Comparative study of hyperaccumulation of nickel by Alyssum murale s.l. populations from the ultramafics of Serbia

• Autorzy: Tumi A.F. , Mihailovic N. , Gajic A. , Niketic M. , Tomovic G.
• Języki publikacji: EN

Abstrakty

EN

Ultramafic areas exist in large blocks or as small outcrops separated from other geological substrates in Serbia and host a certain number of facultative serpentinophytes. Among them is Alyssum murale Waldst & Kit. s.l., widespread species distributed in SE Europe and SW Asia and well known example of Ni hyperaccumulators. The aims of the present study were to investigate the level of concentration of Ni (and some elements such as Fe, Mn, Zn, Cu, Ni, Cr, Pb, Co, and Cd) at several serpentine soils in Serbia and to determine the level of accumulation of these elements in roots, shoots, and leaves, with a focus on Ni. The maximum available concentrations of metals in soil dry matter (DM) were 950 mg·kg⁻¹ Fe, 3,110 mg·kg⁻¹ Ca, 4,600 mg·kg⁻¹ Mg, 443 mg·kg⁻¹ Ni, 803 mg·kg⁻¹ Mn, 26 mg·kg⁻¹ Zn, 4 mg·kg⁻¹ Cu, 43 mg·kg⁻¹ Cr, 82 mg·kg⁻¹ Co, 1 mg·kg⁻¹ Cd, and 17 mg·kg⁻¹ Pb. The Ca/Mg ratio in serpentine soils varied from 0.08 to 6.22. In A. murale plants, the maximum concentrations of Ni were up to 2,926 mg·kg⁻¹ in roots, 6,793 mg·kg⁻¹ in shoots, and 13,160 mg·kg⁻¹ in leaves. Ca/Mg ratio in plant tissues were up to 2.25 (roots), 9.25 (shoots), and 15.23 (leaves). Cu content in the roots and shoots was high (up to 1,044 mg·kg⁻¹ Cu and 849 mg·kg⁻¹ Cu). This survey suggests that some A. murale populations from serpentine soils of Serbia emerge as strong Ni hyperaccumulators and can be used for phytoextraction purposes.

• Wydawca: -
• Czasopismo: Polish Journal of Environmental Studies
• Rocznik: 2012
• Tom: 21
• Numer: 6
• Opis fizyczny: p.1855-1866,fig.,ref.

Twórcy

autor

Tumi A.F.

• Institute of Botany and Botanical Garden, Faculty of Biology, University of Belgrade, Takovska 43, 11000 Belgrade, Serbia

autor

Mihailovic N.

• Institute for the Application of Nuclear Energy – INEP, University of Belgrade, Banatska 31b, 11080 Belgrade, Serbia

autor

Gajic A.

• Laboratory of Soil Physics, Institute of Land Management, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11081 Belgrade, Serbia

autor

Niketic M.

• Natural History Museum, Njegoševa 51, 11000 Belgrade, Serbia

autor

Tomovic G.

• Institute of Botany and Botanical Garden, Faculty of Biology, University of Belgrade, Takovska 43, 11000 Belgrade, Serbia

Bibliografia

• 1. PROCTOR J. Vegetation and soil and plant chemistry on ultramafic rocks in the tropical Far East. Persp. Plant. Ecol. Evol. Syst. 6, (1-2), 105, 2003.
• 2. ALEXANDER E.B., COLEMAN R.G., KEELER-WOLFE T. Serpentine Geoecology of Western North America: Geology, Soils, and Vegetation. Oxford University Press: Cary, NC. 2007.
• 3. WHITTAKER R.H. (Ed.). The Ecology of Serpentine Soils. Ecology 35, (2), 258, 1954.
• 4. STEVANOVIĆ V., TAN K., IATROU G. Distribution of the endemic Balkan flora on serpentine I. – obligate serpentine endemics. Plant. Syst. Evol. 242, (1-4), 149, 2003.
• 5. BRADY K.U., KRUCKEBERG A.R., BRADSHAW H.D. Evolutionary ecology of plant adaptation to serpentine soils. Annu. Rev. Ecol. Evol. Syst. 36, 243, 2005.
• 6. KAZAKOU E., DIMITRAKOPOULOS P.G., BAKER A.J.M., REEVES R.D., TROUMBIS A.Y. Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol. Rev. 83, 495, 2008.
• 7. HARRISON S.P., RAJAKARUNA N. (Eds.) Serpentine: Evolution and Ecology in a Model System. University of California Press: Berkeley. 2011.
• 8. PRASAD M.N.V., FREITAS H. Metal hyperaccumulation in plants – Biodiversity prospecting for phytoremediation technology. Electron. J. Biotechnol. 6, (3), 285, 2003.
• 9. BROOKS R.R., MORRISON R.S., REEVES R.D., DUDLEY T.R., AKMAN Y. Hyperaccumulation of Nickel by Alyssum Linnaeus (Cruciferae). Proc. Royal. Soc. Lond. B 203, (1153), 387, 1979.
• 10. KAZAKOU E., ADAMIDIS G.C., BAKER A.J.M., REEVES R.D., GODINO M., DIMITRAKOPOULOS P.G. Species adaptation in serpentine soils in Lesbos Island (Greece): metal hyperaccumulation and tolerance. Plant Soil 332, 369, 2010.
• 11. CECCHI L., GABBRIELLI R., ARNETOLI M., GONNELLI C., HASKO A., SELVI F. Evolutionary lineages of nickel hyperaccumulation and systematics in European Alysseae (Brassicaceae): evidence from nrDNA sequence data. Ann. Botany 106, (5), 751, 2010.
• 12. HARTVIG P. Alyssum L., in: STRID A., TAN, K. (Eds.), Flora Hellenica 2. A. R. G. Gantner Verlag K. G.: Ruggell, pp 199-224, 2002.
• 13. BROOKS R.R., RADFORD C.C. Nickel Accumulation by European Species of the Genus Alyssum. Proc. Royal. Soc. Lond. B 200, (1139), 217, 1978.
• 14. REEVES R.D., KRUCKEBERG A.R., ADIGÜZEL N., KRÄMER U. Studies on the flora of serpentine and other metalliferous areas of western Turkey. S. Afr. J. Sci. 97, 513, 2001.
• 15. DIKLIĆ N. Alyssum L., In: JOSIFOVIĆ M. (Ed.), Flore de la Serbie 3. Academie Serbe des Sciences et des Arts, Belgrade, pp. 286-311, 1973.
• 16. BABALONAS D., KARATAGLIS S., KABASSAKALIS V. The Ecology of Plant Populations Growing on Serpentine Soils. Phyton 24, (2), 225, 1984.
• 17. BANI A., ECHEVARRIA G., SULÇE S., MULLAJ A., MOREL J.L. In-situ phytoextraction of nickel by native population of A. murale on ultramafic site in Albania. Plant Soil 293, 79, 2007.
• 18. BANI A., ECHEVARRIA G., MULLAJ A., REEVES R., MOREL J.L., SULÇE S. Nickel Hyperaccumulation by Brassicaceae in Serpentine Soils of Albania and Northwestern Greece. – In: Soil and Biota of Serpentine: A World View. Proceedings of the Sixth International Conference on Serpentine Ecology. Northeast. Nat. 16, (sp5), 385, 2009.
• 19. BANI A., PAVLOVA D., ECHEVARRIA G., MULLAJ A. Nickel hyperaccumulation by the species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Bot. Serb. 34, (1), 3, 2010.
• 20. BANI A., THOMA F., SKURA E., ECHEVARRIA G., SULÇE S., MOREL J.L. Biodiversity in Metal Rich Soil. Proceedings of the 4th Conference on Water Observation and Information System for Decission Support BALWOIS, Ohrid, Republic of Macedonia, http://www.balwois.com/2010/. Accessed 22 December 2011. 2010.
• 21. ÇULLAJ A., HASKO A., KONGOLI F. Investigation of the potential of several plants for phytoremediation of nickel contaminated soils and for nickel phytoextraction. Eur. J. Miner. Process. Environ. Protect. 4, (2), 144, 2004.
• 22. HASKO A., ÇULLAJ A. Nickel hyper-accumulating species and their potential use for the phyto-remediation of polluted areas. Options Méditerranéennes. Série A: Séminaires Méditerranéens 47, 137, 2001.
• 23. REEVES R.D., ADIGÜZEL N. The Nickel Hyperaccumulating Plants of the Serpentines of Turkey and Adjacent Areas: A Review with New Data. Turk. J. Bot. 32, 143, 2008.
• 24. REEVES R.D., BROOKS R.R., DUDLEY Th.R. Uptake of Nickel by Species of Alyssum, Bornmuellera, and Other Genera of Old World Tribus Alysseae. Taxon 32, (2), 184, 1983.
• 25. REEVES R.D., ADIGÜZEL N., BAKER A.J.M. Nickel Hyperaccumulation in Bornmuellera kiyakii Aytaç & Aksoy and Associated Plants of the Brassicaceae from Kızıldağ (Derebucak, Konya-Turkey). Turk. J. Bot. 33, 33, 2009.
• 26. SHALLARI S., SCHWARTZA C., HASKOB A., MORELA J.L. Heavy metals in soils and plants of serpentine and industrial sites of Albania. Sci. Total Environ. 209, 133, 1998.
• 27. VINTERHALTER B., SAVIĆ J., PLATIŠA J., RASPOR M., NINKOVIĆ S., MITIĆ N., VINTERHALTER D. Nickel tolerance and hyperaccumulation in shoot cultures regenerated from hairy root cultures of Alyssum murale Waldst et Kit. Plant Cell Tiss. Organ. Cult. 94, (3), 299, 2008. 28. ОBRATOV D., KADOVIĆ R., MIHAJLOVIĆ N. Alyssum markgrafii (Brassicaceae, Capparales) as nickel hiperaccumulator on Goč and Kopaonik serpentinites. Proceedings of the 3rd International Conference on the Development of Forestry & Wood Science/Technology, ICFWST '97 volume II, Belgrade & Mt. Goč, pp. 24-28, 1997.
• 29. VINTERHALTER B., VINTERHALTER D. Nickel hyperccumulation in shoot cultures of Alyssum markgrafii. Biol. Plant. 49, 121, 2005.
• 30. NOVÁK F.A. Ad florae Serbiae cognitionem additamentum alterum. Preslia 5, 65, 1927.
• 31. PAVLOVIĆ Z. Charakteristische Elemente der serpentinischen Flora und Vegetation Serbiens. Glas. Prir. Muz. Beograd B18, 3, 1962.
• 32. NIKOLIĆ V., SIGUNOV A., DIKLIĆ N. Dopuna flori SR Srbije novim podacima o rasprostranjenju biljnih vrsta., in: Sarić M., Diklić N. (Eds.), Flore de la Serbie 10. Academie Serbe des Sciences et des Arts: Belgrade, pp. 259-336, 1986.
• 33. VAN REEUWIJK L.P. (Ed.) Procedures for Soil Analysis. 5th ed. Technical Paper//International Soil Reference and Information Centre: Wageningen. 1995.
• 34. ROWELL D.L. Soil Science. Research methods and their applications. Springer: Berlin. 1997 [In German].
• 35. MCKEAGUE J.A. (Ed.) Manual on soil sampling and methods of analysis. Canadian Society of Soil Science, pp. 66-68, 1978.
• 36. EGNER H., RIEHM H., DOMINGO W.R. Studies on the chemical soil analysis as a basis for the assessment of the ground nutrient status of the soil II Chemical Extraction methods to Phosphorus and Potassium determination. K. Lantbr. Hogsk. Annlr. W.R. 26, 199, 1960 [In German].
• 37. VAN REEUWIJK L.P. (Ed.) Procedures for Soil Analysis. 6th ed. Technical Paper/International Soil Reference and Information Centre: Wageningen. 2002.
• 38. FAO The Euphrates Pilot Irrigation Project. Methods of soil analzsis. Gadeb Soil Laboratory (A laboratory manual). Food and Agriculture Organization: Rome. 1974.
• 39. GARCIA W.J., BLESSIN C.W., SANDFORD H.W., INGLETT G.E. Translation and accumulation of seven heavy metals in tissues of corn plants grown on sludge-treated stripmined soil. J. Agric. Food Chem. 27, (5), 1088, 1979.
• 40. CHEN P.S., TORIBARA T.Y., WARNER H. Microdetermination of phosphorus. Anal. Chem. 28, 1756, 1956.
• 41. GHADERIAN S.M., MOHTADI A., RAHIMINEJAD M.R., BAKER A.J.M. Nickel and other metal uptake and accumulation by species of Alyssum (Brassicaceae) from the ultramafics of Iran. Environ. Pollut. 145, 293, 2007.
• 42. KABATA-PENDIAS A. Trace elements in soils and plants. 4th edn CRC Press. Taylor & Francis Group, Boca Raton: London, New York. 2011.
• 43. GHADERIAN S.M., MOHTADI A., RAHIMINEJAD M.R., REEVES R.D., BAKER A.J.M. Hyperaccumulation of nickel by two Alyssum species from the serpentine soils of Iran. Plant Soil 293, 91, 2007.
• 44. OBRATOV-PETKOVIĆ D., BJEDOV I., BELANOVIĆ S. The content of heavy metals in the leaves of Hypericum perforatum L. on serpentinite soils in Serbia. Bull. Fac. For. 98, 143, 2008.
• 45. ADRIANO D.C. Trace elements in terrestrial environments Biogeochemistry, bioavailability, and risks of metals. Springer-Verlag, New York. 2001.
• 46. LOMBINI A., DINELLI E., FERRARI C., SIMONI A. Plant-soil relationships in the serpentinite screes of Mt Prinzera (Northern Apennines, Italy). J. Geochem. Explor. 64, 19, 1998. 47. PANDOLFINI T., PANCARO L. Biogeochemical survey of some ophiolitic outcrops in Tuscany. Flora 187, 341, 1992.
• 48. REEVES R.D., BAKER A.J.M., BORHIDI A., BERAZAIN R. Nickel hyperaccumulation in the serpentine flora of Cuba. Ann. Bot. 83, 29, 1999.
• 49. LARCHER H. Physiological Plant Ecology. SpringerVerlag: Berlin. 1995.
• 50. NARWAL R.P., SINGH M., SINGH J.P. Effect of Ni enriched sewage water on the accumulation of Ni and other heavy metals in corn. J. Ind. Soc. Soil. Sci. 39, 123, 1991.
• 51. PARIDA B.K., CHHIBBA I.M., NAYYAR V.K. Influence of nickel-contaminated soil on fenugreek (Trigonella corniculata L.) growth and mineral composition. Sci. Hort. 98, 113, 2003.
• 52. INGLE R.A., SMITH J.A.C., SWEETLOVE L.J. Responses to nickel in the proteome of the hyperaccumulator plant Alyssum lesbiacum. BioMetals 18, 527, 2005.
• 53. DUDIĆ B., RAKIĆ T., ŠINŽAR-SEKULIĆ J., ATANACKOVIĆ V., STEVANOVIĆ B. Differences of metal concentrations and morpho-anatomical adaptations between obligate and facultative serpentinophytes from Western Serbia. Arch. Biol. Sci., Belgrade 59, (4), 341, 2007.
• 54. MCNEAR D.H., CHANEY R.L., SPARKS D.L. The hypeaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage. Phytochem. 71, 188, 2010.
• 55. BROADHURST C.L., CHANEY R.L., ANGLE J.S., MAUGEL T.K., ERBE E.F., MURPHY C.A. Simultaneous hyperaccumulation of nickel, manganese and calcium in Alyssum leaf trichomes. Environ. Sci. Technol. 38, 5797, 2004.
• 56. FREITAS H., PRASAD M.N.V., PRATAS J. Analysis of serpentinophytes from north-east of Portugal for trace metal accumulation–relevance to the management of mine environment. Chemosphere 54, (11), 1625, 2004.
• 57. ALLEN W.R., SHEPPARD P.M. Copper Tolerance in Some Californian Populations of the Monkey Flower, Mimulus guttatus. Proc. Royal. Soc. Lond. B 177, (1047), 177, 1971.
• 58. NKOANE B.B.M., SAWULA G.M., WIBETOE G., LUND W. Identification of Cu and Ni indicator plants from mineralised locations in Botswana. J. Geochem. Explor. 86, 130, 2005.
• 59. WELSH R.P.H., DENNY P. The uptake of lead and copper by submerged aquatic macrophytes in two English lakes. J. Ecol. 68, 443, 1980.
• 60. ROBINSON B.H., BROOKS R.R., KIRKMAN J.H., GREGG P.E.H., GREMIGNI P. Plant-available elements in soils and their influence on the vegetation over ultramafic (“serpentine”) rocks in New Zealand. J. Royal Soc. N. Zealand 26, 457, 1996.
• 61. KAUR R., BHARDWAJ R., THUKRAL A.K. Growth and heavy metal uptake in B. juncea seedlings as affected by binary interactions between nickel and other heavy metals. Can. J. Pure. Appl. Sci. 4, 1011, 2010.
• 62. LOPEZ-BUCIO J., NIETO-JACOBO M.F., RAMIREZRODRIGUEZ V., HERREA-ESTRELLA L. Organic acid metabolism in plants: From adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci., 160, 1, 2000.
• 63. ROBINSON B.H., BROOKS R.R., CLOTHIER B.E. Soil amendments affecting nickel and cobalt uptake by Berkheya codii: potential use for phytomining and phytoremediation. Ann. Bot. 84, 689, 1999.
• 64. KÜPPER H., LOMBI E., ZHAO F.J., WIESHAMMER G., MCGRATH S.P. Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J. Exp. Bot. 52, 2291, 2001.
• 65. MIHAILOVIC N., DRAZIC G. Incomplete alleviation of nickel toxicity in bean by nitric oxide supplementation. Plant. Soil. Environ. 57, 396, 2011.