Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Cell wall immobilisation and antioxidant status of Xanthoria parietina thalli exposed to cadmium

Luigi Sanità di Toppi A , Rosita Marabottini B , Zulema Vattuone A , Rita Musetti C , Maria Augusta Favali A , Agostino Sorgonà D and Maurizio Badiani D E
+ Author Affiliations
- Author Affiliations

A Dipartimento di Biologia Evolutiva e Funzionale, Sezione di Biologia Vegetale, Università di Parma, viale delle Scienze 11 / A, I-43100 Parma, Italy.

B Dipartimento di Agrobiologia e Agrochimica, Università della Tuscia, via SC De Lellis, I-01100 Viterbo, Italy.

C Dipartimento di Biologia Applicata alla Difesa delle Piante, Università di Udine, via delle Scienze 208, I-33100 Udine, Italy.

D Dipartimento di Biotecnologie per il Monitoraggio Agro-Alimentare ed Ambientale, Università Mediterranea di Reggio Calabria, Loc. Feo di Vito, I-89124 Reggio Calabria, Italy.

E Corresponding author. Email: mbadiani@unirc.it

Functional Plant Biology 32(7) 611-618 https://doi.org/10.1071/FP04237
Submitted: 13 December 2004  Accepted: 26 April 2005   Published: 7 July 2005

Abstract

Total and cell wall-bound cadmium and the major antioxidants were measured in thalli of the lichen Xanthoria parietina (L.) Th. Fr. exposed to two Cd concentrations, namely 4.5 or 9.0 μm, in liquid medium during exposure periods of either 24 or 48 h. Total Cd in the thalli was within the range of previous field measurements and was proportional to the exposure concentration, but less than proportional with respect to exposure duration. More than half of the total Cd was immobilised by the cell wall. The adopted conditions of Cd stress caused: (i) no changes in dry weight and protein concentration; (ii) an increase in the level of ascorbic acid and a decrease in that of reduced glutathione, as well as an increase in guaiacol peroxidase activity; (iii) no changes or moderate decreases in the activities of superoxide dismutase, catalase, dehydroascorbate-, NADPH-dependent glutathione disulfide-, and monodehydroascorbate reductases and of ascorbate peroxidase; (iv) an increase of the level of thiobarbituric acid-reactive substances, assumed to reflect malondialdehyde formation arising from membrane lipid peroxidation. Thus, X. parietina might withstand realistic levels of Cd stress by: (1) intercepting the heavy metal at cell wall level, (2) the intervention of antioxidant metabolites, and (3) a moderate increase in guaiacol peroxidase activity.

Keywords: antioxidants, cadmium, cell wall, lichens, heavy metals, oxidative stress.


Acknowledgments

We thank the ‘Fondazione Cassa di Risparmio di Parma’ (Italy) for a dedicated doctoral fellowship awarded to ZV.


References


Aebi, H (1983). Catalase. In ‘Methods of enzymatic analysis. Vol. 3. (3rd edn)’. pp. 273–277. (Verlag Chemie: Weinheim)

Amako K, Chen G-X, Asada K (1994) Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant and Cell Physiology 35, 497–504. open url image1

Asada K (1984) Chloroplasts: formation of active oxygen and its scavenging. Methods in Enzymology 105, 422–429. open url image1

Bačkor MD, Fahselt R, Davidson CT, Wu CT (2003) Effects of copper on wild and tolerant strains of the lichen photobiont Trebouxia erici (Chlorophyta) and possible tolerance mechanisms. Archives of Environmental Contamination and Toxicology 45, 159–167.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Borraccino G, Dipierro S, Arrigoni O (1989) Interaction of ascorbate free radical reductase with sulfhydryl reagents. Phytochemistry 28, 715–717.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
PubMed |
open url image1

Branquinho, C (2001). Lichens. In ‘Metals in the environment: analysis by biodiversity’. pp. 117–157. (Marcel Dekker: New York)

Branquinho C, Brown DH, Maguas C, Catarino F (1997) Lead (Pb) uptake and its effects on membrane integrity and chlorophyll fluorescence in different lichen species. Environmental and Experimental Botany 37, 95–105.
Crossref | GoogleScholarGoogle Scholar | open url image1

Branquinho C, Catarino F, Brown DH, Pereira MJ, Soares A (1999) Improving the use of lichens as biomonitors of atmospheric metal pollution. Science of the Total Environment 232, 67–77.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chettri MK, Sawidis T, Zachariadis GA, Stratis JA (1997) Uptake of heavy metals by living and dead Cladonia thalli. Environmental and Experimental Botany 37, 39–52.
Crossref | GoogleScholarGoogle Scholar | open url image1

Collen J, Pinto E, Pedersen M, Colepicolo P (2003) Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutant metals. Archives of Environmental Contamination and Toxicology 45, 337–342.
PubMed |
open url image1

Cuny D, van Haluwyn C, Shirali P, Zerimech F, Jerome L, Haguenoer JM (2004) Cellular impact of metal trace elements in terricolous lichen Diploschistes muscorum (Scop.) R. Sant. — identification of oxidative stress biomarkers. Water, Air, and Soil Pollution 152, 55–69.
Crossref | GoogleScholarGoogle Scholar | open url image1

De Knecht JA, Van Dillen M, Koevoets PLM, Schat H, Verkleji JAC, Ernst WHO (1994) Phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris: chain length distribution and sulphide incorporation. Plant Physiology 104, 255–261.
PubMed |
open url image1

Elstner, EF , Youngman, RJ ,  and  Osswald, W (1983). Superoxide dismutase. In ‘Methods of enzymatic analysis. Vol. 3. (3rd edn)’. pp. 293–302. (Verlag Chemie: Weinheim)

Esterbauer, H (1982). Aldehyde products of lipid peroxidation. In ‘Free radicals, lipid peroxidation and cancer’. pp. 101–128. (Academic Press: Boca Raton)

Favali MA, Fossati F, Pucci S, Sanità di Toppi L (2002) I licheni come bioindicatori dell’inquinamento dell’aria e come bioaccumulatori di metalli pesanti (in Italian). Inquinamento 36, 75–79. open url image1

Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signaling. Physiologia Plantarum 100, 241–254.
Crossref | GoogleScholarGoogle Scholar | open url image1

Garty, J (2000). Trace metals, other chemical elements and lichen physiology: research in the nineties. In ‘Trace elements — their distribution and effects in the environment’. pp. 277–322. (Elsevier: Amsterdam)

Grill E, Winnacker E-L, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230, 674–676. open url image1

Guelfi A, Azevedo RA, Lea PJ, Molina SM (2003) Growth inhibition of the filamentous fungus Aspergillus nidulans by cadmium: an antioxidant enzyme approach. Journal of General and Applied Microbiology 49, 63–73.
PubMed |
open url image1

Halliwell, B ,  and  Gutteridge, JMC (1989). ‘Free radicals in biology and medicine.’ (Clarendon Press: Oxford)

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jacob C, Courbot M, Brun A, Steinman HM, Jacquot JP, Botton B, Chalot M (2001) Molecular cloning, characterization and regulation by cadmium of a superoxide dismutase from the ectomycorrhizal fungus Paxillus involutus.  European Journal of Biochemistry 268, 3223–3232.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Miszalski Z, Botton B, Turnau K (1996) New SOD isoform in Rhizopogon roseulus (Corda in Sturm) in the presence of cadmium. Acta Physiologiae Plantarum 18, 129–134. open url image1

Olmos E, Martinez-Solano JR, Piqueras A, Hellin E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). Journal of Experimental Botany 54, 291–301.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pandolfini T, Gabbrielli R, Comparini C (1992) Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant, Cell and Environment 15, 719–725. open url image1

Pawlik-Skowrońska B, Sanità di Toppi L, Favali MA, Fossati F, Pirszel J, Skowroński T (2002) Lichens respond to heavy metals by phytochelatin synthesis. New Phytologist 156, 95–102.
Crossref | GoogleScholarGoogle Scholar | open url image1

Puckett KJ (1988) Bryophytes and lichens as monitors of metal deposition. Bibliotheca Lichenologica 30, 231–267. open url image1

Purvis OW, Elix JA, Broomhead A, Jones GC (1987) The occurrence of copper-norstictic acid in lichens from cupriferous substrata. Lichenologist 19, 193–203. open url image1

Rijstenbil JW, Sandee A, Van Drie J, Wijnholds JA (1994) Interaction of toxic trace metals and mechanisms of detoxification in the planktonic diatoms Ditylum brightwellii and Thalassiosira pseudonana.  FEMS Microbiology Reviews 14, 387–396.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Romero-Puertas MC, Palma JM, Gòmez M, del Río LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant, Cell and Environment 25, 677–686.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sandalio LM, Dalurzo HC, Gòmez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. Journal of Experimental Botany 52, 2115–2126.
PubMed |
open url image1

Sanità di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environmental and Experimental Botany 41, 105–130.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sanità di Toppi, L , Prasad, MNV ,  and  Ottonello, S (2002). Metal chelating peptides and proteins in plants. In ‘Physiology and biochemistry of heavy metal detoxification and tolerance in plants’. pp. 59–93. (Kluwer Academic Publishers: Dordrecht)

Sanità di Toppi, L , Gremigni, P , Pawlik-Skowrońska, B , Prasad, MNV ,  and  Cobbett, CS (2003). Response to heavy metals in plants: a molecular approach. In ‘Abiotic stresses in plants’. pp. 133–156. (Kluwer Academic Publishers: Dordrecht)

Sanità di Toppi L, Musetti R, Marabottini R, Corradi MG, Vattuone Z, Favali MA, Badiani M (2004) Responses of Xanthoria parietina thalli to environmentally relevant concentrations of hexavalent chromium. Functional Plant Biology 31, 329–338.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sanità di Toppi L, Musetti R, Vattuone Z, Pawlik-Skowrońska B, Fossati F, Bertoli L, Badiani M, Favali MA (2005) Cadmium distribution and effects on ultrastructure and chlorophyll status in photobionts and mycobionts of Xanthoria parietina. Microscopy Research and Technique 66,  – . open url image1

Sarret G, Manceau A, Cuny D, Haluwyn C, Deruelle S, Hazemann JL, Soldo Y, Eybert-Berard L, Menthonnex JJ (1998) Mechanisms of lichen resistance to metallic pollution. Environmental Science and Technology 32, 3325–3330.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. Journal of Experimental Botany 53, 1351–1365.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiology 127, 887–898.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Silberstein L, Siegel BZ, Siegel SM, Mukhtar A, Galun M (1996) Comparative studies on Xanthoria parietina, a pollution-resistant lichen, and Ramalina duriaei, a sensitive species. I. Effects of air pollution on physiological processes. Lichenologist 28, 355–365.
Crossref | GoogleScholarGoogle Scholar | open url image1

Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5′-dithiobis(2-nitrobenzoic acid). Analytical Biochemistry 175, 408–413.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Traina, SJ (1999). The environmental chemistry of cadmium. An overview. In ‘Cadmium in soil and plants’. pp. 11–37. (Kluwer Academic Publishers: Dordrecht)

Vido K, Spector D, Lagniel G, Lopez S, Toledano MB, Labarre J (2001) A proteome analysis of the cadmium response in Saccharomyces cerevisiae. Journal of Biological Chemistry 276, 8469–8474.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wang SY, Jiao HJ, Faust M (1991) Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron-induced bud break of apple. Physiologia Plantarum 82, 231–236.
Crossref | GoogleScholarGoogle Scholar | open url image1