Photosynthetica, 2017 (vol. 55), issue 1

Photosynthetica 2017, 55(1):193-200 | DOI: 10.1007/s11099-016-0229-3

Toxic effects of high copper content on physiological processes in Pinus sylvestris L.

K. Możdżeń1,*, T. Wanic2, G. Rut1, T. Łaciak3, A. Rzepka1
1 Department of Plant Physiology, Institute of Biology, Pedagogical University, Cracow, Poland
2 Department of Forest Soil Science, Institute of Ecology and Silviculture, Faculty of Forestry, University of Agriculture, Cracow, Poland
3 Department of Vertebrate Zoology and Human Biology, Institute of Biology, Pedagogical University, Cracow, Poland

The aim of this study was to determine the impact of increased copper contents on selected physiological processes in oneyear-old Pinus sylvestris L. needles from a former German timber storage area in Warcino Forest District, a subject to an environmental quality survey. Samples were collected from the area with the high copper content in the soil. The control area was a nearby pine tree stand showing unimpeded growth. The significant growth inhibition was found in dwarf shoots and whole needles, increased water content, and reduced dry mass were also observed. The chlorophyll content was lowered, while 20% higher electrolyte leakage was found. Chlorophyll a fluorescence indicated only higher values of the nonphotochemical quenching in P. sylvestris from the Cu-site. Significant differences were shown in the rate of gas exchange measured by changes in carbon dioxide or oxygen concentration. The intensity of photosynthesis in needles of P. sylvestris from the Cu-site measured by CO2 uptake was considerably higher than that of oxygen production. The rate of respiration in the needles from the Cu-site measured by the amount of released CO2 was higher only by 15%, while according to O2 consumed, the rate increased by 30% in relation to the control. Our results suggest that the copper accumulation in P. sylvestris needles affected the morphology and physiology of the studied organs.

Keywords: chlorophyll fluorescence; growth analysis; photosynthesis; respiration

Received: November 4, 2015; Accepted: March 21, 2016; Published: March 1, 2017Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Możdżeń, K., Wanic, T., Rut, G., Łaciak, T., & Rzepka, A. (2017). Toxic effects of high copper content on physiological processes in Pinus sylvestris L. Photosynthetica, 55(1), 193-200. doi: 10.1007/s11099-016-0229-3.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Alaoui-Sossé B., Genet P., Vinit-Dunand F. et al.: Effect of copper on growth in cucumber plants (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. - Plant Sci. 166: 1213-1218, 2004. Go to original source...
    2. Baker N.R., Rosenquist E.: Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. - C J. Exp. Bot. 55: 1607-1621, 2004. Go to original source...
    3. Baranowska-Morek A.: [Plant mechanisms of tolerance to toxic heavy metals.] - Kosmos 52: 283-298, 2003. [In Polish]
    4. Barnes J.D., Balaguer L., Manrique E. et al.: A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. - Environ. Exp. Bot. 32: 85-100, 1992. Go to original source...
    5. Barón M., Arellano J.B., López Gorgé J.: Copper and photosystem II: A controversial relationship. - Physiol. Plantarum 94: 174-180, 1995. Go to original source...
    6. Björkman O., Demmig B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. - Planta 170: 489-504, 1987. Go to original source...
    7. Bouazizi H., Jouili H., Geitmann A. et al.: Copper toxicity in expanding leaves of Phaseolus vulgaris L.: antioxidant enzyme response and nutrient element uptake. - Ecotox. Environ. Safe. 73: 1304-1308, 2010. Go to original source...
    8. Burkhead J.L., Gogolin Reynolds K.A., Abdel-Ghany S.E. et al.: Copper homeostasis. - New Phytol. 182: 799-816, 2009. Go to original source...
    9. Caspi V., Droppa M., Horváth G. et al.: The effect of copper on chlorophyll organization during greening of barley leaves. - Photosynth. Res. 62: 165-174, 1999. Go to original source...
    10. Chen L.M., Lin C.C., Kao C.H.: Cu toxicity in rice seedlings: changes in antioxidative enzyme activities, H2O2 level and cell wall peroxidase activity in roots. - Bot. Bull. Acad. Sin. 41: 99-103, 2000.
    11. Clijsters H., Cuypers A., Vangronsveld J.: Physiological responses to heavy metals in higher plants; defense against oxidative stress. - C Z. Naturforsch. 54c: 730-734, 1999. Go to original source...
    12. Cruz J.A., Avenson T.J., Kanazawa A. et al.: Plasticity in light reactions of photosynthesis for energy production and photoprotection. - C J. Exp. Bot. 56: 395-406, 2005.
    13. Demidchik V., Sokolik A., Yurin V.: Characteristics of nonspecific permeability and H+-ATPase inhibition induced in the plasma membrane of Nitella flexilis by excessive Cu2+. - Planta 212: 583-590, 2001. Go to original source...
    14. Demidchik V., Sokolik A., Yurin V.: The effect of Cu2+ on ion transport systems of the plant cell plasmalemma. - Plant Physiol. 114: 1313-1325, 1997. Go to original source...
    15. Dmuchowski, W., Bytnerowicz, A.: Monitoring environmental pollution in Poland by chemical analysis of Scots pine (Pinus sylvestris L.) needles. - Environ. Pollut. 87: 87-104, 1995. Go to original source...
    16. Ebbert V., Demmig-Adams B., Adams W.W. et al.: Correlation between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation. - Photosynth. Res. 67: 63-78, 2001. Go to original source...
    17. Elleuch A., Chaabene Z., Grubb D.C. et al.: Morphological and biochemical behavior of fenugreek (Trigonella foenumgraecum) under copper stress. - Ecotoxicol. Environ. Safe. 98: 46-53, 2013. Go to original source...
    18. Gruca-Królikowska S., Wacławek W.: Metals in the environment. Part II. Effect of heavy metals on plants. - Chem. Didact. Ecol. Metrol. 11: 41-55, 2006.
    19. Gupta D., Abdullah: Toxicity of copper and cadmium on germination and seedling growth maize (Zea mays L.) seeds. - Ind. J. Sci. Res. 2: 67-70, 2011.
    20. Hall J.L.: Cellular mechanisms for heavy metal detoxification and tolerance. - C J. Exp. Bot. 53: 53-71, 2002. Go to original source...
    21. Havaux M.: Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. - Plant Cell Environ. 16: 461-467, 1993. Go to original source...
    22. Jegerschöld C., Arellano J.B., Schröder W.P. et al.: Copper (II) inhibition of electron transport through photosystem II studied by EPR spectroscopy. - Biochemistry 34: 12747-12754, 1995. Go to original source...
    23. Jiang W., Liu D., Liu X.: Effects of copper on root growth, cell division, and nucleolus of Zea mays. - Biol. Plantarum 44: 105-109, 2001. Go to original source...
    24. Kalaji H.M., Carpentier R., Allakhverdiev S.I. et al.: Fluorescence parameters as early indicators of light stress in barley. - C J. Photoch. Photobio. B. 112: 1-6, 2012.. Go to original source...
    25. Kalaji M.H., Goltsev V., Bosa K. et al.: Experimental in vivo measurements of light emission in plants: a perspective dedicated to David Walker. - Photosynth. Res. 114: 69-96, 2012.. Go to original source...
    26. Kalaji M.H., Nalborczyk E.: Gas exchange of barley seedlings growing under salinity stress. - Photosynthetica 25: 197-202, 1991.
    27. Kalaji M.H., Schansker G., Ladle R.J. et al.: Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. - Photosynth. Res. 122: 121-158, 2014. Go to original source...
    28. Kopittke P.M., Menzies N.W.: Effect of Cu toxicity on growth of Cowpea (Vigna unguiculata). - Plant Soil 279: 287-296, 2006. Go to original source...
    29. Kramer D.M., Evans J.R.: The importance of energy balance in improving photosynthetic productivity. - Plant Physiol. 155: 70-78, 2011. Go to original source...
    30. Kukkola E., Rautio P., Huttunen S.: Stress indications in copperand nickel-exposed Scots pine seedlings. - Environ. Exp. Bot. 43: 197-210, 2000. Go to original source...
    31. Kurczyńska E.U., Dmuchowski W., Włoch W. et al.: The influence of air pollutants on needles and stems of Scots pine (Pinus sylvestris L.) trees. - Environ. Pollut. 98: 325-334, 1997. Go to original source...
    32. Lichtenthaler H.K., Buschmann C., Knapp M.: How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio Rfd of leaves with the PAM fluorometer. - Photosynthetica 43: 379-393, 2005. Go to original source...
    33. Lichtenthaler H.K., Knapp M., Buschmann C.: Measurement of chlorophyll fluorescence kinetics (Kautsky effect) and the chlorophyll fluorescence decrease ratio (RFd-values) with the PAM-fluorymeter. - In: Filek N., Biesaga-Kościelniak J., Marcińska I. (ed.): Analytical Methods in Plant Stress Biology. Pp. 93-111. The Franciszek Gorski Institute of Plant Physiol. Polish Acad. Sci., Cracow 2004.
    34. Liu D., Jiang W., Meng O. et al.: Cytogenetical and ultrastructural effects of copper on root meristem cells of Allium sativum L. - Biocell 33: 25-32, 2009.
    35. Liu J., Xiong Z.T., Li T.Y. et al.: Bioaccumulation and ecophysiological responses to copper stress in two populations of Rumex dentatus L. from Cu contaminated and noncontaminated sites. - Environ. Exp. Bot. 52: 43-51, 2004. Go to original source...
    36. MacFarlane G.R., Burchett M.D.: Toxicity, growth and accumulation relationships of copper, lead and zinc in the grey mangrove Avicennia marina (Forsk.) Vierh. - Mar. Environ. Res. 54: 65-84, 2002. Go to original source...
    37. Maksymiec W.: Effect of copper on cellular processes in higher plants. - Photosynthetica 34: 321-342, 1997. Go to original source...
    38. Maxwell K., Johnson G.N.: Chlorophyll fluorescence - a practical guide. - C J. Exp. Bot. 51: 659-668, 2000. Go to original source...
    39. Monni S., Salemaa M., White C. et al.: Copper resistance of Calluna vulgaris originating from the pollution gradient of a Cu-Ni smelter, in southwest Finland. - Environ. Pollut. 109: 211-219, 2000. Go to original source...
    40. Monni S., Uhlig C., Hansen E. et al.: Ecophysiological responses of Empetrum nigrum to heavy metal pollution. - Environ. Pollut. 112: 121-129, 2001. Go to original source...
    41. Moreira I.N., Mourato M.P., Reis R. et al.: Oxidative stress induced by cadmium and copper in Brassica rapa leaves: indicators of stress, oxidative damage, and antioxidant mechanisms. - Commun. Soil Sci. Plant 46: 2475-2489, 2015.
    42. Müller P., Li X.P., Niyogi K.K.: Non-photochemical quenching. A response to excess light energy. - Plant Physiol. 125: 1558-1566, 2001. Go to original source...
    43. Osmond B., Badger M., Maxwell K. et al.: Too many photons: photorespiration, photoinhibition and photooxidation. - Trends Plant Sci. 2: 119-121, 1997. Go to original source...
    44. Ostrowska A., Porębska G., Sienkiewicz J. et al.: [Properties of soils and plants in the forest environment monitoring.] Pp. 159. Instytut Ochrony Środowiska, Warszawa 2006. [In Polish]
    45. Ouzounidou G., Eleftheriou E., Karataglis S.: Ecophysiological and ultrastructural effects of copper in Thlaspi ochroleucum (Cruciferae). - Can. J. Bot. 70: 947-957, 1992. Go to original source...
    46. Ouzounidou G., Symeonidis L., Babalonas D. et al.: Comparative responses of a copper-tolerant and a coppersensitive population of Minuartia hirsuta to copper toxicity. - C J. Plant Physiol. 144: 109-115, 1994. Go to original source...
    47. Pádua M., Cavaco A.M., Aubert S. et al.: Effects of copper on the photosynthesis of intact chloroplasts: interaction with manganese. - Physiol. Plantarum 138: 301-311, 2010. Go to original source...
    48. Parzych A., Sobisz Z.: The macro- and microelemental content of Pinus sylvestris L. and Pinus nigra J.F. Arn. needles in Cladonio-Pinetum habitat of the Słowiński National Park. - Forest Res. Pap. 73: 295-303, 2012.
    49. Pätsikkä E., Aro E.-M., Tyystjärvi E.: Increase in the quantum yield of photo inhibition contributes to copper toxicity in vivo. - Plant Physiol. 117: 619-627, 1998. Go to original source...
    50. Pätsikkä E., Kairavuo M., Šeršen F. et al.: Excess copper predisposes photosystem IIto photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. - Plant Physiol. 129: 1359-1367, 2002. Go to original source...
    51. Peng H., Wang-Müller Q., Witt T. et al.: Differences in copper accumulation and copper stress between eight populations of Haumaniastrum katangense. - Environ. Exp. Bot. 79: 58-65, 2012. Go to original source...
    52. Pilon M., Abdel-Ghany S., Cohu C.M. et al.: Copper cofactor delivery in plant cells. - Curr. Opin. Plant Biol. 9: 256-263, 2006. Go to original source...
    53. Porcar-Castell A.: A high-resolution portrait of the annual dynamics of photochemical and non-photochemical quenching in needles of Pinus sylvestris. - Physiol. Plantaru 143: 139-153, 2011. Go to original source...
    54. Rintamäki E., Salo R., Lehtonen E. et al.: Regulation of D1 protein-degradation during photoinhibition of photosystem-II in vivo phosphorylation of the D1 protein in various plant groups. - Planta 195: 379-386, 1995. Go to original source...
    55. Rouphael Y., Cardarelli M., Rea E. et al.: Grafting of cucumber as a means to minimize copper toxicity. - Environ. Exp. Bot. 63: 49-58, 2008. Go to original source...
    56. Ruban A.V., Horton P.: The xanthophyll cycle modulates the kinetic of nonphotochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts, and leaves of spinach. - Plant Physiol. 119: 531-542, 1999. Go to original source...
    57. Rut G., Rzepka A., Krupa J.: The effect of hypoxia and posthypoxia on the fluctuations in concentrations of malate and citrate, the activity of malic enzyme, and on the intensity of gas exchange in moss gametophores. - Photosynthetica 48: 79-86, 2010. Go to original source...
    58. Schachtman D.P., Reid R.J., Ayling S.M.: Phosphorus uptake by plants: from soil to cell. - Plant Physiol. 116: 447-453, 1998. Go to original source...
    59. Sch¨<sup>1</sup>tzend¨<sup>1</sup>bel A., Polle A.: Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. - C J. Exp. Bot. 53: 1351-1365, 2002.
    60. Shaw A.K., Ghosh S., Kalaji M.H. et al.: Nano-CuO stress induced modulation of antioxidative defense and photosynthetic performance of Syrian barley (Hordeum vulgare L.). - Environ. Exp. Bot. 102: 37-47, 2014. Go to original source...
    61. Siwek M.: [Plants in the environment contaminated with heavy metals. Part II.Detoxification mechanisms and strategies adaptation of plants to high concentrations of heavy metals.] - Wiad. Bot. 52: 7-23, 2008. [In Polish]
    62. Stolarska A., Wróbel J., Woźniak A. et al.: Influence of copper and zinc in soil on physiological reaction on wheat seedlings. - Ecol. Chem. Eng. 13: 687-693, 2006.
    63. Tukendorf A., Wójcik A.: [Strategy for avoiding stress in plant resistance to heavy metals.] - Wiad. Bot. 39: 33-40, 1995. [In Polish]
    64. Valko M., Morris H., Cronin M.T.D.: Metals, toxicity and oxidative stress. - Curr. Med. Chem. 12: 1161-1208, 2005. Go to original source...
    65. van Kooten O., Snel J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. - Photosynth. Res. 25: 147-150, 1990. Go to original source...
    66. Vinit-Dunand F., Epron D., Alaoui-Sossé B. et al.: Effects of copper on growth and on photosynthesis of mature and expanding leaves in cucumber plants. - Plant Sci. 163: 53-58, 2002. Go to original source...
    67. Vries W., Heij G.J.: Critical loads and critical levels for the environment effects of air pollutants. - In: Heij G.J., Schneider T. (ed.): Final Report of the Dutch Priority Programme on Acidification Research in the Netherlands. Pp. 205-214. Elsevier, Bilthoven 1991. Go to original source...
    68. Wanic T., Lasota J., Błońska E. et al.: [Valorization of soils under the former German timber depot in the forest district Warcino and the IBL forest reference plot, covered by a long-term research program in the forest district Polanów. - In: Dominik J. (ed.): [The Fifth Days of Biodiversity in the Promotional Forest Complex; Forests Środkowopomorskie]. - Pp. 47-53. Ekwita, Gdańsk 2013. [In Polish]
    69. Williams L.E., Mills R.F.: P1B-ATPases - an ancient family of transition metal pumps with diverse functions in plants. - Trends Plant Sci. 10: 491-502, 2005. Go to original source...
    70. Wisniewski L., Dickinson N.M.: Toxicity of copper to Quercus robur (English Oak) seedlings from a copper-rich soil. - Environ. Exp. Bot. 50: 99-107, 2003. Go to original source...
    71. Yilmaz S., Zengin M.: Monitoring environmental pollution in Erzurum by chemical analysis of Scots pine (Pinus sylvestris L.) needles. - Environ. Int. 29: 1041-1047, 2004. Go to original source...
    72. Yruela I., Alfonso M., Barón M. et al.: Copper effect on the protein composition of photosystem II. - Physiol. Plantarum 110: 551-557, 2008.
    73. Yruela I., Alfonso M., de Zarate I.O. et al.: Precise location of the Cu (II)-inhibitory binding site in higher plants and bacterial photosynthetic reaction centres as probed by light-induced absorbance changes. - C J. Biol. Chem. 268: 1684-1689, 1993.
    74. Yruela I., Pueyo J.J., Alonso P.J. et al.: Photoinhibition in photosystem II from higher plants. Effect of copper inhibition. - C J. Biol. Chem. 271: 27408-27415, 1996. Go to original source...
    75. Yruela I.: Copper in plants. - Braz. J. Plant Physiol. 17: 145-146, 2005. Go to original source...
    76. Yruela I.: Copper in plants: acquisition, transport and interactions. - Funct. Plant Biol. 36: 409-430, 2009. Go to original source...

    Return to the content