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

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Photosynthetica

Abstract

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.

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Abbreviations

C i :

substomatal CO2 concentration

Cd:

cadmium

Cd-S:

Cd concentration in shoots

Cd-R:

Cd concentration in roots

Chl:

chlorophyll

CK:

control

DMR:

dry mass of roots

DMS:

dry mass of shoots

F0 :

minimum fluorescence

Fm :

maximum fluorescence

Fv/Fm :

maximal quantum efficiency of PSII

g s :

stomatal conductance to the CO2

LP:

lipid peroxidation

MDA:

malondialdehyde

MSI:

membrane stability index

P N :

net photosynthetic rate

ROS:

reactive oxygen species

TBA:

thiobarbituric acid

TBARS:

thiobarbituric acid reactive substances

TCA:

trichloroacetic acid

TLA:

total leaf area per plant

References

  • Alia, Saradhi P.P.: Proline accumulation under heavy metal stress. — J. Plant Physiol. 138: 554–558, 1991.

    Article  CAS  Google Scholar 

  • Arnon, D.I.: Copper enzymes in isolated chloroplast polyphenoloxidase in Beta vulgaris. — Plant Physiol. 24: 1–15, 1949.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ashraf M., Harris P.J.C.: Potential biochemical indicators of salinity tolerance in plants. — Plant Sci. 166: 3–16, 2004.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bates L.S., Waldran R.P., Teare I.D.: Rapid determination of free proline for water studies. — Plant Soil 39: 205–208, 1973.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Benavides M.P., Gallego S.M., Tomaro M.L.: Cadmium toxicity in plant. — Brazil. J. Plant Physiol. 17: 21–34, 2005.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Clemens S., Palmgren M.G., Krämer U.: A long way ahead: understanding and engineering plant metal accumulation. — Trend. Plant Sci. 7: 309–315, 2002.

    Article  CAS  Google Scholar 

  • Delauney A.J., Verma D.P.S.: Proline biosynthesis and osmoregulation in plants. — Plant J. 4: 215–223, 1993.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hare P.D., Cress W.A.: Metabolic implications of stressinduced proline accumulation in plants. — Plant Growth Regul. 21: 79–102, 1997.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Nriagu J.O.: Global inventory of natural and anthropogenic emissions of trace metals to the atmosphere. — Nature 279: 409–411, 1979.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Potters G., Pasternak T.P., Guisez Y. et al.: Stress-induced morphogenic responses: growing out of trouble? — Trend. Plant Sci. 12: 98–105, 2007.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • Sanità di Toppi L., Gabbrielli R.: Response to cadmium in higher plants. — Environ. Exp. Bot. 41: 105–130, 1999.

    Article  Google Scholar 

  • Sarić M.R.: Theoretical and practical approaches to the genetic specificity of mineral nutrition of plants. — Plant Soil 72: 137–150, 1983.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Sayed O.H.: Chlorophyll fluorescence as a tool in cereal crop research. — Photosynthetica 41: 321–330, 2003.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. College of Agriculture, Department of Agronomy and Plant Breeding, Isfahan University of Technology, Isfahan, 84156-83111, Iran

    L. Moradi & P. Ehsanzadeh

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  1. L. Moradi
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  2. P. Ehsanzadeh
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Correspondence to P. Ehsanzadeh.

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Acknowledgements: The authors are indebted to the Isfahan University of Technology for the financial aid.

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Moradi, L., Ehsanzadeh, P. Effects of Cd on photosynthesis and growth of safflower (Carthamus tinctorius L.) genotypes. Photosynthetica 53, 506–518 (2015). https://doi.org/10.1007/s11099-015-0150-1

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  • DOI: https://doi.org/10.1007/s11099-015-0150-1

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