REACTION OF THE SUNFLOWER (Helianthus annuus L.) TO NICKEL CONDITIONED BY THE WAY OF METAL PENETRATION
Maria Szymańska
Agricultural University of LublinRenata Matraszek
Agricultural University of LublinAbstract
The purpose of this paper was to determine the sunflower (Helianthus annuus L.) reaction to nickel depending on the metal concentration and penetration way, i.e. through roots or leaves. Nickel was introduced into the nutritional solution (intraroot application) at amounts: 0 (control), 35, 100 or 200 μM, while intraleaf application was performed by spraying plants with water (control) or nickel containing solution at the concentration of 5 or 10 μM. Plants treated with nickel intraroot than intraleaf were characterized by a considerably higher metal content in roots and lower in leaves. Independently of the penetration way increasing metal concentrations caused a significant decrease of the parameters of physiological root activity, i.e. the root volume, total and active adsorption surface and 1 cm3 root active surface, in that a greater decrease of the root parameters was shown on intraroot than intraleaf application of the metal. Environment contamination with nickel
caused also a chlorophyll concentration decrease in leaves, in that intraleaf nickel application, in contrast to intraroot, resulted in a higher decrease of chlorophyll b than a. Older than younger leaves showed a higher susceptibility to nickel applied intraroot, whereas roots were resistant to nickel applied intraleaf. The content of S-SO4 in the sunflower depended on the nickel concentration and penetration way – intraleaf nickel application caused significant S-SO4 increase in leaves and roots, whereas intraroot application resulted in S-SO4 content increase especially in roots.
Keywords:
chlorophyll, nickel, physiological parameters of root, sunflower, S-SO4References
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Abrol Y.P., Ahmad A., 2003. Sulphur in plants. Kluwer Academic Publishers. 420 pp.
Arvik J.H., Zimdahl R.L., 1974. Barriers to the foliar uptake of lead. J. Environm. Qual. 4, 369.
Äyräs M., Niskavaara H., Bogatyrev I., 1997. Regional patterns of heavy metals (Co, Cr, Cu, Fe, Ni, Pb, V and Zn) and sulphur in terrestrial moss samples as indication of airborne pollution in a 188 000 km2 area in northern Finland, Norway and Russia. J. Geochem. Explor. 58, 269–281.
Barałkiewicz D., Siepak J., 1999. Chromium, nickel and cobalt in environmental samples and existing legal norms. Environm. Stud. 4, 201–208.
Barcan V., Kovnatsky E., 1998. Soil surface geochemical anomaly around the cooper-nickel metallurgical smelter. Water, Air, and Soil Pollution. 103, 197–218.
Basławska S.S., Trubieckowa O.M., 1964. Plant physiology practice (in Russian). Praktikum po fizjołogii rastenii. Izdatelstwo Moskowskowo Uniwersiteta. 198–205.
Crooke W.M., 1956. Effect of soil reaction on uptake of nickel from serpentine soil. Soil Sci. 81, 269–276.
Drążkiewicz M., 1994. Nickel influence on plant photosynthetic apparatus (in Polish). Wpływ niklu na aparat fotosyntetyczny roślin. Wiad. Bot. 38, 77–84.
Emsley J., 1997. The elements (in Polish). Chemia. Przewodnik po pierwiastkach. Wyd. Nauk. PWN, Warszawa, 255 pp
Foyer C.H., Theodoulou F.L., Delrot S., 2001. The functions of inter-and intracellular glutathione transport systems in plants. Trends in Plant Sci. 6(10), 486–492.
Galler J., 1992. Schwermetalltransfer in der Nahrungskette. Forderungsdienst Beratungsservice. 9, 61–68.
Gorlach E., Gambuś F., 1992. A comparison of sensitivity to the toxic action of heavy metals in various plant species. Pol. J. Soil Sci. 25 (2), 107–213.
Gorlach E., Gambuś F., Brydak K., 1994. Heavy metals content in soils and plants around Sendzimir smelting works (in Polish). Zawartość metali ciężkich w glebach i roślinach wokół Huty im. Tadeusza Sendzimira. Acta Agr. Silv. Agr. 32, 13–24.
Gorlach E., Gambuś F., 1997. Phosphorus and multicomponent fertilizers as a source of soil pollution by heavy metals (in Polish). Nawozy fosforowe i wieloskładnikowe jak źródło zanieczyszczenia metalami ciężkimi. Zesz. Probl. Post. Nauk Roln. 448a, 139–146.
Hartmann T., Honicke P., Wirtz M., Hell R., Rennenberg H., Kopriva S., 2004. Regulation of sulphate assimilation by glutathione in poplars (Populus tremula L. × P. alba.) of wild type and overexpressing (gamma)-glutamylcysteine synthetase in the cytosol. J. Exp. Bot. 55(398), 837–845.
Hunter J.G., Vergnano O., 1953. Trace elements toxicities in oat plants. Ann. App. Biol. 40, 746–777.
Jasiewicz Cz., Buczek J., Sendor R., 1998. Nickel contents in soil and winter wheat cultivated along the E-4 Tarnów – Rzeszów – Przemyśl highway (in Polish). Zawartość niklu w glebie i pszenicy ozimej uprawianej przy trasie E-4 Tarnów-Rzeszów-Przemyśl. Zesz. Nauk. AR im. H. Kołłątaja w Krakowie. 330, 423–428.
Jensen D.L., Holm P.E., Christensen T.H., 2000. Soil and groundwater contamination with heavy metals and two scrap iron and metal recycling facilities. Waste Management & Research 18 (1), 52.
Kączkowski J., 1992. Plant Biochemistry (in Polish). Biochemia roślin. Wyd. Nauk. PWN, Warszawa, 372 pp
Kabata-Pendias A., Motowicka-Terelak T., Piotrowska M., Terelak H., Witek T., 1993. Estimation of the degree of soil and plants contamination with heavy metals and sulphur (in Polish). Ocena stopnia zanieczyszczenia gleb i roślin metalami ciężkimi i siarką. Wyd. IUNG Puławy P(53), 20.
Kabata-Pendias A., Pendias H., 1999. Trace elements biogeochemistry (in Polish). Biogeochemia pierwiastków śladowych. Wyd. Nauk. PWN, Warszawa, 398 pp.
Kopriva S., Rennenberg H., 2004. Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J. Exp. Bot. 55(404), 1831–1842.
Krasowski E., Burski Z., Kulewicz W., 1994. Air pollution nearby highway and its influence on natural agricultural environment (in Polish). Zanieczyszczenie powietrza w pobliżu autostrad i jego wpływ na naturalne środowisko rolnicze. Przegl. Techn. Roln. 10, 24–25.
Krämer U., Smith R.D., Wenzel W.W., Raskin I., Salt D.E., 1997. The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halacsy. Plant Physiol. 115, 1641–1650.
Krupa Z., Siedlecka A., Maksymiec W., Baszyński T., 1993. In vitro response on photosynthetic apparatus of Phaseolus vulgaris L. to nickel toxicity. J. Plant. Physiol. 142, 664–668.
Leustek T., Saito K., 1999. Sulphate transport and assimilation in plants. Plant Physiol. 120(3), 637–644.
Lichtenthaler H.K., Wellburn A., 1983. Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Bioch. Soc. Trans. 603, 591–592.
Macioszczyk A., Dobrzyński D., 2002. Hydrogeochemistry (in Polish). Hydrogeochemia. Wyd. Nauk. PWN, Warszawa, 448 pp.
Marques, L., Cossegal, M., Bodin, S., Czernic, P., Lebrun, M., 2004. Heavy metal specifity of cellular tolerance in two hyperaccumulating plants, Arabidopsis halleri and Thlaspi caerulescens. New Phytologist. 164 (2), 289–295.
Matraszek R., 1998. Chlorophyll content in plants as an indicator of nickel phytotoxcity neutralization by intensive iron fertilization (in Polish). Zawartość chlorofilu w roślinach jako wskaźnik neutralizacji fitotoksyczności niklu przez intensywne żywienie żelazem. Polish Botany on the threshold of the XXI century. J. Miądlikowska (Ed.) Proceeding of the 51 Congress of the Polish Botanical Society ‘Polish Botany on the threshold of the XXI century’, Gdańsk 15–19 September 1998, p. 321.
May M., Vernoux T., Leaver C., Van Montagu M., Inze D., 1998. Reviev article. Glutathione homeostasis in plants: implications for environmental sensing and plant development. J. Exp. Bot. 49, 649–667.
Mishra D., Kar M., 1974. Nickel in plant growth and metabolism. Bot. Rev. 40, 395–452.
Monitor Polski, 1986. no 26, position 170, 285.
Moya J.E., Ros R., Picaza I., 1993. Influence of cadmium and nickel on growth, net photosynthesis and carbohydrate distribution in rice plants. Photosynth. Res. 36, 75-80.
Murashige T., Skoog F., 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473–497.
Obroucheva N.V., Ivanov V.B., Sobotik M., Bergmann H., Antipova O.V., Bystrova E.I., Seregin I.V., Shipgun L.K., 2001. Lead effect on cereal roots in terms of cell growth, root architecture and metal accumulation. In: O. Gasparikova et al. Eds., Kluwer, pp. 165–170.
Ostrowska A., Gawliński S., Szczubiałka Z., 1991. Methods of analysis and estimation of soils and plants properties (in Polish). Metody analizy i oceny właściwości gleb i roślin. Katalog Instytutu Ochrony Środowiska, Warszawa, 334 pp.
Ouzounidou G., 1995. Cu-ions mediated changes in growth, chlorophyll and other ion contents in Cu-tolerant Koeleria splendens. Biol. Plant. 37, 71–78.
Pandey N., Sharma C., 2002. Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci. 163, 753–758.
Punz W.F., Sieghardt H., 1993. The response of roots of herbaceous plant species to heavy metals. Environmental & Experimental Botany. 33(1), 85–98.
Reid R.J., Dunbar M., McLaughlin W., 2003. Cadmium loading into potato tubers: the roles of the periderm, xylem and phloem. Plant, Cell and Environment 26 (2), 201–206.
Rennenberg H., 1982. Glutathione metabolism and possible biological roles in higher plants. Phytochem. 21, 2771–2781.
Robinson B.H., Lombi E., Zhao F.J., McGrath P., 2003. Uptake and distribution of nickel and other metals in the hyperaccumulator Berkhleya coddii. New Phytologist. 158, 279–285.
Salim R., Asubu M.M., Atallah A., 1993. Effects of root and foliar treatments with lead, cadmium and cooper on the uptake, distribution and growth of radish plants. Environ. Inter. 19 (4), 3933–4004.
Sarosiek J., Wożakowska-Natkaniec H., 1993. Chromium and nickel in Lemnaceae family plants in their environment. In: Chromium, nickel and aluminium – ecological and methodical problems (in Polish). Chrom i nikiel w roślinach z rodziny Lemnaceae w ich środowisku. W: Chrom, nikiel i glin – problemy ekologiczne i metodyczne. A. Kabata-Pendias (Red). Zesz. Nauk PAN. Kom. Człowiek i Środowisko 5, 49–54.
Scherer H.W., 2001. Sulphur in crop production – invited paper. Europ. J. Agronomy 14, 81–111.
Seregin I.V., Kozhevnikova A.D., Kazyumina E.M., Ivanov V.B., 2003. Nickel toxicity and distribution in maize roots. Rus. J. Plant Physiol. 50(5), 793–800.
Spiak Z., 1993. Estimation of the toxicity level for spring wheat. In: Chromium, nickel and aluminium – ecological and methodical problems (in Polish). Określenie granicy toksyczności niklu dla pszenicy jarej. W: Chrom, nikiel i glin – problemy ekologiczne i metodyczne. A. Kabata-Pendias (Red). Zesz. Nauk PAN. Kom. Człowiek i Środowisko 5, 153–158.
Spiak Z., 1996. Sensitivity of various plant species to the high concentration of nickel in soil (in Polish). Gatunkowa odporność roślin na wysokie stężenie niklu w glebie. Zesz. Probl. Post. Nauk Roln. 434 (2), 979–984.
Stiborova M., Dubrawowa M., Brezinowa A., Friedrich A., 1986. Effect of heavy metal ions on growth biochemical characteristics of photosynthesis of barley (Hordeum vulgare L.). Photosynthetica 20, 418–425.
Szkolnik M., 1980. Microelemens in plants life (in Polish). Mikroelementy w życiu roślin. Państwowe Wydawnictwo Rolnicze i Leśne, Warszawa, 167 pp.
Szymańska M., Matraszek R., 1996. Iron content in bread bean plants in relation to nickel level in the substrate. (in Polish). Zawartość żelaza w roślinach bobu w zależności od poziomu niklu w podłożu. Zesz. Probl. Post Nauk Roln. 434, 805–810.
Szymańska M., Molas J., 1994. Toxic influence of nickel on cucumber (Cucumis sativus. L.) early development stages at in vitro cultures (in Polish). Toksyczny wpływ niklu na wczesne fazy rozwoju Cucumis sativus L. w warunkach in vitro. Materials of 1st Conference ‘In vitro cultures in plant physiology’, Kraków 15–17 December 1994, pp. 343–351.
Taylor R.W., Allison D.W., 1981. Influence of lead, cadmium and nickel on the growth of alfalfa. Plant Soil. 60, 223–236.
Terelak H., Stuczyński T., Piotrowska M., 1997. Heavy metals in agricultural soils in Poland. Pol. J. Soil Sci. 30 (2), 35–42.
Tolgyessy J., Haranngozo M., Dillinger P., 1993. Determination of Cu, Ni, Zn and Pb contents in Taraxacum officinale near the highway DD-61 Bratislava – Trnava (SR) by radionuclide X-ray fluorescence analysis. J. Radioanal. Nucl. Chem. Letts. 176, 451–455.
Tukendorf A., Rauser W.E., 1990. Changes in glutathione and phytochelatins in roots of maize seedlings exposed to cadmium. Plant. Sci. 70, 155–166.
Vergnano O., Hunter J. G., 1952. Nickel and cobalt toxicities in oat plants. Ann. Bot. 17, 317–328.
Watson C., Pulford I.D., Riddel-Black D., 2003. Development of a hydroponic screening technique to assess heavy metal resistance in willow (Salix). International Journal of Phytoremediation. 5(4), 333–349.
Ye Z.H., Baker A.J.M., Wong M.H., Willis A.J., 1997. Copper and nickel uptake, accumulation and tolerance in Typha latifolia with and without iron plaque on the root surface. New Phytologist 22, 481–488.
Zimdahl R.L., Koeppe D.E., 1978. Uptake by plants. In: W.R. Bogess (Ed), Lead in the environment, Washington, DC, Nat. Sci. Foundation. pp. 99–104.
Abrol Y.P., Ahmad A., 2003. Sulphur in plants. Kluwer Academic Publishers. 420 pp.
Arvik J.H., Zimdahl R.L., 1974. Barriers to the foliar uptake of lead. J. Environm. Qual. 4, 369.
Äyräs M., Niskavaara H., Bogatyrev I., 1997. Regional patterns of heavy metals (Co, Cr, Cu, Fe, Ni, Pb, V and Zn) and sulphur in terrestrial moss samples as indication of airborne pollution in a 188 000 km2 area in northern Finland, Norway and Russia. J. Geochem. Explor. 58, 269–281.
Barałkiewicz D., Siepak J., 1999. Chromium, nickel and cobalt in environmental samples and existing legal norms. Environm. Stud. 4, 201–208.
Barcan V., Kovnatsky E., 1998. Soil surface geochemical anomaly around the cooper-nickel metallurgical smelter. Water, Air, and Soil Pollution. 103, 197–218.
Basławska S.S., Trubieckowa O.M., 1964. Plant physiology practice (in Russian). Praktikum po fizjołogii rastenii. Izdatelstwo Moskowskowo Uniwersiteta. 198–205.
Crooke W.M., 1956. Effect of soil reaction on uptake of nickel from serpentine soil. Soil Sci. 81, 269–276.
Drążkiewicz M., 1994. Nickel influence on plant photosynthetic apparatus (in Polish). Wpływ niklu na aparat fotosyntetyczny roślin. Wiad. Bot. 38, 77–84.
Emsley J., 1997. The elements (in Polish). Chemia. Przewodnik po pierwiastkach. Wyd. Nauk. PWN, Warszawa, 255 pp
Foyer C.H., Theodoulou F.L., Delrot S., 2001. The functions of inter-and intracellular glutathione transport systems in plants. Trends in Plant Sci. 6(10), 486–492.
Galler J., 1992. Schwermetalltransfer in der Nahrungskette. Forderungsdienst Beratungsservice. 9, 61–68.
Gorlach E., Gambuś F., 1992. A comparison of sensitivity to the toxic action of heavy metals in various plant species. Pol. J. Soil Sci. 25 (2), 107–213.
Gorlach E., Gambuś F., Brydak K., 1994. Heavy metals content in soils and plants around Sendzimir smelting works (in Polish). Zawartość metali ciężkich w glebach i roślinach wokół Huty im. Tadeusza Sendzimira. Acta Agr. Silv. Agr. 32, 13–24.
Gorlach E., Gambuś F., 1997. Phosphorus and multicomponent fertilizers as a source of soil pollution by heavy metals (in Polish). Nawozy fosforowe i wieloskładnikowe jak źródło zanieczyszczenia metalami ciężkimi. Zesz. Probl. Post. Nauk Roln. 448a, 139–146.
Hartmann T., Honicke P., Wirtz M., Hell R., Rennenberg H., Kopriva S., 2004. Regulation of sulphate assimilation by glutathione in poplars (Populus tremula L. × P. alba.) of wild type and overexpressing (gamma)-glutamylcysteine synthetase in the cytosol. J. Exp. Bot. 55(398), 837–845.
Hunter J.G., Vergnano O., 1953. Trace elements toxicities in oat plants. Ann. App. Biol. 40, 746–777.
Jasiewicz Cz., Buczek J., Sendor R., 1998. Nickel contents in soil and winter wheat cultivated along the E-4 Tarnów – Rzeszów – Przemyśl highway (in Polish). Zawartość niklu w glebie i pszenicy ozimej uprawianej przy trasie E-4 Tarnów-Rzeszów-Przemyśl. Zesz. Nauk. AR im. H. Kołłątaja w Krakowie. 330, 423–428.
Jensen D.L., Holm P.E., Christensen T.H., 2000. Soil and groundwater contamination with heavy metals and two scrap iron and metal recycling facilities. Waste Management & Research 18 (1), 52.
Kączkowski J., 1992. Plant Biochemistry (in Polish). Biochemia roślin. Wyd. Nauk. PWN, Warszawa, 372 pp
Kabata-Pendias A., Motowicka-Terelak T., Piotrowska M., Terelak H., Witek T., 1993. Estimation of the degree of soil and plants contamination with heavy metals and sulphur (in Polish). Ocena stopnia zanieczyszczenia gleb i roślin metalami ciężkimi i siarką. Wyd. IUNG Puławy P(53), 20.
Kabata-Pendias A., Pendias H., 1999. Trace elements biogeochemistry (in Polish). Biogeochemia pierwiastków śladowych. Wyd. Nauk. PWN, Warszawa, 398 pp.
Kopriva S., Rennenberg H., 2004. Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J. Exp. Bot. 55(404), 1831–1842.
Krasowski E., Burski Z., Kulewicz W., 1994. Air pollution nearby highway and its influence on natural agricultural environment (in Polish). Zanieczyszczenie powietrza w pobliżu autostrad i jego wpływ na naturalne środowisko rolnicze. Przegl. Techn. Roln. 10, 24–25.
Krämer U., Smith R.D., Wenzel W.W., Raskin I., Salt D.E., 1997. The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halacsy. Plant Physiol. 115, 1641–1650.
Krupa Z., Siedlecka A., Maksymiec W., Baszyński T., 1993. In vitro response on photosynthetic apparatus of Phaseolus vulgaris L. to nickel toxicity. J. Plant. Physiol. 142, 664–668.
Leustek T., Saito K., 1999. Sulphate transport and assimilation in plants. Plant Physiol. 120(3), 637–644.
Lichtenthaler H.K., Wellburn A., 1983. Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Bioch. Soc. Trans. 603, 591–592.
Macioszczyk A., Dobrzyński D., 2002. Hydrogeochemistry (in Polish). Hydrogeochemia. Wyd. Nauk. PWN, Warszawa, 448 pp.
Marques, L., Cossegal, M., Bodin, S., Czernic, P., Lebrun, M., 2004. Heavy metal specifity of cellular tolerance in two hyperaccumulating plants, Arabidopsis halleri and Thlaspi caerulescens. New Phytologist. 164 (2), 289–295.
Matraszek R., 1998. Chlorophyll content in plants as an indicator of nickel phytotoxcity neutralization by intensive iron fertilization (in Polish). Zawartość chlorofilu w roślinach jako wskaźnik neutralizacji fitotoksyczności niklu przez intensywne żywienie żelazem. Polish Botany on the threshold of the XXI century. J. Miądlikowska (Ed.) Proceeding of the 51 Congress of the Polish Botanical Society ‘Polish Botany on the threshold of the XXI century’, Gdańsk 15–19 September 1998, p. 321.
May M., Vernoux T., Leaver C., Van Montagu M., Inze D., 1998. Reviev article. Glutathione homeostasis in plants: implications for environmental sensing and plant development. J. Exp. Bot. 49, 649–667.
Mishra D., Kar M., 1974. Nickel in plant growth and metabolism. Bot. Rev. 40, 395–452.
Monitor Polski, 1986. no 26, position 170, 285.
Moya J.E., Ros R., Picaza I., 1993. Influence of cadmium and nickel on growth, net photosynthesis and carbohydrate distribution in rice plants. Photosynth. Res. 36, 75-80.
Murashige T., Skoog F., 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473–497.
Obroucheva N.V., Ivanov V.B., Sobotik M., Bergmann H., Antipova O.V., Bystrova E.I., Seregin I.V., Shipgun L.K., 2001. Lead effect on cereal roots in terms of cell growth, root architecture and metal accumulation. In: O. Gasparikova et al. Eds., Kluwer, pp. 165–170.
Ostrowska A., Gawliński S., Szczubiałka Z., 1991. Methods of analysis and estimation of soils and plants properties (in Polish). Metody analizy i oceny właściwości gleb i roślin. Katalog Instytutu Ochrony Środowiska, Warszawa, 334 pp.
Ouzounidou G., 1995. Cu-ions mediated changes in growth, chlorophyll and other ion contents in Cu-tolerant Koeleria splendens. Biol. Plant. 37, 71–78.
Pandey N., Sharma C., 2002. Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci. 163, 753–758.
Punz W.F., Sieghardt H., 1993. The response of roots of herbaceous plant species to heavy metals. Environmental & Experimental Botany. 33(1), 85–98.
Reid R.J., Dunbar M., McLaughlin W., 2003. Cadmium loading into potato tubers: the roles of the periderm, xylem and phloem. Plant, Cell and Environment 26 (2), 201–206.
Rennenberg H., 1982. Glutathione metabolism and possible biological roles in higher plants. Phytochem. 21, 2771–2781.
Robinson B.H., Lombi E., Zhao F.J., McGrath P., 2003. Uptake and distribution of nickel and other metals in the hyperaccumulator Berkhleya coddii. New Phytologist. 158, 279–285.
Salim R., Asubu M.M., Atallah A., 1993. Effects of root and foliar treatments with lead, cadmium and cooper on the uptake, distribution and growth of radish plants. Environ. Inter. 19 (4), 3933–4004.
Sarosiek J., Wożakowska-Natkaniec H., 1993. Chromium and nickel in Lemnaceae family plants in their environment. In: Chromium, nickel and aluminium – ecological and methodical problems (in Polish). Chrom i nikiel w roślinach z rodziny Lemnaceae w ich środowisku. W: Chrom, nikiel i glin – problemy ekologiczne i metodyczne. A. Kabata-Pendias (Red). Zesz. Nauk PAN. Kom. Człowiek i Środowisko 5, 49–54.
Scherer H.W., 2001. Sulphur in crop production – invited paper. Europ. J. Agronomy 14, 81–111.
Seregin I.V., Kozhevnikova A.D., Kazyumina E.M., Ivanov V.B., 2003. Nickel toxicity and distribution in maize roots. Rus. J. Plant Physiol. 50(5), 793–800.
Spiak Z., 1993. Estimation of the toxicity level for spring wheat. In: Chromium, nickel and aluminium – ecological and methodical problems (in Polish). Określenie granicy toksyczności niklu dla pszenicy jarej. W: Chrom, nikiel i glin – problemy ekologiczne i metodyczne. A. Kabata-Pendias (Red). Zesz. Nauk PAN. Kom. Człowiek i Środowisko 5, 153–158.
Spiak Z., 1996. Sensitivity of various plant species to the high concentration of nickel in soil (in Polish). Gatunkowa odporność roślin na wysokie stężenie niklu w glebie. Zesz. Probl. Post. Nauk Roln. 434 (2), 979–984.
Stiborova M., Dubrawowa M., Brezinowa A., Friedrich A., 1986. Effect of heavy metal ions on growth biochemical characteristics of photosynthesis of barley (Hordeum vulgare L.). Photosynthetica 20, 418–425.
Szkolnik M., 1980. Microelemens in plants life (in Polish). Mikroelementy w życiu roślin. Państwowe Wydawnictwo Rolnicze i Leśne, Warszawa, 167 pp.
Szymańska M., Matraszek R., 1996. Iron content in bread bean plants in relation to nickel level in the substrate. (in Polish). Zawartość żelaza w roślinach bobu w zależności od poziomu niklu w podłożu. Zesz. Probl. Post Nauk Roln. 434, 805–810.
Szymańska M., Molas J., 1994. Toxic influence of nickel on cucumber (Cucumis sativus. L.) early development stages at in vitro cultures (in Polish). Toksyczny wpływ niklu na wczesne fazy rozwoju Cucumis sativus L. w warunkach in vitro. Materials of 1st Conference ‘In vitro cultures in plant physiology’, Kraków 15–17 December 1994, pp. 343–351.
Taylor R.W., Allison D.W., 1981. Influence of lead, cadmium and nickel on the growth of alfalfa. Plant Soil. 60, 223–236.
Terelak H., Stuczyński T., Piotrowska M., 1997. Heavy metals in agricultural soils in Poland. Pol. J. Soil Sci. 30 (2), 35–42.
Tolgyessy J., Haranngozo M., Dillinger P., 1993. Determination of Cu, Ni, Zn and Pb contents in Taraxacum officinale near the highway DD-61 Bratislava – Trnava (SR) by radionuclide X-ray fluorescence analysis. J. Radioanal. Nucl. Chem. Letts. 176, 451–455.
Tukendorf A., Rauser W.E., 1990. Changes in glutathione and phytochelatins in roots of maize seedlings exposed to cadmium. Plant. Sci. 70, 155–166.
Vergnano O., Hunter J. G., 1952. Nickel and cobalt toxicities in oat plants. Ann. Bot. 17, 317–328.
Watson C., Pulford I.D., Riddel-Black D., 2003. Development of a hydroponic screening technique to assess heavy metal resistance in willow (Salix). International Journal of Phytoremediation. 5(4), 333–349.
Ye Z.H., Baker A.J.M., Wong M.H., Willis A.J., 1997. Copper and nickel uptake, accumulation and tolerance in Typha latifolia with and without iron plaque on the root surface. New Phytologist 22, 481–488.
Zimdahl R.L., Koeppe D.E., 1978. Uptake by plants. In: W.R. Bogess (Ed), Lead in the environment, Washington, DC, Nat. Sci. Foundation. pp. 99–104.
Maria Szymańska
Agricultural University of Lublin
Agricultural University of Lublin
Renata Matraszek
Agricultural University of Lublin
Agricultural University of Lublin
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