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Cannabis sativa L. growing on heavy metal contaminated soil: growth, cadmium uptake and photosynthesis

  • Published:
Biologia Plantarum

Abstract

The effects of different cadmium concentrations [17 mg(Cd) kg−1(soil) and 72 mg(Cd) kg− 1(soil)] on Cannabis sativa L. growth and photosynthesis were examined. Hemp roots showed a high tolerance to Cd, i.e. more than 800 mg(Cd) kg−1(d.m.) in roots had no major effect on hemp growth, whereas in leaves and stems concentrations of 50 – 100 mg(Cd) kg−1(d.m.) had a strong effect on plant viability and vitality. For control of heavy metal uptake and xylem loading in hemp roots, the soil pH plays a central role. Photosynthetic performance and regulation of light energy consumption were analysed using chlorophyll fluorescence analysis. Seasonal changes in photosynthetic performance were visible in control plants and plants growing on soil with 17 mg(Cd) kg−1(soil). Energy distribution in photosystem 2 is regulated in low and high energy phases that allow optimal use of light and protect photosystem 2 from overexcitation, respectively. Photosynthesis and energy dissipation were negatively influenced by 72 mg(Cd) kg−1(soil). Cd had detrimental effects on chlorophyll synthesis, water splitting apparatus, reaction centre, antenna and energy distribution of PS 2. Under moderate cadmium concentrations, i.e. 17 mg(Cd) kg−1(soil), hemp could preserve growth as well as the photosynthesis apparatus, and long-term acclimation to chronically Cd stress occurred.

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Abbreviations

AAS:

atomic absorption spectroscopy

Cd1, Cd2:

cadmium concentration 1, 2

d.m.:

dry mass

ET:

electron transport

f.m.:

fresh mass

PPFD:

photosynthetic photon flux density

PS 2:

photosystem 2

ΔpH:

proton gradient

ΦPS2 :

quantum efficiency of photosystem 2

qP :

photochemical quenching

qN :

non-photochemical quenching

qE :

energy dependent quenching

qT :

quenching related to state transition

qI :

photoinhibitory quenching

qF :

fast-relaxing non-photochemical quenching

References

  • Adriano, D.C.: Trace Elements in the Terrestrial Environment.-Springer, Berlin 1986.

    Google Scholar 

  • Allaway, W.H.: The environmental cycling of trace elements.-Adv. Agron. 20: 235–274, 1968.

    Google Scholar 

  • Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris.-Plant Physiol. 24: 1–15, 1949.

    Google Scholar 

  • Axelsen, B.A., Palmgren, M.G.: Inventory of the superfamily of P-type ion pumps in Arabidopsis.-Plant Physiol. 126: 696–706, 2001.

    Article  PubMed  Google Scholar 

  • Bansal, P., Sharma, P., Goyal, V.: Impact of lead and cadmium on enzyme of citric acid cycle in germinating pea seeds.-Biol. Plant. 45: 125–127, 2002.

    Article  Google Scholar 

  • Baryla, A., Carrier, P., Franck, F., Coulomb, C., Sahut, C., Havaux, M.: Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth.-Planta 212: 696–709, 2001.

    Article  PubMed  Google Scholar 

  • Baszynski, T., Wajda, L., Krol, M., Wolinska, D., Krupa, Z., Tukendorf, A.: Photosynthetic activities of cadmium-treated tomato plants.-Physiol. Plant. 48: 365–370, 1980.

    Google Scholar 

  • Bjorkman, O., Demmig, B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants diverse origins.-Planta 170: 489–504, 1987.

    Article  Google Scholar 

  • Boddi, B., Oravecz, A.R., Lehoczki, E.: Effect of cadmium on organization and photoreduction of protochlorophyllide in dark-grown leaves and etioplast inner membrane preparations of wheat.-Photosynthetica 31: 411–420, 1995.

    Google Scholar 

  • Bolhar-Nordenkampf, H.R., Long, S.P., Lechner, E.G.: Die Bestimmung der Photosynthesekapazitatuber die Chlorophyllfluoreszenz als Maß fur die Streßbelastung von Baumen.-Phyton 29: 119–135, 1989.

    Google Scholar 

  • Chugh, L.K., Sawhney, S.K.: Photosynthetic activities of Pisum sativum seedlings grown in presence of cadmium.-Plant Physiol. Biochem. 37: 297–303, 1999.

    Article  Google Scholar 

  • Chronopoulos, J., Haidouti, C., Chronopoulou-Sereli, A., Massas, I.: Variations in plant and soil lead and cadmium content in urban parks in Athens, Greece.-Sci. total Environ. 196: 91–98, 1997.

    Article  Google Scholar 

  • Dahmani-Muller, H., Van Oort, F., Balabane, M.: Strategies of heavy metal uptake by three plant species growing near a metal smelter.-Environ. Pollut. 109: 231–238, 2000.

    Article  PubMed  Google Scholar 

  • Dietz, K.-J., Baier, M., Kramer, U.: Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants.-In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants. Pp. 73–98. Springer, Heidelberg 1999.

    Google Scholar 

  • Dubey, R.S.: Photosynthesis in plants under stressful conditions.-In: Pessarakli, M. (ed.): Handbook of Photosynthesis. Pp. 859–876. Marcel Dekker, New York 1997.

    Google Scholar 

  • El-Shintinawy, F.: Glutathione counteracts the inhibitory effect induced by cadmium on photosynthetic process in soybean.-Photosynthetica 36: 171–179, 1999.

    Article  Google Scholar 

  • Ernst, W.: Physiological and biochemical aspects of metal tolerance.-In: Mansfield, T.A. (ed.): Effects of Air Pollutants on Plants. Pp. 115–133. Cambridge University Press, Cambridge 1976.

    Google Scholar 

  • Ernst, W.H.O.: Bioavailability of heavy metals and decontamination of soils by plants.-Appl. Geochem. 11: 163–167, 1996.

    Article  Google Scholar 

  • Felix, H.: Field trials for in situ decontamination of heavy metal polluted soils using crops of metal-accumulating plants.-Z. Pflanzenernahr. Bodenk. 160: 525–529, 1997.

    Google Scholar 

  • Foy, C.D., Chaney, R.L., White, M.C.: The physiology of metal toxicity in plants.-Ann. Rev. Plant Physiol. 29: 511–566, 1978.

    Article  Google Scholar 

  • Genty, B., Briantais, J.-M., Baker, N.R.: The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.-Biochim. biophys. Acta 990: 87–92, 1989.

    Google Scholar 

  • Greer, D.H., Ottander, C., Oquist, G.: Photoinhibition and recovery of photosynthesis in intact barley leaves at 5 °C and 20 °C.-Physiol. Plant. 81: 203–210, 1991.

    Article  Google Scholar 

  • Greger, M.: Metal availability and bioconcentration in plants.-In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants. Pp. 1–28. Springer, Heidelberg 1999.

    Google Scholar 

  • Heber, U., Bukhov, N.G., Shuvalov, V.A., Kobayashi, Y., Lange, O.L.: Protection of the photosynthetic apparatus against damage by excessive illumination in homoiohydric leaves and poikilohydric mosses and lichens.-J. exp. Bot. 52: 1999–2006, 2001.

    Article  PubMed  Google Scholar 

  • Hetherington, S.E., He, J., Smillie, R.M.: Photoinhibition at low temperature in chilling-sensitive and-resistant plants.-Plant Physiol. 90: 1609–1615, 1989.

    Google Scholar 

  • Horton, P., Ruban, A.V., Walters, R.G.: Regulation of light harvesting in green plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 655–694, 1996.

    PubMed  Google Scholar 

  • Horvath, G., Droppa, M., Oravecz, A., Raskin, V.I., Marder, J.B.: Formation of the photosynthetic apparatus during greening of cadmium-poisoned barley leaves.-Planta 199: 238–244, 1996.

    Google Scholar 

  • Jiang, W., Liu, D.: Effects of Pb2+ on root growth, cell division, and nucleolus of Zea mays L.-Bull. Environ. Contam. Toxicol. 65: 786–793, 2000.

    Article  PubMed  Google Scholar 

  • Kevresan, S., Kirsek, S., Kandrae, J., Petrovic, N., Kelemen, Dj.: Dynamics of cadmium distribution in the intercellular space and inside cell in soybean roots, stems and leaves.-Biol. Plant. 46: 85–88, 2003.

    Article  Google Scholar 

  • Khudsar, T., Mahmooduzzafar, Iqbal, M., Sairam, R.K.: Zinc-induced changes in morpho-physiological and biochemical parameters in Artemisia annua.-Biol. Plant. 48: 255–260, 2004.

    Article  Google Scholar 

  • Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: The basics.-Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 313–349, 1991.

    Article  Google Scholar 

  • Krupa, Z., Baszynski, T.: Some aspects of heavy metal toxicity towards photosynthetic apparatus-direct and indirect effects on light and dark reaction.-Acta Physiol. Plant. 17: 177–190, 1995.

    Google Scholar 

  • Lee, K.C., Cunningham, B.A., Paulsen, G.M., Liang, G.H., Moore, R.B.: Effects of cadmium on respiration rate and activities of several enzymes in soybean seedlings.-Physiol. Plant. 36: 4–6, 1976.

    Google Scholar 

  • Linger, P., Bruggemann, W.: Correlations between chlorophyll fluorescence quenching parameters and photosynthesis in a segregating Lycopersicon esculentum × L. peruvianum population as measured under constant conditions.-Photosynth. Res. 61: 145–156, 1999.

    Article  Google Scholar 

  • Linger, P., Mussig, J., Fischer, H., Kobert, J.: Industrial hemp (Cannabis sativa L.) growing on heavy metal contaminated soil: fibre quality and phytoremediation potential.-Ind. Crops Prod. 16: 33–42, 2002.

    Article  Google Scholar 

  • Liu, D., Jiang, W., Gao, X.: Effects of cadmium on root growth, cell division and nucleoli in root tip cells of garlic.-Biol. Plant. 47: 79–83, 2003/4.

    Article  Google Scholar 

  • Losch, R., Kohl, K.I.: Plant respiration under the influence of heavy metals.-In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants. Pp. 139–156. Springer, Heidelberg 1999.

    Google Scholar 

  • Lunackova, L., Masarovicova, E., Kral’ova, K., Stresko, V.: Responses of fast growing woody plants from family Salicaceae to cadmium treatment.-Bull. Envrion. Contam. Toxicol. 70: 576–585, 2003.

    Article  Google Scholar 

  • Mazen, A.M.A.: Accumulation of four metals in tissues of Corchorus olitorius and possible mechanisms of their tolerance.-Biol. Plant. 48: 267–272, 2004.

    Article  Google Scholar 

  • Oquist, G., Chow, W.S., Anderson, J.M.: Photoinhibition of photosynthesis represents a mechanism for long-term regulation of photosystem II.-Planta 186: 450–460, 1992.

    Google Scholar 

  • Oquist, G., Hurry, V.M., Huner, N.P.A.: The temperature dependence of the redox state of QA and susceptibility of photosynthesis to photoinhibition.-Plant Physiol. Biochem. 31: 683–691, 1993.

    Google Scholar 

  • Ouzounidou, G., Moustakas, M., Eleftheriou, E.P.: Physiological and ultrastructural effects of cadmium on wheat (Triticum aestivum L.) leaves.-Arch. Environ. Contam. Toxicol. 32: 154–160, 1997.

    Article  PubMed  Google Scholar 

  • Prasad, M.N.V.: Cadmium toxicity and tolerance in vascular plants.-Environ. exp. Bot. 35: 525–545, 1995.

    Article  Google Scholar 

  • Prasad, M.N.V., Strzalka, K.: Impact of heavy metals on photosynthesis.-In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants. Pp. 117–138. Springer, Heidelberg 1999.

    Google Scholar 

  • Rama Devi, S., Prasad, M.N.V.: Membrane lipid alterations in heavy metal exposed plants.-In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants. Pp. 99–116, Springer, Heidelberg 1999.

    Google Scholar 

  • Robinson, B.H., Leblanc, M., Petit, D., Kirkham, K.H., Gregg, P.E.H.: The potential of Thlaspi caerulescens for phytoremediation of contaminated soils.-Plant Soil 203: 47–56, 1998.

    Article  Google Scholar 

  • Ruban, A.V., Horton, P.: Regulation of non-photochemical quenching of chlorophyll fluorescence in plants.-Aust. J. Plant Physiol. 22: 221–230, 1995.

    Google Scholar 

  • Salt, D.E., Blaylock, M., Kumar, N.P.B.A., Dushenkov, V., Ensley, B.D., Chet, I., Raskin, I.: Phytoremediation: a novel strategy for removal of toxic metals from environment using plants.-Biotechnology 13, 468–474, 1995a.

    Article  PubMed  Google Scholar 

  • Salt, D.E., Prince, R.C., Pickering, I.J., Raskin, I.: Mechanisms of cadmium mobility and accumulation in Indian mustard.-Plant Physiol. 109: 1427–1433, 1995b.

    PubMed  Google Scholar 

  • Sanita di Toppi, L., Gabbrielli, R.: Response to cadmium in higher plants.-Environ. exp. Bot. 41: 105–130, 1999.

    Article  Google Scholar 

  • Saxena, P.K., Krishna Raj, S., Perras, M.R., Vettakkorumakankav, N.N.: Phytoremediation of heavy metal contaminated and polluted soils.-In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants. Pp. 305–329. Springer, Heidelberg 1999.

    Google Scholar 

  • Schreiber, U., Bilger, W.: Rapid assessment of stress effects on plant leaves by chlorophyll fluorescence measurements.-In: Tenhunen, J.D., Catarino, F.M., Lange, O.L., Oechel, W.D. (ed.): Plant Response to Stress. Pp. 27–53. Springer, Heidelberg 1987.

    Google Scholar 

  • Schreiber, U., Neubauer, C.: O2-dependent electron flow, membrane energization and the mechanisms of nonphotochemical quenching of chlorophyll fluorescence.-Photosynth. Res. 25: 279–293, 1990.

    Article  Google Scholar 

  • Schreiber, U., Schliwa, U., Bilger, W.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.-Photosynth. Res. 10: 51–62, 1986.

    Article  Google Scholar 

  • Seregin, I.V., Ivanov, V.B.: Physiological aspects of cadmium and lead toxic effects on higher plants.-Russ. J. Plant Physiol. 48: 523–544, 2001.

    Article  Google Scholar 

  • Sheoran, I.S., Singal, H.R., Singh, R.: Effect of cadmium and nickel on photosynthesis and the enzymes of photosynthetic carbon reduction cycle in pigeon-pea (Cajanus cajan L.).-Photosynth. Res. 23: 345–351, 1990.

    Article  Google Scholar 

  • Siedlecka, A., Krupa, Z.: Cd/Fe interaction in higher plants-its consequences for the photosynthetic apparatus.-Photosynthetica 36: 321–331, 1999.

    Article  Google Scholar 

  • Simonovicova, M., Tamas, L., Huttova, J., Mistrik, I.: Effect of aluminium on oxidative stress related enzymes activities in barley roots.-Biol. Plant. 48: 261–266, 2004.

    Article  Google Scholar 

  • Stiborova, M.: Cd2+ ions affect the quaternary structure of ribulose-1,5-bisphosphate carboxylase from barley leaves.-Biochem. Physiol. Pflanz. 183: 371–378, 1988.

    Google Scholar 

  • Stobart, A.K., Griffiths, W.T., Ameen-Bukhari, I., Sherwood, R.P.: The effect of Cd2+ on biosynthesis of chlorophyll in leaves of barley.-Physiol. Plant. 63: 293–298, 1985.

    Google Scholar 

  • Walters, R.G., Horton, P.: Resolution of components of nonphotochemical chlorophyll fluorescence quenching in barley leaves.-Photosynth. Res. 27: 121–133, 1991.

    Article  Google Scholar 

  • Weigel, H.J.: The effect of Cd2+ on photosynthetic reactions of mesophyll protoplasts.-Physiol. Plant. 63: 192–200, 1985.

    Google Scholar 

  • Weis, E., Berry, J.A.: Plants and high temperature stress.-In: Longe, S.F., Woodward, F.I. (ed.): Plants and Temperature. Pp. 329–346. Company of Biologists Ltd, Cambridge 1988.

    Google Scholar 

  • Yang, X., Baligar, V.C., Martens, D.C., Clark, R.B.: Cadmium effects on influx and transport of mineral nutrients in plant species.-J. Plant Nutr. 19: 643–656, 1996.

    Google Scholar 

  • Zenk, M.H.: Heavy metal detoxification in higher plants-a review.-Gene 179: 21–30, 1996.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Physiological Chemistry of Plants, Dept. C - Mathematics and Science, Bergische University of Wuppertal, Gauss Str. 20, D-42097, Wuppertal, Germany

    P. Linger & A. Ostwald

  2. Geobotany, Heinrich-Heine-University, Universitatsstr. 1, D-40225, Dusseldorf, Germany

    J. Haensler

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  1. P. Linger
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  2. A. Ostwald
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  3. J. Haensler
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Correspondence to P. Linger.

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Linger, P., Ostwald, A. & Haensler, J. Cannabis sativa L. growing on heavy metal contaminated soil: growth, cadmium uptake and photosynthesis. Biol Plant 49, 567–576 (2005). https://doi.org/10.1007/s10535-005-0051-4

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  • DOI: https://doi.org/10.1007/s10535-005-0051-4

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