Photosynthetica 2018, 56(4):1249-1258 | DOI: 10.1007/s11099-018-0827-3

Zinc accumulation, photosynthetic gas exchange, and chlorophyll a fluorescence in Zn-stressed Miscanthus × giganteus plants

G. Andrejić1,3, G. Gajić2, M. Prica1, Ž. Dželetović3, T. Rakić1,*
1 Department of Plant Ecology and Phytogeography, Faculty of Biology, University of Belgrade, Belgrade, Serbia
2 Department of Ecology, Institute for Biological Research "Siniša Stanković", University of Belgrade, Belgrade, Serbia
3 Institute for the Application of Nuclear Energy, University of Belgrade, Zemun, Serbia

Accumulation and distribution of zinc within Miscanthus × giganteus plants grown on elevated Zn concentrations and their photosynthetic performance were investigated. High concentrations of Zn in soils caused an increase of its concentrations in all plant organs. The bioconcentration factor, bioaccumulation factor, and translocation factor were lower than one indicating that M. × giganteus is an excluder plant species. Excessive Zn induced visible leaf damage, i.e. chlorosis and necrosis, only in the oldest leaves, pointing to Zn accumulation. Elevated amounts of Zn in leaves significantly lowered the photosynthetic rate, transpiration rate, stomatal conductance, intercellular CO2 concentrations, parameters of chlorophyll a fluorescence, and chlorophyll b content. Despite Zn excess in leaves, there was no severe reduction in the maximal quantum yield of PSII photochemistry, indicating a high photosynthetic capacity, high tolerance to elevated Zn concetrations, and ability of M. × giganteus to grow on Zn-contaminated soils.

Keywords: pigments; photosynthesis; phytoremediation; Zn tolerance

Received: August 31, 2017; Accepted: January 10, 2018; Prepublished online: December 1, 2018; Published: November 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Andrejić, G., Gajić, G., Prica, M., Dželetović, Ž., & Rakić, T. (2018). Zinc accumulation, photosynthetic gas exchange, and chlorophyll a fluorescence in Zn-stressed Miscanthus × giganteus plants. Photosynthetica56(4), 1249-1258. doi: 10.1007/s11099-018-0827-3.
Download citation

References

  1. Arnon D.I.: Copper enzymes in isolated chloroplasts: polyphenoloxidases in Beta vulgaris.-Plant Physiol. 24: 1-15, 1949. Go to original source...
  2. Baker A.J.M.: Accumulators and excluders-strategies in the response of plants to heavy metals. - J. Plant Nutr. 3: 643-654, 1981. Go to original source...
  3. Baker N.R., Rosenqvist E.: Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities.-J. Exp. Bot. 55: 1607-1621, 2004. Go to original source...
  4. Bang J., Kamala-Kannan S., Lee K.J. et al.: Phytoremediation of heavy metals in contaminated water and soil using Miscanthus sp. Goedae-Uksae 1.-Int. J. Phytoremediat. 17: 515-20, 2015. Go to original source...
  5. Beale C.V., Bint D.A., Long S.P.: Leaf photosynthesis in the C4-grass Miscanthus x giganteus, growing in the cool temperate climate of southern England.-J. Exp. Bot. 47: 267-273, 1996. Go to original source...
  6. Björkman O., Demmig B.: Photon yield of O2 evolution and chlorophyll fluorescence at 77k among vascular plants of diverse origins.-Planta 170: 489-504, 1987. Go to original source...
  7. Bonnet M., Camares O., Veisseire P.: Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium prenne L. cv. Apollo).-J. Exp. Bot. 51: 945-953, 2000.
  8. Bremner J.M.: Nitrogen total.-In: Sparks D.L. (ed.): Methods of Soil Analysis, Part 3: Chemical Methods. Pp. 1085-1122. SSSA Book Series 5. Soil Science Society of America, Madison 1996.
  9. Clifton-Brown J.C., Lewandowski I., Bangerth F. et al.: Comparative responses to water stress in stay-green, rapid-and slow senecing genotypes of the biomass crop, Miscanthus.‒New Phytol. 154: 335-345, 2002. Go to original source...
  10. Dhir B., Sharmila P., Pardha Saradhi P.P.: Photosynthetic performance of Salvinia natans exposed to chromium and zinc rich wastewater.-Braz. J. Plant Physiol. 20: 61-70, 2008.
  11. Dželetović Ž., Mihailović N., Živanović I.: Prospects of using bioenergy crop Miscanthus × giganteus in Serbia.-In: Méndez-Vilas A. (ed.): Materials and Processes for Energy: Communicating Current Research and Technological Developments. Pp. 360-370. Formatex Research Center, Badajoz 2013.
  12. Egner H., Riehm H., Domingo W.R.: [Studies on the chemical soil analysis as a basis for the assessment of nutrient status of the soil, II: chemical extractions metods to phosphorus and potassium determination.].-Kungliga Lantbrukshügskolans Annaler 26: 199-215, 1960. [In German]
  13. Eriksson J.E.: Concentrations of 61 Trace Elements in Sewage Sludge, Farmyard Manure, Mineral Fertilizers, Precipitation and in Oil and Crops. Pp. 69. Swedish EPA, Stockholm 2001.
  14. FAO (Food and Agriculture Organization): Guidelines: Land Evaluation for Rainfed Agriculture. Soils Bulletin No 52. Pp. 237. FAO, Rome 1983.
  15. Farage P.K., Blowers D., Long S.P. et al.: Low growth temperatures modify the efficiency of light use by photosystem II for CO2 assimilation in leaves of two chilling-tolerant C-4 species, Cyperus longus L. and Miscanthus×giganteus.-Plant Cell Environ. 29: 720-728, 2006. Go to original source...
  16. Fernando A.L., Oliviera J.F.S.: Phytoremediation by Miscanthus x giganteus of soils contaminated with heavy metals.‒In: Gaballah I. (ed.): REWAS' 04-Global Symposium on Recycling, Waste Treatment and Clean Technology. Pp. 2419-2427. Minerals, Metals & Materials Society, Madrid 2004.
  17. Figala J., Vranová V., Rejšek K. et al.: Giant Miscanthus (Miscanthus × giganteus Greef et Deu.)‒a promising plant for soil remediation: a minireview.‒Acta Univ. Agric. Silvic. Mendelianae Brun. 63: 2241-2246, 2015. Go to original source...
  18. Firmin S., Labidi S., Fontaine J. et al.: Arbuscular mycorrhizal fungal inoculation protects Miscanthus x giganteus against trace element toxicity in a highly metal-contaminated site.-Sci. Total Environ. 527-528: 91-99, 2015. Go to original source...
  19. Fonteyne S., Lootens P., Muylle H. et al.: Chilling tolerance and early vigour-related characteristics evaluated in two Miscanthus genotypes.‒Photosynthetica 54: 295-306, 2016. Go to original source...
  20. Gajić G., Djurdjević L., Kostić O. et al.: Assessment of phytoremediation potential and an adaptive response of Festuca rubra L., sown on fly ash deposits: Native grass has a pivotal role in ecorestoration management.‒Ecol. Eng. 93: 250-261, 2016.
  21. Głowacka K., Jørgensen U., Kjeldsen J.B. et al.: Can the exceptional chilling tolerance of C4 photosynthesis found in Miscanthus x giganteus be exceeded? Screening of a novel Miscanthus Japanese germplasm collection.-Ann. Bot.-London 115: 981-990, 2015.
  22. Guo H., Hong C., Chen X. et al.: Different growth and physiological responses to cadmium of the three Miscanthus species.‒PLoS ONE 11: e0153475, 2016. Go to original source...
  23. Herselman J.E., Steyn C.E., Fey M.V.: Baseline concentration of Cd, Co, Cr, Cu, Pb, Ni and Zn in surface soils of South Africa.-S. Afr. J. Sci. 101: 509-512, 2005.
  24. Hiscox J.D., Israelstam G.F.: A method for the extraction of chlorophyll from leaf tissue without maceration.-Can. J. Bot. 57: 1332-1334, 1979.
  25. Ings J., Mur L.A.J., Robson R.R.H. et al.: Physiological and growth responses to water deficit in the bioenergy crop Miscanthus x giganteus.-Front. Plant Sci. 4: 468, 2013.
  26. Jiao X., Kørup K., Andersen M.N. et al.: Low-temperature leaf photosynthesis of a Miscanthus germplasm collection correlates positively to shoot growth rate and specific leaf area.‒Ann. Bot.-London 117: 1229-1239, 2016. Go to original source...
  27. Jiao X., Kørup K., Andersen M.N. et al.: Can miscanthus C4 photosynthesis compete with festulolium C3 photosynthesis in a temperate climate?‒GCB Bioenergy 9: 18-30, 2017. Go to original source...
  28. Kabata-Pendias A.: Trace Elements in Soils and Plants. 4th ed. Pp. 505. Taylor and Francis, Boca Raton 2011. Go to original source...
  29. Kloke A., Sauerbeck D.R., Vetter H.: The contamination of plants and soils with heavy metals and the transport of metals in terrestrial food chains.-In: Nriagu J.O., Andreae M.O. (ed.): Changing Metal Cycles and Human Health. Report of the Dahlem Workshop on Changing Metal Cycles and Human Health Berlin. Pp. 446. Springer-Verlag GmbH, Berlin 1983.
  30. Korzeniowska J., Stanislawska-Glubiak E.: Phytoremediation potential of Miscanthus x giganteus and Spartina pectinata in soil contaminated with heavy metals.‒Environ. Sci. Polutt. R. 22: 11648-11657, 2015. Go to original source...
  31. Kocoń A., Jurga B.: The evaluation of growth and phytoextraction potential of Miscanthus x giganteus and Sida hermafrodita on soil contaminated simultaneously with Cd, Cu, Ni, Pb, and Zn.‒Environ. Sci. Polutt. R. 24: 4990-5000, 2017.
  32. Lambers H., Chapin F.S., Pons T.L.: Plant Physiological Ecology. Pp. 540. Springer-Verlag, New York 1998. Go to original source...
  33. Li C., Xiao B., Wang Q.H. et al.: Phytoremediation of Zn-and Cr-contaminated soil using two promising energy grasses.‒Water Air Soil Pollut. 225: 2027, 2014. Go to original source...
  34. Lu Y.: The occurrence of a thylakoid-localized small zinc finger protein in land plants.‒Plant Signal. Behav. 6: 1881-1885, 2011. Go to original source...
  35. Ma J.-Y., Sun W., Koteyeva N.K. et al.: Influence of light and nitrogen on the photosynthetic efficiency in the C4 plant Miscanthus x giganteus.‒Photosynth. Res. 131: 1-13, 2017. Go to original source...
  36. Macnicol R.D., Beckett P.H.T.: Critical tissue concentrations of potentially toxic elements.‒Plant Soil 85: 107-129, 1985. Go to original source...
  37. Marschner H.: Mineral Nutrition of Higher Plants, 2nd Ed. Pp. 889. Academic Press Limited, London 1995.
  38. Martens J., Smolders E. Zinc.‒In: Alloway B.J. (ed.): Heavy Metals in Soils‒Trace Metals and Metalloids in Soils and their Bioavailability. Series: Environmental Pollution 22. Pp. 465-493. Springer, Dordrecht 2013. Go to original source...
  39. McCalmont J.P., Hastings A., McNamara N.P. et al.: Environmental costs and benefits of growing Miscanthus for bioenergy in the UK.-GCB Bioenergy 9: 489-507, 2017. Go to original source...
  40. Nadgórska-Socha A., Ptasiński B., Kita A.: Heavy metal bioaccumulation and antioxidative responses in Cardaminopsis arenosa and Plantago lanceolata leaves from metalliferous and non-metalliferous sites: a field study.‒Ecotoxicology 22: 1422-1434, 2013. Go to original source...
  41. Naidu S.L., Long S.P.: Potential mechanisms of low-temperature tolerance of C4 photosynthesis in Miscanthus × giganteus: an in vivo analysis.-Planta 220: 145-155, 2004.
  42. Nsanganwimana F., Pourrut B., Mench M. et al.: Suitability of Miscanthus species for managing inorganic and organic contaminated land and restoring ecosystem services. A review.‒J. Environ. Manage. 143: 123-134, 2014.
  43. Pandey V.C., Bajpai O., Singh N.: Energy crops in sustainable phytoremediation.‒Renew. Sust. Energ. Rev. 54: 58-73, 2016. Go to original source...
  44. Pansu M., Gautheyroy J.: Handbook of Soil Analysis. Mineralogical, Organic and Inorganic Methods. Pp. 993. Springer, Berlin 2006.
  45. Pavel P.B., Puschenreiter M., Wenzel W.W. et al.: Aided phytostabilization using Miscanthus sinensis × giganteus on heavy metal-contaminated soils.‒Sci. Total Environ. 479-480: 125-131, 2014. Go to original source...
  46. Pelfrêne A, Kleckerová A, Pourrut B. et al.: Effect of Miscanthus cultivation on metal fractionation and human bioaccessibility in metal-contaminated soils: comparison between greenhouse and field experiments.‒Environ. Sci. Pollut. R. Int. 22: 3043-54, 2015. Go to original source...
  47. Pidlisnyuk V., Stefanovska T., Lewis E.E. et al.: Miscanthus as a productive biofuel crop for phytoremediation.‒Crit. Rev. Plant Sci. 33: 1-19, 2014. Go to original source...
  48. Pilgrim W., Hughes R.N.: Lead, cadmium, arsenic and zinc in the ecosystem surrounding a lead smelter.-Environ. Monit. Assess. 32: 1-20, 1994. Go to original source...
  49. Pogrzeba M., Rusinowski S., Sitko K. et al.: Relationships between soil parameters and physiological status of Miscathus x giganteus cultivated on soil contaminated with trace elements under NPK fertilization vs. microbial inoculation.-Environ. Pollut. 225: 163-174, 2017. Go to original source...
  50. Prasad M.N.V.: Heavy Metal Stress in Plants‒From Biomolecules to Ecosystems. Pp. 462. Springer-Verlag, Berlin-Heidelberg 2004.
  51. Rutkowska B., Szulc W., Bomze K.: Plant availability of zinc in differentiated soil conditions.‒Fresen. Environ. Bull. 22: 2542-2546, 2013.
  52. Sagardoy R., Morales F., López-Millán A.F. et al..: Effects of zinc toxicity in sugar beet (Beta vulgaris L.) plants grown in hydroponics.‒Plant Biol. 11: 339-350, 2009. Go to original source...
  53. Sagardoy R., Vázquez S., Florez-Sarasa I. et al.: Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc.‒New Phytol. 187: 145-158, 2010. Go to original source...
  54. Sinclair S.A., Krämer U.: The zinc homeostasis network of land plants.‒Biochim Biophys Acta. 1823: 1553-1567, 2012.
  55. Sun Q., Ye Z.H., Wang X.R. et al.: Increase of glutathione in mine population of Sedum alfredii: a Zn hyperaccumulator and Pb accumulator.‒Phytochemistry 66: 2549-3256, 2005. Go to original source...
  56. Sun W., Ubierna N., Ma J.-Y. et al.: The influence of light quality on C4 photosynthesis under steady-state conditions in Zea mays and Miscanthus × giganteus: changes in rates of photosynthesis but not the efficiency of the CO2 concentrating mechanism.‒Plant Cell Environ. 35: 982-993, 2012. Go to original source...
  57. Sun W., Ubierna N., Ma J.-Y. et al.: The coordination of C4 photosynthesis and the CO2-concentrating mechanism in maize and Miscanthus × giganteus in response to transient changes in light quality.‒Plant Physiol. 164: 1283-1292, 2014. Go to original source...
  58. Szalontai B., Horváth L., Debreczeny M. et al.: Molecular rearrangements of thylakoids after heavy metal poisoning, as seen by Fourier transform infrared (FTIR) and electron spin resonance (ESR) spectroscopy.‒Photosynth Res. 61: 241-252, 1999. Go to original source...
  59. Takeda A., Kimura K., Yamasaki S.I.: Analysis of 57 elements in Japanese soils, with special reference to soil group, and agricultural use.-Geoderma 119: 291-307, 2004. Go to original source...
  60. Técher D., Laval-Gilly P., Bennasroune A. et al.: An appraisal of Miscanthus x giganteus cultivation for fly ash revegetation and soil restoration.-Ind. Crop. Prod. 36: 427-433, 2012. Go to original source...
  61. Tsalandzono N.G., Omokolo N.D., Tita A.M.: Effect of Fe2+, Mn2+, Zn2+, and Pb2+ on H+/K+ fluxes in excised Pistia stratiotes roots.-Biol. Plantarum 36: 591-597, 1994.
  62. Tsonev T., Lidon F.J.C.: Zinc in plants‒An overview.‒Emir. J. Food Agr. 24: 322-333, 2012.
  63. Tjurin I.V.: Agrochemical Methods of Soil Analysis. Pp. 75-102. Nauka, Moscow 1965.
  64. Ubierna N., Sun W., Kramer D.M. et al.: The efficiency of C4 photosynthesis under low light conditions in Zea mays, Miscanthus × giganteus and Flaveria bidentis.‒Plant Cell Environ. 36: 365-381, 2013. Go to original source...
  65. USEPA Method 3051: Microwave assisted acid digestion of sediments, sludges and oils.‒In: Test Methods for Evaluating Solid Waste, SW-846. Environmental Protection Agency, Washington, DC 1998.
  66. USEPA Method 3052: Microwave assisted acid digestion of siliceous and organically based matrices.‒In: Test Methods for Evaluating Solid Waste, SW-846. Environmental Protection Agency, Washington, DC 1996.
  67. Vaillant N., Monnet F., Hitmi A. et al.: Comparative study of responses in four Datura species to a zinc stress.-Chemosphere 59: 1005-1013, 2005. Go to original source...
  68. van Assche F., Clijsters H.: Inhibition of photosynthesis in Phaseoulus vugaris by treatment with toxic concentration of zinc: effect on ribulose-1,5-bisphosphate carboxylase/oxygenase.‒J. Plant Physiol. 125: 355-360, 1986. Go to original source...
  69. Wanat N., Austruy A., Joussein E. et al.: Potential of Miscanthus x giganteus grown on highly contaminated technosols.‒J. Geochem. Explor. 126-127: 78-84, 2013. Go to original source...
  70. Wellburn A.R.: The spectral determination of chlorophylls a and b, as well as total carotenoids using various solvents with spectrophotometers of different resolution.-J. Plant Physiol. 144: 307-313, 1994. Go to original source...
  71. Yang H.M., Zhang X.Y., Wang G.X.: Effects of heavy metals on stomatal movements in broad bean leaves.-Russ. J. Plant Physl+ 51: 464-468, 2004.
  72. Zub H.W., Brancourt-Hulmel M.: Agronomic and physiological performances of different species of Miscanthus, a major energy crop. A review.-Agron. Sustain. Dev. 30: 201-214, 2010. Go to original source...