Photosynthesis Research

, Volume 125, Issue 1–2, pp 291–303 | Cite as

Cadmium accumulation in chloroplasts and its impact on chloroplastic processes in barley and maize

  • Eugene A. Lysenko
  • Alexander A. Klaus
  • Natallia L. Pshybytko
  • Victor V. Kusnetsov
Regular Paper


Data on cadmium accumulation in chloroplasts of terrestrial plants are scarce and contradictory. We introduced CdSO4 in hydroponic media to the final concentrations 80 and 250 μM and studied the accumulation of Cd in chloroplasts of Hordeum vulgare and Zea mays. Barley accumulated more Cd in the chloroplasts as compared to maize, whereas in the leaves cadmium accumulation was higher in maize. The cadmium content in the chloroplasts of two species varied from 49 to 171 ng Cd/mg chlorophyll, which corresponds to one Cd atom per 728–2,540 chlorophyll molecules. Therefore, Mg2+ can be substituted by Cd2+ in a negligible amount of antenna chlorophylls only. The percentage of chloroplastic cadmium can be estimated as 0.21–1.32 % of all the Cd in a leaf. Photochemistry (Fv/Fm, ΦPSII, qP) was not influenced by Cd. Non-photochemical quenching of chlorophyll-excited state (NPQ) was greatly reduced in barley but not in maize. The decrease in NPQ was due to its fast relaxing component; the slow relaxing component rose slightly. In chloroplasts, Cd did not affect mRNA levels, but content of some photosynthetic proteins was reduced: slightly in the leaves of barley and heavily in the leaves of maize. In all analyzed C3-species, the effect of Cd on the content of photosynthetic proteins was mild or absent. This is most likely the first evidence of severe reduction of photosynthetic proteins in leaves of a Cd-treated C4-plant.


Cadmium Chloroplasts mRNA Proteins Barley Maize Photosystem II activity 


BEP clade

Main branch of Poaceae family that includes subfamilies Bambusoideae, Ehrhatoideae, Pooideae






Coefficient of electron-transport rate


Dry weight


Minimum Chl a fluorescence in the dark-adapted state


Maximum Chl a fluorescence


Maximum quantum yield of PSII


Fresh weight


Heavy metal


Large or small subunits of Rubisco


Coefficient of non-photochemical quenching of excited Chl state

PACMAD clade

Main branch of Poaceae family that includes subfamilies Panicoideae, Aristidoideae, Chloridoideae, Micrairoideae, Arundinideae, Danthonioideae


Phosphate buffer saline


Phosphoenolpyruvate carboxylase


Photosystems I


Photosystems II


Fast relaxing component of NPQ (energy/ΔpH dependent)


Slow relaxing component of NPQ (dependent mainly on photoinhibition)


Coefficient of photochemical quenching of excited Chl state


Coefficient of non-photochemical quenching of excited Chl state


Sodium dodecylsulfate polyacrylamide gel electrophoresis


Effective quantum yield of PSII

Supplementary material

11120_2014_47_MOESM1_ESM.pdf (106 kb)
Supplementary material 1 (PDF 105 kb)


  1. Anikeev VV, Kutuzov FF (1961) New technique for the determination of cereal leaf surface area. Soviet Plant Physiol 8:375–377Google Scholar
  2. Baker AJM (1981) Accumulators and excluders—strategies in response of plants to heavy metals. J Plant Nutr 3:643–654. doi:10.1080/01904168109362866 CrossRefGoogle Scholar
  3. Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212:696–709. doi:10.1007/s004250000439 PubMedCrossRefGoogle Scholar
  4. Bazzaz MB, Govindjee (1974) Effects of cadmium nitrate on spectral characteristics and light reactions of chloroplasts. Environ Lett 6:1–12PubMedCrossRefGoogle Scholar
  5. Burzynski M, Zurek A (2007) Effects of copper and cadmium on photosynthesis in cucumber cotyledons. Photosynthetica 45:239–244. doi:10.1007/s11099-007-0038-9 CrossRefGoogle Scholar
  6. Cai Y, Cao F, Cheng W, Zhang G, Wu F (2011) Modulation of exogenous glutathione in phytochelatins and photosynthetic performance against Cd stress in the two rice genotypes differing in Cd tolerance. Biol Trace Element Res 143:1159–1173. doi:10.1007/s12011-010-8929-1 CrossRefGoogle Scholar
  7. Choi Y-E, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H (2001) Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213:45–50. doi:10.1007/s004250000487 PubMedCrossRefGoogle Scholar
  8. Drazkiewicz M, Tukendorf A, Baszynski T (2003) Age-dependent response of maize leaf segments to cadmium treatment: effect on chlorophyll fluorescence and phytochelatin accumulation. J Plant Physiol 160:247–254. doi:10.1078/0176-1617-00558 PubMedCrossRefGoogle Scholar
  9. Ekmekci Y, Tanyolac D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611. doi:10.1016/j.jplph.2007.01.017 PubMedCrossRefGoogle Scholar
  10. Fagioni M, D’Amici GM, Timperio AM, Zolla L (2009) Proteomic analysis of multiprotein complexes in the thylakoid membrane upon cadmium treatment. J Proteome Res 8:310–326. doi:10.1021/pr800507x PubMedCrossRefGoogle Scholar
  11. Faller P, Kienzler K, Krieger-Liszkay A (2005) Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of photosystem II by competitive binding to the essential Ca2+ site. Biochim Biophys Acta 1706:158–164. doi:10.1016/j.bbabio.2004.10.005 PubMedCrossRefGoogle Scholar
  12. Filek M, Koscielniak J, Łabanowska M, Bednarska E, Bidzinska E (2010) Selenium-induced protection of photosynthesis activity in rape (Brassica napus) seedlings subjected to cadmium stress. Fluorescence and EPR measurements. Photosynth Res 105:27–37. doi:10.1007/s11120-010-9551-y PubMedCrossRefGoogle Scholar
  13. Franco E, Alessandrelli S, Masojidek J, Margonelli A, Giardi MT (1999) Modulation of D1 protein turnover under cadmium and heat stresses monitored by (35S)methionine incorporation. Plant Sci 144:53–61. doi:10.1016/S0168-9452(99)00040-0 CrossRefGoogle Scholar
  14. Geiken B, Masojidek J, Rizzuto M, Pompili ML, Giardi MT (1998) Incorporation of (35S)methionine in higher plants reveals that stimulation of the D1 reaction centre II protein turnover accompanies tolerance to heavy metal stress. Plant, Cell Environ 21:1265–1273. doi:10.1046/j.1365-3040.1998.00361.x CrossRefGoogle Scholar
  15. Hagemeyer J, Waisel Y (1988) Excretions of ions (Cd2+, Li+, Na+, and Cl) by Tamarix aphylla. Physiol Plant 73:541–546. doi:10.1111/j.1399-3054.1988.tb05438.x CrossRefGoogle Scholar
  16. He J-Y, Ren Y-F, Zhu C, Yan Y-P, Jiang D-A (2008) Effect of Cd on growth, photosynthetic gas exchange, and chlorophyll fluorescence of wild and Cd-sensitive mutant rice. Photosynthetica 46:466–470. doi:10.1007/s11099-008-0080-2 CrossRefGoogle Scholar
  17. Horton P, Hague A (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. IV. Resolution of non-photochemical quenching. Biochim Biophys Acta 932:107–115. doi:10.1016/0005-2728(88)90144-2 CrossRefGoogle Scholar
  18. Iglesias AA, Andreo CS (1984) Involvement of thiol groups in the activity of phosphoenolpyruvate carboxylase from maize leaves. Photosynth Res 5:215–226. doi:10.1007/BF00030021 PubMedCrossRefGoogle Scholar
  19. Inouhe M, Ninomiya S, Tohoyama H, Joho M, Murayama T (1994) Different characteristics of roots in the cadmium-tolerance and Cd-binding complex formation between mono- and dicotyledonous plants. J Plant Res 107:201–207. doi:10.1007/BF02344245 CrossRefGoogle Scholar
  20. Janik E, Maksymiec W, Mazur R, Garstka M, Gruszecki WI (2010) Structural and functional modifications of the major light-harvesting complex II in cadmium- or copper-treated Secale cereale. Plant Cell Physiol 51:1330–1340. doi:10.1093/pcp/pcq093 PubMedCrossRefGoogle Scholar
  21. Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dabrowski P, Elsheery NI, Lorenzo L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli DB, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serôdio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res Online first. doi:10.1007/s11120-014-0024-6 Google Scholar
  22. Klaus AA, Lysenko EA, Kholodova VP (2013) Maize plant growth and accumulation of photosynthetic pigments at short- and long-term exposure to cadmium. Russ J Plant Physiol 60:250–259. doi:10.1134/S1021443713020118 CrossRefGoogle Scholar
  23. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349. doi:10.1146/annurev.pp.42.060191.001525 CrossRefGoogle Scholar
  24. Kumar BV, Lakshmi MV, Atkinson JP (1985) Fast and efficient method for detection and estimation of proteins. Biochem Biophys Res Commun 131:883–891. doi:10.1016/0006-291X(85)91322-1 PubMedCrossRefGoogle Scholar
  25. Küpper H, Küpper F, Spiller M (1998) In situ detection of heavy metal substituted chlorophylls in water plants. Photosynth Res 58:123–133. doi:10.1023/A:1006132608181 CrossRefGoogle Scholar
  26. Küpper H, Parameswaran A, Leitenmaier B, Trtílek M, Setlík I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674. doi:10.1111/j.1469-8137.2007.02139.x PubMedCrossRefGoogle Scholar
  27. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. doi:10.1038/227680a0 PubMedCrossRefGoogle Scholar
  28. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. doi:10.1016/0076-6879(87)48036-1 Google Scholar
  29. Lichtenthaler HK, Buschmann C, Knapp M (2005) 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. doi:10.1007/s11099-005-0062-6 CrossRefGoogle Scholar
  30. Liu K-L, Shen L, Wang J-Q, Sheng J-P (2008) Rapid inactivation of chloroplastic ascorbate peroxidase is responsible for oxidative modification to Rubisco in tomato (Lycopersicon esculentum) under cadmium stress. J Integr Plant Biol 50:415–426. doi:10.1111/j.1744-7909.2007.00621.x PubMedCrossRefGoogle Scholar
  31. Liu N, Lin ZF, Lin G-Z, Song L-Y, Chen S-W, Mo H, Peng C-L (2010) Lead and cadmium induced alterations of cellular functions in leaves of Alocasia macrorrhiza L. Schott. Ecotoxicol Environ Safety 73:1238–1245. doi:10.1016/j.ecoenv.2010.06.017 PubMedCrossRefGoogle Scholar
  32. Lysenko EA, Klaus AA, Kuznetsov VV (2013) Analysis of intron-containing pre-mRNA and spliced mRNA in maize chloroplasts by RT-PCR. Mol Biol 47:112–119. doi:10.1134/S002689331301007X CrossRefGoogle Scholar
  33. Mendoza-Cozalt D, Devars S, Loza-Tavera H, Moreno-Sanchez R (2002) Cadmium accumulation in the chloroplast of Euglena gracilis. Physiol Plant 115:276–283. doi:10.1034/j.1399-3054.2002.1150214.x CrossRefGoogle Scholar
  34. Nagel K, Adelmeier U, Voigt J (1996) Subcellular distribution of cadmium in the unicellular green alga Chlamydomonas reinhardtii. J Plant Physiol 149:86–90. doi:10.1016/S0176-1617(96)80178-7 CrossRefGoogle Scholar
  35. Pagliano C, Raviolo M, Dalla Vecchia F, Gabbrielli R, Gonnelli C, Rascio N, Barbato R, La Rocca N (2006) Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.). J Photochem Photobiol, B 84:70–78. doi:10.1016/j.jphotobiol.2006.01.012 CrossRefGoogle Scholar
  36. Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. Plant Physiol 133:829–837. doi:10.1104/pp.103.026518 PubMedCentralPubMedCrossRefGoogle Scholar
  37. Pietrini F, Zacchini M, Iori V, Pietrosanti L, Ferretti M, Massacci A (2010) Spatial distribution of cadmium in leaves and its impact on photosynthesis: examples of different strategies in willow and poplar clones. Plant Biol 12:355–363. doi:10.1111/j.1438-8677.2009.00258.x PubMedCrossRefGoogle Scholar
  38. Rascio N, Dalla Vecchia F, La Rocca N, Barbato R, Pagliano C, Raviolo M, Gonnelli C, Gabbrielli R (2008) Metal accumulation and damage in rice (cv. Vialone nano) seedlings exposed to cadmium. Environ Exp Bot 62:267–278. doi:10.1016/j.envexpbot.2007.09.002 CrossRefGoogle Scholar
  39. Rolland N, Dorne A-J, Amoroso G, Sültemeyer DF, Joyard J, Rochaix J-D (1997) Disruption of the plastid ycf10 open reading frame affects uptake of inorganic carbon in the chloroplast of Chlamydomonas. EMBO J 16:6713–6726. doi:10.1093/emboj/16.22.6713 PubMedCentralPubMedCrossRefGoogle Scholar
  40. Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433. doi:10.1104/pp.109.4.1427 PubMedCentralPubMedGoogle Scholar
  41. Siedlecka A, Krupa Z (1999) Cd/Fe interaction in higher plants—its consequences for the photosynthetic apparatus. Photosynthetica 36:321–331. doi:10.1023/A:1007097518297 CrossRefGoogle Scholar
  42. Stirbet A, Riznichenko GYu, Rubin AB, Govindjee (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochemistry (Mosc) 79:291–323. doi:10.1134/S0006297914040014 CrossRefGoogle Scholar
  43. Talarico L (2002) Fine structure and X-ray microanalysis of a red macrophyte cultured under cadmium stress. Environ Pollut 120:813–821. doi:10.1016/S0269-7491(02)00156-2 PubMedGoogle Scholar
  44. Tang L, Ying R-R, Jiang D, Zeng X-W, Morel J-L, Tang Y-T, Qiu R-L (2013) Impaired leaf CO2 diffusion mediates Cd-induced inhibition of photosynthesis in the Zn/Cd hyperaccumulator Picris divaricata. Plant Physiol Biochem 73:70–76. doi:10.1016/j.plaphy.2013.09.008 PubMedCrossRefGoogle Scholar
  45. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. PNAS USA 76:4350–4354PubMedCentralPubMedCrossRefGoogle Scholar
  46. Walters RG, Horton P (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27:121–133. doi:10.1007/BF00033251 PubMedCrossRefGoogle Scholar
  47. Wu FB, Zhang GP, Yu JS (2003) Genotypic differences in effect of Cd on photosynthesis and chlorophyll fluorescence of barley (Hordeum vulgare L.). Bull Environ Contam Toxicol 71:1272–1281. doi:10.1007/s00128-003-8718-z PubMedGoogle Scholar
  48. Zhou W, Qiu B (2005) Effects of cadmium hyperaccumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae). Plant Sci 169:737–745. doi:10.1016/j.plantsci.2005.05.030 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Eugene A. Lysenko
    • 1
  • Alexander A. Klaus
    • 1
  • Natallia L. Pshybytko
    • 2
  • Victor V. Kusnetsov
    • 1
  1. 1.Timiryazev Institute of Plant Physiology, RASMoscowRussia
  2. 2.Institute of Biophysics and Cell Engineering, NASBMinskBelarus

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