) Zinc tolerance and hyperaccumulation are genetically independent characters. Proc R Soc Lond Ser B 266:2175–2179

    Article  CAS  Google Scholar 

  • Marshall AT (1980a) Freeze-substitution as a preparation technique for biological X-ray microanalysis. Scan Electron Microsc 2:395–408

    Google Scholar 

  • Marshall AT (1980b) Sections of freeze-substituted sections. In: Hayat MA (ed) X-ray microanalysis in biology. University Park Press, Baltimore, pp 207–239

    Google Scholar 

  • McGrath SP, Zhao FJ, Lombi E (2002) Phytoremediation of metals, metalloids and radionuclides. Adv Agron 75:1–56

    CAS  Google Scholar 

  • McNear DH, Peltier E, Everhart J, Chaney RL, Sutton S, Neville M, Revers M, Sparks DL (2005) Application of quantitative fluorescence and absorption-edge computed microtomography to image metal compartmentalization in Alyssum murale. Environ Sci Technol 39:2210–2218

    Article  PubMed  CAS  Google Scholar 

  • Mesjasz-Przybylowicz J, Balkwill K, Przybylowicz WJ, Annegarn HJ (1994) Proton microprobe and X-ray fluorescence investigations of nickel distribution in serpentine flora from South Africa. Nucl Inst Meth Phys Res B 89:208–212

    Article  CAS  Google Scholar 

  • Neumann D, zur Nieden U, Lichtenberger O, Leopold I (1995) How does Armeria maritima tolerate high heavy metal concentration? J Plant Physiol 146:704–717

    CAS  Google Scholar 

  • Orlovich DA, Ashford AE (1995) X-ray microanalysis of ion distribution in frozen salt/dextran droplets after freezesubstitution and embedding in anhydrous conditions. J Microsc 180:117–126

    CAS  Google Scholar 

  • Pålsgård E, Lindh U, Roomans GM (1994) Comaparative study of freeze-substitution techniques for X-ray microanalysis of biological tissue. Microsc Res Tech 28:254–258

    Article  PubMed  Google Scholar 

  • Parker DR, Norvell WA, Chaney RL (1995) GEOCHEM-PC: a chemical speciation program for IBM and compatible personal computers. In: Loeppert RH (ed) Chemical equilibrium and reaction models. ASA, SSSA, Madison, pp 253–269

    Google Scholar 

  • Parker DR, Norvell WA (1999) Advances in solution culture methods for plant mineral nutrition research. Adv Agron 65:151–213

    CAS  Google Scholar 

  • Perronnet K, Schwartz C, Gerard E, Morel JL (2000) Availability of cadmium and zinc accumulated in the leaves of Thlaspi caerulescens incorporated into soil. Plant Soil 227:257–263

    Article  CAS  Google Scholar 

  • Persans MW, Nieman H, Salt DE (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc Natl Acad Sci USA 98:9995–10000

    Article  PubMed  CAS  Google Scholar 

  • Proctor J (1999) Toxins, nutrient shortages and droughts: the serpentine challenge. Trends Ecol Evol 14:334–335

    Article  Google Scholar 

  • Przybylowicz WJ, Pineda CA, Prozesky VM, Mesjasz-Przybylowicz J (1995) Investigation of Ni hyperaccumulation by the true elemental imaging. Nucl Inst Meth Phys Res B104:176–181

    Google Scholar 

  • Psaras GK, Constantinidis Th, Cotsopoulos B, Manetas Y (2000) Relative abundance of nickel in the leaf epidermis of eight hyperaccumulators: evidence that the metal is excluded from both guard cells and trichomes. Ann Bot 86:73–78

    Article  CAS  Google Scholar 

  • Reeves RD, Baker AJM (1984) Studies on metal uptake by plants from serpentine and nonserpentine populations of Thlaspi goesingense Halácsy (Cruciferae). New Phytol 98:191–204

    Article  CAS  Google Scholar 

  • Robinson BH, Lombi E, Zhao FJ, McGrath SP (2003) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytol 158:279–285

    Article  CAS  Google Scholar 

  • Sato T (1968) A modified method for lead staining of thin sections. J Electron Microsc 17:158–159

    CAS  Google Scholar 

  • Schat H, Vooijs R, Kuiper E (1996) Identical major gene loci for heavy metal tolerances that have independently evolved in different local populations and subspecies of Silene vulgaris. Evolution 50:1888–1895

    Article  CAS  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 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  PubMed  CAS  Google Scholar 

  • Van Steveninck RFM, Van Steveninck ME (1991) Microanalysis. In: Hall JL, Hawes C (eds) Electron microscopy of plant cells. Academic, London, pp 415–455

    Google Scholar 

  • Vázquez MD, Poschenrieder C, Barceló J, Baker AJM, Hatton P, Cope GH (1994) Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator Thlaspi caerulescens J & C Presl. Bot Acta 107:243–250

    Google Scholar 

  • Verkleij JAC, Schat H (1990) Mechanisms of metal tolerance in higher plants. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, pp 179–193

    Google Scholar 

  • Vögeli-Lange R, Wagner GJ (1990) Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves. Plant Physiol 92:1086–1093

    Article  PubMed  Google Scholar 

  • Zhao FJ, Lombi E, Breedon T, McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514

    Article  CAS  Google Scholar 

Download references

Acknowledgments

A scholarship from the Ministry of Science, Research and Technology of Iran (MSRT), Yasuj University and Isfahan University to TA is gratefully acknowledged. We are very grateful to Dr R. Glaisher (La Trobe University) for assistance with EDX microanalyses and elemental mapping. We also thank the School of Botany (University of Melbourne) for providing research facilities.

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Authors and Affiliations

  1. Department of Biology, University of Isfahan, Isfahan, Iran

    T. Asemaneh & S. M. Ghaderian

  2. School of Botany, University of Melbourne, Parkville, VIC, 3010, Australia

    T. Asemaneh, S. A. Crawford & A. J. M. Baker

  3. School of Zoology, La Trobe University, Bundoora, VIC, 3083, Australia

    A. T. Marshall

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  1. T. Asemaneh
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  2. S. M. Ghaderian
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  3. S. A. Crawford
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  5. A. J. M. Baker
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Correspondence to A. J. M. Baker.

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Asemaneh, T., Ghaderian, S.M., Crawford, S.A. et al. Cellular and subcellular compartmentation of Ni in the Eurasian serpentine plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome heratensis (Capparaceae). Planta 225, 193–202 (2006). https://doi.org/10.1007/s00425-006-0340-y

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