Skip to main content
SpringerLink
Log in

Biochemical characterization of cell types within leaves of metal-hyperaccumulating Noccaea praecox (Brassicaceae)

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Distinct metal distribution patterns within leaves of metal hyperaccumulating plants are repeatedly observed however, the presumable role of key structural biochemical molecules in determining and regulating their allocation remains largely unknown. We aimed to characterise in a spatially resolved manner the distribution of the main biochemical components in leaves of field-collected Cd/Zn-hyperaccumulating Noccaea praecox in order to relate them to metal distribution patterns at tissue level.

Methods

The biomolecular composition of the leaves was spatially analysed using synchrotron radiation Fourier Transform Infrared (FTIR) and the distribution of Zn with synchrotron radiation Low-Energy X-Ray Fluorescence (LEXRF) microspectroscopy was determined on the same tissues of interest (epidermis, sub-epidermis, mesophyll).

Results

In epidermal cells high proportion of free-carboxyl, nitro and phosphate groups standing for pectin, nitroaromatics, phytic and other organic acids were found. Adjacent mesophyll cells had higher proportions of proteins, carbohydrates and cellulosic compounds.

Conclusions

Pectin compounds were indicated as important components of Zn enriched epidermal cell walls. In addition, intense lignification of epidermal cell walls might limit leakage of the trapped metals back to the metabolically active and thus more sensitive mesophyll. Distribution of metal-binding compounds in particular cell types/tissues may therefore predispose metal distribution patterns and tolerance in leaves.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Andrade LR, Leal RN, Noseda M, Duarte MER, Pereira MS, Mourão PAS, Farina M, Amado Filho GM (2010) Brown algae overproduce cell wall polysaccharides as a protection mechanism against the heavy metal toxicity. Mar Pollut Bull 60:1482–1488

    Article  PubMed  CAS  Google Scholar 

  • Bonetta DT, Facette M, Raab TK, Somerville CR (2002) Genetic dissection of plant cell-wall biosynthesis. Biochem Soc Trans 30:298–301

    Article  PubMed  CAS  Google Scholar 

  • Cabaniss SE, Leenheer JA, McVey IF (1998) Aqueous infrared carboxylate absorbances, aliphatic di-acids. Spectrochim Acta A 54:449–458

    Article  Google Scholar 

  • Chabannes M, Ruel K, Yoshinaga A, Chabbert B, Jauneau A, Joseleau JP, Boudet AM (2001) In-situ analysis of lignins in transgenic tobacco reveals a differential impact of individual transformations on the spatial patterns of lignin deposition at the cellular and subcellular levels. Plant J 28:271–282

    Article  PubMed  CAS  Google Scholar 

  • Chakravarty S, Mohanty A, Sudha TN, Upadhyay AK, Konar J, Sircar JK, Madhukar A, Gupta KK (2010) Removal of Pb(II) ions from aqueous solution by adsorption using bael leaves (Aegle marmelos). J Hazard Mater 173:502–509

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Coimbra MA, Barros A, Barros M, Rutledge DN, Delgadillo I (1998) Multivariate analysis of uranic acid and neutral sugars in whole pectic samples by FT-IR spectroscopy. Carbohydr Polym 37:241–248

    Article  CAS  Google Scholar 

  • Colzi I, Doumet S, Del Bubba M, Fornaini J, Arnetoli M, Gabbrielli R, Gonnelli C (2011) On the role of the cell wall in the phenomenon of copper tolerance in Silene paradoxa L. Environ Exp Bot 72:77–83

    Article  CAS  Google Scholar 

  • Dokken KM, Davis LC, Marinkovic NS (2005) Use of infrared microspectroscopy in plant growth and development. Appl Spectrosc Rev 40:301–326

    Article  Google Scholar 

  • Ebbs SD, Zambrano MC, Spiller SM, Newville M (2009) Cadmium sorption, influx, and efflux at the mesophyll layer of leaves from ecotypes of the Zn/Cd hyperaccumulator Thlaspi caerulescens. New Phytol 181:626–636

    Article  PubMed  CAS  Google Scholar 

  • Eichert D, Gregoratti L, Kaulich B, Marcello A, Melpignano P, Quaroni L, Kiskinova M (2007) Imaging with spectroscopic micro-analysis using synchrotron radiation. Anal Bioanal Chem 389:1121–1132

    Article  PubMed  CAS  Google Scholar 

  • Eichert D, Lupi S, Perucchi A, Nucara A, Calvani P, Vaccari L, Morgera F, Kiskinova M (2008) Infrared microspectroscopy at SISSI, the ELETTRA Sincrotron Trieste infrared beamline. Synchrotron Radiat News 21:45–50

    Article  Google Scholar 

  • Ernst WHO (2006) Evolution of metal tolerance in higher plants. For Snow Landsc Res 80:251–274

    Google Scholar 

  • Faix O (1992) Fourier transform infrared spectroscopy. In: Lin SY, Dense CW (eds) Methods in lignin chemistry, 6. Springer-Verlag, Berlin, pp 83–109

  • Galichet A, Sockalingum GD, Belarbi A, Manfai M (2001) FTIR spectroscopic analysis of Saccharomyces cerevisiae cell walls: study of an anomalous strain exhibiting a pink-colored cell phenotype. FEMS Microbiol Lett 197:179–186

    Article  PubMed  CAS  Google Scholar 

  • Gianoncelli A, Kaulich B, Alberti R, Klatka T, Longoni A, De Marco A, Marcello A, Kiskinova M (2009) Simultaneous soft X-ray transmission and emission microscopy. Nucl Intrum Meth A 608:195–198

    Article  CAS  Google Scholar 

  • Grant GT, Morris ER, Rees DA, Smith PJC, Thom D (1973) Biological interactions between polysaccharides and divalent cations: the egg-box model. FEBS Lett 32:195–198

    Article  CAS  Google Scholar 

  • Grube M, Muter O, Strikauska S, Gavare M, Limane B (2008) Application of FT-IR spectroscopy for control of the medium composition during the biodegradation of nitroaromatic compounds. J Ind Microbiol Biotechnol 35:1545–1549

    Article  PubMed  CAS  Google Scholar 

  • Guo X, Zhang S, Shan XQ (2008) Adsorption of metal ions on lignin. J Hazard Mater 151:134–142

    Article  PubMed  CAS  Google Scholar 

  • Harris MJ, Turver RJ (1970) Sulphates monosaccharides and derivatives: part VIII. Infrared spectra and optical rotations of some glycoside sulphates. Carbohydr Res 15:51–56

    Article  CAS  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    Article  PubMed  CAS  Google Scholar 

  • He Z, Honeycutt CW, Zhang T, Bertsch PM (2006) Preparation and FT-IR characterization of metal phytate compounds. J Environ Qual 35:1319–1328

    Article  PubMed  CAS  Google Scholar 

  • Himmelsbach D, Khalili S, Akin D (1998) FT-IR microspectroscopic imaging of flax (Linum usitatissimum L.) stems. Cell Mol Biol 44:99–108

    PubMed  CAS  Google Scholar 

  • Hori R, Sugiyama J (2003) A combined FT-IR microscopy and principal component analysis on softwood cell walls. Carbohydr Polym 52:449–453

    Article  CAS  Google Scholar 

  • Ide-Ektessabi A (2007) Applications of synchrotron radiation: microbeams in cell microbiology and medicine. Springer Verlag, Berlin, Heidelberg

    Google Scholar 

  • Ivanova DG, Singh BR (2003) Nondestructive FTIR monitoring of leaf senescence and elicitin-induced changes in plant leaves. Biopolymers 72:79–85

    Article  PubMed  CAS  Google Scholar 

  • Jones L, Milne JL, Ashford D, McCann MC, McQueen-Mason SJ (2005) A conserved functional role of pectic polymers in stomatal guard cells from a range of plant species. Planta 221:255–264

    Article  PubMed  CAS  Google Scholar 

  • Kačuráková M, Wilson RH (2001) Developments in mid infrared FT-IR spectroscopy of selected carbohydrates. Carbohydr Polym 44:291–303

    Article  Google Scholar 

  • Kačuráková M, Capek P, Sasinková V, Wellner N, Ebringerová A (2000) FTIR study of plant cell wall model compounds: pectic polysaccharides and hemicelluloses. Carbohydr Polym 43:195–203

    Article  Google Scholar 

  • Kaulich B, Bacescu D, Susini J, David C, di Fabrizio E, Morrison GR, Charalambous P, Thieme J, Wilhein T, Kovač J, Cocco D, Salomé M, Dhez O, Weitkamp T, Cabrini S, Cojoc D, Gianoncelli A, Vogt U, Podnar M, Zangrando M, Zacchigna M, Kiskinova M (2006) TwinMic - A European twin X-ray microscopy station commissioned at ELETTRA. In: Aoki S, Kagoshima Y, Suzuki Y (eds) Proceedings of the 8th International Conference in X-ray Microscopy. Conference Proceedings Series IPAP 7. The Institute of Pure and Applied Physics, Tokyo, pp 22–25

  • Kaulich B, Gianoncelli A, Beran A, Eichert D, Kreft I, Pongrac P, Regvar M, Vogel-Mikuš K, Kiskinova M (2009) Low-energy X-ray fluorescence microscopy opening new opportunities for bio-related research. J R Soc Interface 6:S641–S647

    Article  PubMed  CAS  Google Scholar 

  • Ke HYD, Anderson WL, Moncrief RM, Rayson GD, Jackson PJ (1994) Luminescence studies of metal ion-binding sites in Datura innoxia biomaterial. Environ Sci Technol 28:586–591

    Article  PubMed  CAS  Google Scholar 

  • Knox JP (2008) Revealing the structural and functional diversity of plant cell walls. Curr Opin Plant Biol 11:308–313

    Article  PubMed  CAS  Google Scholar 

  • Krzesłowska M, Lenartowska M, Mellerowicz EJ, Samardakiewicz S, Woźny A (2009) Pectinous cell wall thickenings formation – a response of moss protonemata cells to lead. Environ Exp Bot 65:119–131

    Article  Google Scholar 

  • Küpper H, Zhao F-J, McGrath S (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–311

    Article  Google Scholar 

  • Küpper H, Mijovilovich A, Meyer-Klauchke W, Kroneck PMH (2004) Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy. Plant Physiol 134:748–757

    Article  PubMed  Google Scholar 

  • Lang I, Wernitznig S (2011) Sequestration at the cell wall and plasma membrane facilitates zinc tolerance in the moss Pohlia drummondii. Environ Exp Bot 74:186–193

    Article  CAS  Google Scholar 

  • Leitenmaier B, Küpper H (2011) Cadmium uptake and sequestration kinetics in individual leaf cell protoplasts of the Cd/Zn hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 34:208–219

    Article  PubMed  CAS  Google Scholar 

  • Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: Impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Biochem 48:673–682

    Article  PubMed  CAS  Google Scholar 

  • Lupi S, Nucara A, Perucchi A, Calvani P, Ortolani M, Quaroni L, Kiskinova M (2007) Performance of SISSI, the infrared beamline of the ELETTRA storage ring. J Opt Soc Am B 24:959–964

    Article  CAS  Google Scholar 

  • Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–736

    Article  PubMed  CAS  Google Scholar 

  • Mari S, Lebrun M (2005) Metal immobilization: where and how? In: Tamás MJ, Martinova E (eds) Molecular biology of metal homeostasis and detoxification. Springer, Berlin, pp 273–298

    Google Scholar 

  • Marry M, Roberts K, Jopson SJ, Huxham IM, Jarvis MC, Corsar J, Robertson E, McCann MC (2006) Cell-cell adhesion in fresh sugar-beet root parencyhma requires both pectin esters and calcium cross-links. Physiol Plant 126:243–256

    Article  CAS  Google Scholar 

  • McCann MC, Shi J, Roberts K, Carpita NC (1994) Changes in pectin structure and localization during the growth of unadapted and NaCl-adapted tobacco cells. Plant J 5:773–785

    Article  CAS  Google Scholar 

  • McKenna BA, Wehr JB, Kopittke PM, Blamey FP, Menzies NW (2010) Novel methods to investigate metal interactions with plant cell walls. In: Gilkes RJ, Prakongkep N (eds) Proceedings of 19th World Congress of Soil Science, Soil Solutions for a Changing World. International Union of Soil Sciences, Brisbane, pp 80–83

  • McNear DH Jr, Chaney RL, Sparks DL (2010) The hyperaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage. Phytochemistry 7:188–200

    Article  Google Scholar 

  • Miller LM, Dumas P (2006) Chemical imaging of biological tissue with synchrotron infrared light. Biochim Biophys Acta 1758:846–857

    Article  PubMed  CAS  Google Scholar 

  • Milner MJ, Kochian LW (2008) Investigating heavy metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13

    Article  PubMed  CAS  Google Scholar 

  • Nari J, Noat G, Ricard J (1991) Pectin methylesterase, metal ions and plant cell-wall extension. Biochem J 279:351–354

    PubMed  Google Scholar 

  • Naumann D (2000) Infrared spectroscopy in microbiology. In: Meyers RA (ed) Encyclopedia of analytical chemistry. John Wiley and Sons, Inc., Chichester, pp 102–131

    Google Scholar 

  • Nelson WH (1991) Modern techniques for rapid microbiological analysis. VCH Publishers, New York

    Google Scholar 

  • Owens HS, McCready RM, Shepherd AD, Schultz TH, Pippen EL, Swenson HS, Miers JC, Erlandsen RF, Maclay MD (1952) Methods used at western regional research laboratory for extraction and analysis of pectic materials. Bureau of Agricultural and Industrial Chemistry, Agricultural Research Administration, U.S. Department of Agriculture, pp 24

  • Pawlukojc A, Leciejewicz J, Ramirez-Cuesta A, Nowicka-Scheibe J (2005) L-cysteine: neutron spectroscopy, Raman, IR and ab initio study. Spectrochim Acta A 61:2474–2481

    Article  CAS  Google Scholar 

  • Pongrac P, Vogel-Mikuš K, Kump P, Nečemer M, Tolrà R, Poschenrieder C, Barceló J, Regvar M (2007) Changes in elemental uptake and arbuscular mycorrhizal colonisation during the life cycle of Thlaspi praecox Wulfen. Chemosphere 69:1602–1609

    Article  PubMed  CAS  Google Scholar 

  • Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181

    Article  PubMed  CAS  Google Scholar 

  • Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 33:713–717

    Article  CAS  Google Scholar 

  • Sattelmacher B (2001) The apoplast and its significance for plant mineral nutrition. New Phytol 149:167–192

    Article  CAS  Google Scholar 

  • Schneider T, Scheloske S, Povh B, Traxel K (2002) A method for cryosectioning of plant roots for proton microprobe analysis. Int J PIXE 12:101–107

    Article  CAS  Google Scholar 

  • Schulz H, Baranska M (2007) Identification and quantification of valuable plant substances by IR and Raman spectroscopy. Vib Spectrosc 43:13–25

    Article  CAS  Google Scholar 

  • Séné CF, McCann MC, Wilson RH, Grinter R (1994) Fourier-transform Raman and Fourier-transform infrared spectroscopy. An investigation of five higher plant cell walls and their components. Plant Physiol 106:1623–1631

    PubMed  Google Scholar 

  • Sinclair SA, Krämer U (2012) The zinc homeostasis network in land plants. Biochim Biophys Acta Mol Cell Res 1823:1553–1567

    Article  CAS  Google Scholar 

  • Singh BK, Sharma RK, Garg BS (2006) Cobalt(II) complexes of biologically active glutathione: spectroscopic and molecular modelling studies. Spectrochim Acta A 63:96–102

    Article  Google Scholar 

  • Solé VA, Papillon E, Cotte M, Walter P, Susini J (2007) A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochim Acta B 62:63–68

    Article  Google Scholar 

  • Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004) Toward a systems approach to understanding plant cell walls. Science 306:2206–2211

    Article  PubMed  CAS  Google Scholar 

  • Stewart D (1995) Fourier-transform infrared microspectroscopy of plant tissues. Appl Spectrosc 50:357–365

    Article  Google Scholar 

  • Thakur BR, Singh RK, Handa AK (1997) Chemistry and uses of pectin – a review. CRC Crit Rev Food Sci Nutr 37:47–73

    Article  CAS  Google Scholar 

  • van de Mortel JE, AlmarVillanueva LA, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Ver Loren van Themaat E, Koornneef M, Aarts MGM (2006) Large expression differences in genes for iron and zinc homeostasis, stress response and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147

    Article  PubMed  Google Scholar 

  • van de Mortel JE, Schat H, Moerland PD, Ver Loren van Theemat E, van der Ent S, Blankestijn H, Ghandilya A, Tsiatsiani S, Aarts MGM (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324

    Article  PubMed  Google Scholar 

  • Vogel JP, Raab TK, Schiff C, Somerville SC (2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14:2095–2106

    Article  PubMed  CAS  Google Scholar 

  • Vogel-Mikuš K, Regvar M, Mesjasz-Przybyłowicz J, Przybyłowicz WJ, Simčič J, Pelicon P, Budnar M (2008a) Spatial distribution of Cd in leaves of metal hyperaccumulating Thlaspi praecox using micro-PIXE. New Phytol 179:712–721

    Article  PubMed  Google Scholar 

  • Vogel-Mikuš K, Simčič J, Pelicon P, Budnar M, Kump P, Nečemer M, Mesjasz-Przybyłowicz J, Przybyłowicz WJ, Regvar M (2008b) Comparison of essential and non-essential element distribution in leaves of the Cd/Zn hyperaccumulator Thlaspi praecox as revealed by micro-PIXE. Plant Cell Environ 31:1484–1496

    Article  PubMed  Google Scholar 

  • Vogel-Mikuš K, Pongrac P, Pelicon P, Vavpetič P, Povh B, Bothe H, Regvar M (2009) Micro-PIXE analysis for localization and quantification of elements in roots of mycorrhizal metal-tolerant plants. In: Varma A, Kharkwal AC (eds) Symbiotic fungi. Soil biology 18. Springer-Verlag, Berlin, pp 227–242

    Chapter  Google Scholar 

  • Wang D, Mills ES, Deal RB (2012) Technologies for system-level analysis of specific cell types in plants. Plant Sci 197:21–29

    Article  PubMed  CAS  Google Scholar 

  • Wellner N, Kačuráková M, Malovikova A, Wilson RH, Belton PS (1998) FT-IR study of pectate and pectinate gels formed by divalent cations. Carbohydr Res 308:123–131

    Article  CAS  Google Scholar 

  • Wetzel DL, Eilert AJ, Pietrzak LN, Miller SS, Sweat JA (1998) Ultraspatially-resolved synchrotron infrared microspectroscopy of plant tissue in situ. Cell Mol Biol 44:145–168

    PubMed  CAS  Google Scholar 

  • Yang J, Hungchen EY (2002) Early salt stress effects on the changes in chemical composition in leaves of ice plant and Arabidopsis. A fourier transform infrared spectroscopy study. Plant Physiol 130:1032–1042

    Article  PubMed  CAS  Google Scholar 

  • Yang YJ, Cheng LM, Liu ZH (2007) Rapid effect of cadmium on lignin biosynthesis in soybean roots. Plant Sci 172:632–639

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by Slovenian Research Agency -ARRS [P1-0212 Biology of Plants], the ARRS Young Researchers Programme, and the EU COST 859 research programmes. Beamtime was provided by Elettra and EU support [proposals number 20085258 and 20085261]. CB is acknowledged for a lecture of the manuscripts English.

Author information

Author notes

  1. Burkhard Kaulich

    Present address: Diamond Light Source Ltd, Diamond House, Harwell Science and Innovation Campus, Didcot, Oxfordshire, OX11 0DE, UK

Authors and Affiliations

  1. Department of Biology, Biotechnical Faculty, University of Ljubljana, Večna pot 111, 1000, Ljubljana, Slovenia

    Marjana Regvar, Paula Pongrac & Katarina Vogel-Mikuš

  2. Elettra-Sincrotrone Trieste, S.S. 14 Km 163.5 in Area Science Park, 34149, Basovizza, Trieste, Italy

    Diane Eichert, Burkhard Kaulich & Alessandra Gianoncelli

Authors
  1. Marjana Regvar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diane Eichert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Burkhard Kaulich
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alessandra Gianoncelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paula Pongrac
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Katarina Vogel-Mikuš
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marjana Regvar.

Additional information

Responsible Editor: Juan Barcelo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Regvar, M., Eichert, D., Kaulich, B. et al. Biochemical characterization of cell types within leaves of metal-hyperaccumulating Noccaea praecox (Brassicaceae). Plant Soil 373, 157–171 (2013). https://doi.org/10.1007/s11104-013-1768-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1768-z

Keywords

Search

Navigation