, Volume 53, Issue 4, pp 506–518 | Cite as

Effects of Cd on photosynthesis and growth of safflower (Carthamus tinctorius L.) genotypes

  • L. Moradi
  • P. Ehsanzadeh
Original Papers


Heavy metals such as cadmium (Cd) may affect different physiological functions in plants. We carried out a hydroponic experiment under greenhouse conditions in order to evaluate the effect of Cd on photosynthetic and physiological parameters of safflower. The responses of six safflower genotypes (Nebraska-10, 2811, Kouseh, S149, C111, and K12) to four concentrations of CdCl2 (0, 1.5, 3, and 4.5 mg L−1) were examined. Mean shoot and root dry masses of safflower plants were reduced by nearly 57% after the treatment by 4.5 mg(CdCl2) L−1. Contrary to the mean proline content, which increased by 121%, the mean total leaf area per plant, net photosynthetic rate, stomatal conductance to the CO2, leaf chlorophyll a, b, and (a+b), carotenoid content, and quantum efficiency of PSII decreased by 84.4, 50.5, 50.0, 31.6, 32.2, 31.8, 32.9, and 11.2%, respectively, at the presence of 4.5 mg(CdCl2) L−1. The mean Cd concentration in shoots and roots of safflower genotypes exhibited 52- and 157-fold increase, respectively, due to the addition of 4.5 mg(CdCl2) L−1 to the growing media. The mean malondialdehyde content was enhanced by 110% with the increasing CdCl2 concentration, indicating the occurrence of a considerable lipid peroxidation in the plant tissues. Even though the membrane stability index was adversely affected by the application of 1.5 mg(CdCl2) L−1, the decrease ranged from 45 to 62% when plants were treated with 4.5 mg(CdCl2) L−1. Genotype Nebraska-10 seemed to be different from the remaining genotypes in response to the 4.5 mg(CdCl2) L−1; its net photosynthetic rate tended to be the greatest and the Cd concentration in shoots and roots was the lowest among genotypes studied. This study proved Cd-induced decline in growth, photosynthesis, and physiological functions of safflower.

Additional key words

cadmium chlorophyll gas exchange lipid peroxidation proline 



substomatal CO2 concentration




Cd concentration in shoots


Cd concentration in roots






dry mass of roots


dry mass of shoots


minimum fluorescence


maximum fluorescence


maximal quantum efficiency of PSII


stomatal conductance to the CO2


lipid peroxidation




membrane stability index


net photosynthetic rate


reactive oxygen species


thiobarbituric acid


thiobarbituric acid reactive substances


trichloroacetic acid


total leaf area per plant


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alia, Saradhi P.P.: Proline accumulation under heavy metal stress. — J. Plant Physiol. 138: 554–558, 1991.CrossRefGoogle Scholar
  2. Arnon, D.I.: Copper enzymes in isolated chloroplast polyphenoloxidase in Beta vulgaris. — Plant Physiol. 24: 1–15, 1949.PubMedCentralCrossRefPubMedGoogle Scholar
  3. Ashraf M., Harris P.J.C.: Potential biochemical indicators of salinity tolerance in plants. — Plant Sci. 166: 3–16, 2004.CrossRefGoogle Scholar
  4. Bajji M., Kinet J.M., Lutts S.: The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. — Plant Growth Regul. 36: 61–70, 2002.CrossRefGoogle Scholar
  5. Barceló J., Poschenrieder Ch., Andreu I., Gunsé B.: Cadmiuminduced decrease of water stress resistance in bush bean plants (Phaseolus vulgaris L. cv. Contender) I. Effects of Cd on water potential, relative water content, and cell wall elasticity. — J. Plant Physiol. 125: 17–25, 1986.CrossRefGoogle Scholar
  6. Baryla A., Carrier P., Franck F. et al.: 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.CrossRefPubMedGoogle Scholar
  7. Bates L.S., Waldran R.P., Teare I.D.: Rapid determination of free proline for water studies. — Plant Soil 39: 205–208, 1973.CrossRefGoogle Scholar
  8. Bazrafshan A.H., Ehsanzadeh P.: Growth, photosynthesis and ion balance of sesame (Sesamum indicum L.) genotypes in response to NaCl concentration in hydroponic solutions. — Photosynthetica 52: 134–147, 2014.CrossRefGoogle Scholar
  9. Benavides M.P., Gallego S.M., Tomaro M.L.: Cadmium toxicity in plant. — Brazil. J. Plant Physiol. 17: 21–34, 2005.Google Scholar
  10. Blum W.H.: Cadmium uptake by higher plants. — In: Iskandar I.K., Hardy S.E., Chang A.C., Pierzynski G.M. (ed.). Proceedings of Extended Abstracts from the Fourth International Conference on the Biochemistry of Trace Elements. Pp. 109–110. University of California, Berkeley 1997.Google Scholar
  11. Cakmak I., Welch R.M., Hart J. et al.: Uptake and retranslocation of leaf-applied cadmium (109Cd) in diploid, tetraploid and hexaploid wheats. — J. Exp. Bot. 51: 221–226, 2000.CrossRefPubMedGoogle Scholar
  12. Chaney R.L.: Metal speciation and interactions among elements affect trace element transfer in agricultural and environmental food-chains. — In: Kramer J.R., Allen H.E. (ed.): Metal Speciation Theory, Analysis and Application. Pp. 219–260, Lewis Publishers, Chelsea, 1998.Google Scholar
  13. Chen S.L., Kao C. H.: Cd induced changes in proline level and peroxydase activity in roots of rice seedlings. — Plant Growth Regul. 17: 67–71, 1995.Google Scholar
  14. Cherif J., Derbel N., Nakkach M. et al.: Spectroscopic studies of photosynthetic responses of tomato plants to the interaction of zinc and cadmium toxicity. — J. Photoch. Photobio. B 111: 9–16, 2012.CrossRefGoogle Scholar
  15. Clemens S., Palmgren M.G., Krämer U.: A long way ahead: understanding and engineering plant metal accumulation. — Trend. Plant Sci. 7: 309–315, 2002.CrossRefGoogle Scholar
  16. Delauney A.J., Verma D.P.S.: Proline biosynthesis and osmoregulation in plants. — Plant J. 4: 215–223, 1993.CrossRefGoogle Scholar
  17. Demiral T., Türkan I.: Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. — Environ. Exp. Bot. 53: 247–257, 2005.CrossRefGoogle Scholar
  18. Ekvall L., Greger M.: Effects of environmental biomassproducing factors on Cd uptake in two Swedish ecotypes of Pinus sylvestris. — Environ. Pollut. 121: 401–411, 2003.CrossRefPubMedGoogle Scholar
  19. Frank A.: Automated wet ashing and multi-metal determination in biological materials by atomic absorption spectrometry. — J. Anal. Chemist. 31: 101–102, 1976.Google Scholar
  20. Ghnaya T., Nouairi I., Slama I. et al.: Cadmium effects on growth and mineral nutrition of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum. — J. Plant Physiol. 162: 1133–1140, 2005.CrossRefPubMedGoogle Scholar
  21. Gilbert G.A., Gadush M.V., Wilson C., Madore M.A.: Amino acid accumulation in sink and source tissues of Coleus blumei Benth. During salinity stress. — J. Exp. Bot. 49: 107–114, 1998.CrossRefGoogle Scholar
  22. Greger M., Löfstedt M.: Comparison of uptake and distribution of cadmium in different cultivars of bread and durum wheat. — Crop Sci. 44: 501–507, 2004.CrossRefGoogle Scholar
  23. Guo T.R., Zhang G.P., Zhang Y. H.: Physiological changes in barley plants under combined toxicity of aluminum, copper and cadmium. — Colloid. Surface. B 57: 182–188, 2007.CrossRefGoogle Scholar
  24. Hare P.D., Cress W.A.: Metabolic implications of stressinduced proline accumulation in plants. — Plant Growth Regul. 21: 79–102, 1997.CrossRefGoogle Scholar
  25. Iqbal N., Masood A., Nazar R. et al.: Photosynthesis, growth and antioxidant metabolism in mustard (Brassica juncea L.) cultivars differing in cadmium tolerance. — Agric. Sci. China 9: 519–527, 2010.CrossRefGoogle Scholar
  26. Johnson C.M.A., Stout P.R., Broyer T.C., Carlton A.B.: Comparative chlorine requirements of different plants species. — Plant Soil 8: 337–353, 1957.CrossRefGoogle Scholar
  27. Judy B.M., Lower W.R., Miles C.D. et al.: Chlorophyll fluorescence of a higher plant as an assay for toxicity assessment of soil and water. — In: Wang W., Gorsuch J.W., Lower W.L. (ed.): Plants for Toxicity Assessment. Pp. 308–318. American Society for Testing and Materials, Philadelphia 1990.CrossRefGoogle Scholar
  28. Katsuhara M., Otsuka T., Ezaki B.: Salt stress-induced lipid peroxidation is reduced by glutathione S-transferase, but this reduction of lipid peroxides is not enough for a recovery of root growth in Arabidopsis. — Plant Sci. 169: 369–373, 2005.CrossRefGoogle Scholar
  29. Köleli N., Eker S., Cakmak I.: Effect of zinc fertilization on cadmium toxicity in durum and bread wheat grown in zincdeficient soil. — Environ. Pollut. 131: 453–459, 2004.CrossRefPubMedGoogle Scholar
  30. Krantev A., Yordanova R., Janda T. et al.: Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. — J. Plant Physiol. 165: 920–931, 2008.CrossRefPubMedGoogle Scholar
  31. Krevešan S., Kiršek S., Kandrač J. et al.: Dynamics of cadmium distribution in the intercellular space and inside cells in soybean roots, stems and leaves. — Biol. Plantarum 46: 85–88, 2003.CrossRefGoogle Scholar
  32. Larsson E.H., Bornmann J.F., Asp H.: Influence of UV-B radiation and Cd2+ on chlorophyll fluorescence, growth and nutrient content in Brassica napus. — J. Exp. Bot. 49: 1031–1039, 1998.CrossRefGoogle Scholar
  33. Laspina N.V., Groppa M.D., Tomaro M.L., Benavides M.P.: Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. — Plant Sci. 169: 323–330, 2005.CrossRefGoogle Scholar
  34. Liao B., Liu H., Zeng Q. et al.: Complex toxic effects of Cd2+, Zn2+, and acid rain on growth of kidney bean (Phaseolus vulgaris L). — Environ. Int. 31: 891–895, 2005.CrossRefPubMedGoogle Scholar
  35. Lichtenthaler H.K., Wellburn A.R.: Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. — Biochem. Soc. Trans. 11: 591–592, 1983.CrossRefGoogle Scholar
  36. Liu J., Qian M., Cai G. et al.: Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain. — J. Hazard. Mater. 143: 443–447, 2007.CrossRefPubMedGoogle Scholar
  37. Nagajyoti P.C., Lee K.D., Sreekanth T.V.M.: Heavy metals, occurrence and toxicity for plants: a review. — Environ. Chem. Lett. 8: 199–216, 2010.CrossRefGoogle Scholar
  38. Nasir Khan M., Siddiqui M.H., Mohammad F. et al.: Salinity induced changes in growth, enzyme activities, photosynthesis, proline accumulation and yield in linseed genotypes. — World J. Agric. Sci. 3: 685–695, 2007.Google Scholar
  39. Nedjimi B., Daoud Y.: Cadmium accumulation in Atriplex halimus subsp. schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. — Flora 204: 316–324, 2009.CrossRefGoogle Scholar
  40. Nriagu J.O.: Global inventory of natural and anthropogenic emissions of trace metals to the atmosphere. — Nature 279: 409–411, 1979.CrossRefPubMedGoogle Scholar
  41. Österås A.H., Ekvall L., Greger M.: Sensitivity to and accumulation of Cd in Betula pendula, Picea abies and Pinus sylvestris seedlings from different regions in Sweden. — Can. J. Bot. 78: 1440–1449, 2000.Google Scholar
  42. Poschenrieder C., Gunsé B., Barceló J.: Influence of cadmium on water relations, stomatal resistance, and abscisic acid content in expanding bean leaves. — Plant Physiol. 90: 1365–1371, 1989.PubMedCentralCrossRefPubMedGoogle Scholar
  43. Potters G., Pasternak T.P., Guisez Y. et al.: Stress-induced morphogenic responses: growing out of trouble? — Trend. Plant Sci. 12: 98–105, 2007.CrossRefGoogle Scholar
  44. Potters G., Pasternak T.P., Guisez Y. et al.: Different stresses, similar morphogenic responses: integrating a plethora of pathways. — Plant Cell Environ. 32: 158–169, 2009.CrossRefPubMedGoogle Scholar
  45. Pourghasemian N., Ehsanzadeh P., Greger M.: Genotypic variation in safflower (Carthamus spp.) cadmium accumulation and tolerance affected by temperature and cadmium levels. — Environ. Exp. Bot. 87: 218–226, 2013.CrossRefGoogle Scholar
  46. Sabzalian M.R., Saeidi G., Mirlohi A.: Oil content and fatty acid composition in seeds of three safflower species. — J. Am. Oil Chem. Soc. 85: 717–721, 2008.CrossRefGoogle Scholar
  47. Saeidi G., Rickauer M., Gentzbittel L.: Tolerance for cadmium pollution in a core-collection of the model legume, Medicago truncatula L. at seedling stage. — Aust. J. Crop Sci. 6: 641–648, 2012.Google Scholar
  48. Samani Majd S., Taebi A., Afyuni M.: Lead and cadmium distribution in urban roadside soils of Isfahan, Iran. — J. Env. Studies 33: 1–10, 2007.Google Scholar
  49. Sanità di Toppi L., Gabbrielli R.: Response to cadmium in higher plants. — Environ. Exp. Bot. 41: 105–130, 1999.CrossRefGoogle Scholar
  50. Sarić M.R.: Theoretical and practical approaches to the genetic specificity of mineral nutrition of plants. — Plant Soil 72: 137–150, 1983.CrossRefGoogle Scholar
  51. Sayyad G., Afyuni M., Mousavi S. F. et al.: Transport of Cd, Cu, Pb and Zn in a calcareous soil under wheat and safflower cultivation-a column study. — Chemosphere 154: 311–320, 2010.Google Scholar
  52. Sayed O.H.: Chlorophyll fluorescence as a tool in cereal crop research. — Photosynthetica 41: 321–330, 2003.CrossRefGoogle Scholar
  53. Seemann J.R., Critchley C.: Effects of salt stress on the growth, ion content, stomatal behaviour and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. — Planta 164: 151–162, 1985.CrossRefPubMedGoogle Scholar
  54. Shevyakova N.I., Netronina I.A., Aronova E.E., Kuznetsov V.V.: Compartmentation of cadmium and iron in Mesembryanthemum crystallinum plants during the adaptation to cadmium stress. — Russ. J. Plant Physl+ 50: 678–685, 2003.CrossRefGoogle Scholar
  55. Shi G., Liu C., Cai O. et al.: Cadmium accumulation and tolerance of two safflower cultivars in relation to photosynthesis and antioxidative enzymes. — Bull. Environ Contam. Toxic. 85: 256–263, 2010.CrossRefGoogle Scholar
  56. Singh S., Eapen S., D’souza S.F.: Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. — Chemosphere 62: 233–246, 2006.CrossRefPubMedGoogle Scholar
  57. Son K.H., Kim D.Y., Koo N. et al.: Detoxification through phytochelatin synthesis in Oenothera odorata exposed to Cd solutions. — Environ. Exp. Bot. 75: 9–15, 2012.CrossRefGoogle Scholar
  58. Tran T. A., Popova L.P.: Functions and toxicity of cadmium in plants: recent advances and future prospects. — Turk. J. Bot. 37: 1–13, 2013.Google Scholar
  59. Vassilev A., Berova M., Stoeva N., Zlatev Z.: Chronic Cd toxicity of bean plants can be partially reduced by supply of ammonium sulphate. — J. Cent. Eur. Agric. 6: 389–396, 2005.Google Scholar
  60. Xiong Z.T., Peng Y.H.: Response of pollen germination and tube growth to cadmium with special reference to low concentration exposure. — Ecotoxicol. Environ. Safety 48: 51–55, 2001.CrossRefPubMedGoogle Scholar
  61. Zribi L., Fatma G., Fatma R. et al.: Application of chlorophyll fluorescence for the diagnosis of salt stress in tomato Solanum lycopersicum (variety Rio Grande). — Sci. Hortic.-Amsterdam 120: 367–372, 2009.CrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2015

Authors and Affiliations

  1. 1.College of Agriculture, Department of Agronomy and Plant BreedingIsfahan University of TechnologyIsfahanIran

Personalised recommendations