Acta Physiologiae Plantarum

, Volume 35, Issue 4, pp 1281–1289 | Cite as

Cadmium toxicity affects photosynthesis and plant growth at different levels

  • Maria Celeste Dias
  • Cristina Monteiro
  • José Moutinho-Pereira
  • Carlos Correia
  • Berta Gonçalves
  • Conceição Santos
Original Paper


In this article we discuss and update some of the effects of Cd toxicity on the photosynthetic apparatus in a model crop Lactuca sativa. Seeds of L. sativa were germinated in solutions with 0, 1, 10 and 50 μM of Cd(NO3)2 and then transferred to a hydroponic culture medium. After 28 days, the effects of Cd on the photosynthetic apparatus of lettuce were analysed. Exposure of lettuce to 1 μM Cd(NO3)2 affected already plant growth (dry biomass), but, did not induce serious damages in the photosynthetic apparatus. However, increasing concentrations of this metal to 10 and 50 μM promoted a strong reduction of the maximum photochemical efficiency of PSII and an impairment of net CO2 assimilation rate, putatively due to Rubisco activity decrease. This ultimately results in a strong inhibition of plant growth. Nutrient uptake and carbohydrate assimilation were also severely affected by Cd.


Cadmium Nutrients Photosynthesis Pigments Rubisco 



Net CO2 assimilation rate


Ratio of intercellular to atmospheric CO2 concentration




Dry weight


Transpiration rate


Fresh weight


Maximal efficiency of PSII


Stomatal conductance


Ribulose 1,5 bisphosphate carboxylase/oxygenase


Relative water content



This work was supported by the Portuguese Foundation for Science and technology (FCT) FCT/PTDC/AAC-AMB/112804/2009, BioRem: integration of multiple Biomarkers of toxicity in an assay of phytoremediation in contaminated sites. FCT also supported a post-doctoral fellowship of M. C. Dias (SFRH/BPD/41700/2007) and the doctoral fellowship of C. Monteiro (SFRH/BD/48204/2008).


  1. Ammar WB, Nouairi I, Zarrouk M, Ghorbel MH, Jemal F (2008) Antioxidative response to cadmium in roots and leaves of tomato plants. Biol Plant 52:727–731CrossRefGoogle Scholar
  2. Azevedo H, Pinto G, Fernandes J, Loureiro S, Santos C (2005a) Cadmium effects on sunflower: growth and photosynthesis. J Plant Nutr 28:2211–2220CrossRefGoogle Scholar
  3. Azevedo H, Pinto G, Santos C (2005b) Cadmium effects in sunflower: membrane permeability and changes in catalase and peroxidase activity in leaves and calluses. J Plant Nutr 28:2233–2241CrossRefGoogle Scholar
  4. Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Brazilian J Plant Physiol 17:21–34Google Scholar
  5. Bi Y, Chen W, Zhang W, Zhou Q, Yun L, Xing D (2009) Production of reactive oxygen species, impairment of photosynthetic function and dynamic changes in mitochondria are early events in cadmium-induced cell death in Arabidopsis thaliana. Biol Cell 100:629–643CrossRefGoogle Scholar
  6. Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  7. Burzynski M, Klobus G (2004) Changes of photosynthetic parameters in cucumber leaves under Cu, Cd, and Pb stress. Photosynth 42:505–510CrossRefGoogle Scholar
  8. Chaffei C, Pageau K, Suzuki A, Gouia H, Ghorbel HM, Mascalaux-Daubresse C (2004) Cadmium toxicity induced changes in nitrogen management in Lycopersicon esculentum leading to a metabolic safeguard through an amino acid storage strategy. Plant Cell Physiol 45:1681–1693PubMedCrossRefGoogle Scholar
  9. Choudhury NK, Behera RK (2001) Photoinhibition of photosynthesis: role of carotenoids in photoprotection of chloroplasts. Photosynthetica 39:481–488CrossRefGoogle Scholar
  10. Correia MJ, Fonseca F, Azedo-Silva J, Dias C, David MM, Barrote I, Osório ML, Osório J (2005) Effects of water deficit on the activity of nitrate reductase and contents of sugars, nitrate and free amino acids in the leaves and roots of sunflower and with lupin plants growing under two nutrient supply regimes. Physiol Plantarum 124:61–70CrossRefGoogle Scholar
  11. Costa G, Morel J (1994) Water relations, gas exchange and amino acid content in Cd-treated lettuce. Plant Physiol Biochem 32:561–570Google Scholar
  12. Dias MC, Brüggemann W (2007) Photosynthesis under drought stress in Flaveria species with different degrees of development of the C4 syndrome. Photosynthetica 45:75–84CrossRefGoogle Scholar
  13. Dias MC, Pinto G, Santos C (2011) Acclimatization of micropropagated plantlets induces an antioxidative burst: a case study with Ulmus minor Mill. Photosynthetica 49:259–266CrossRefGoogle Scholar
  14. Dias MC, Pinto G, Correia C, Moutinho-Pereira J, Silva S, Santos C (2012) Photosynthetic parameters of Ulmus minor plantlets affected by irradiance during acclimatization. Biol Plant. doi: 10.1007/s10535-012-0234-8 Google Scholar
  15. Dong J, Wu FB, Zhang GP (2006) Influence of cadmium on antioxidant capacity and four microelement concentrations in tomato seedlings (Lycopersicon esculentum). Chemosphere 64:1659–1666PubMedCrossRefGoogle Scholar
  16. Ekmekçi Y, Tanyolç D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611PubMedCrossRefGoogle Scholar
  17. Fodor F (2002) Physiological responses of vascular plants to heavy metals. In: Prasad MNV, Strzalka K (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer Academic Publishers, Dordrecht, pp 149–177Google Scholar
  18. Gill SS, Khan N, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182:112–120PubMedCrossRefGoogle Scholar
  19. Krapp A, Stitt M (1995) An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady state transcript levels after cold-girdling source leaves. Planta 195:313–323CrossRefGoogle Scholar
  20. Krupa Z, Siedlecka A, Kleczkowski L (1999) Cadmium-affected level of inorganic phosphate in rye leaves influences Rubisco subunits. Acta Physiol Plantarum 21:257–261CrossRefGoogle Scholar
  21. Kummerová M, Zezulka Š, Králóvá K, Masarovičová E (2010) Effect of zinc and cadmium on physiological and production characteristics in Matricaria recutita. Biol Plant 54:308–314CrossRefGoogle Scholar
  22. Küpper H, Aravind P, Leitenmaier B, Trtílek M, Šetlík I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to Cd-stress in the Cd hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674PubMedCrossRefGoogle Scholar
  23. Lagriffoul A, Mocquot B, Mench M, Vangronsveld J (1998) Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant Soil 200:241–250CrossRefGoogle Scholar
  24. Lilley RM, Walker DA (1974) An improved spectrophotometric assay for ribulose bisphosphate carboxylase. Bioch Biophysic Acta 358:226–229CrossRefGoogle Scholar
  25. López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2011) Effects of cadmium on gas exchange and phytohormone contents in citrus. Biol Plantarum 55:187–190CrossRefGoogle Scholar
  26. López-Millán A-F, Sagardoy R, Solanas M, Abadía A, Abadía J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ Exp Botany 65:376–385CrossRefGoogle Scholar
  27. McBride MB (2003) Cadmium concentration limits in agricultural soils: weaknesses in USEPA’s risk assessment and the 503 rule. Hum Ecol Risk Assess 9:661–674CrossRefGoogle Scholar
  28. Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610PubMedCrossRefGoogle Scholar
  29. Monteiro MS, Santos C, Soares AM, Mann RM (2009) Assessment of biomarkers of cadmium stress in lettuce. Ecotoxicol Environ Saf 72:811–819PubMedCrossRefGoogle Scholar
  30. Monteiro C, Santos C, Pinho S, Oliveira H, Pedrosa T, Dias MC (2012) Cadmium-induced cyto- and genotoxicity are organ-dependent in lettuce. Chem Res Toxicol 25:1423–1434PubMedCrossRefGoogle Scholar
  31. Nelson WO, Campbell PGC (1991) The effects of acidification on the geochemistry of Al, Cd, Pb and Hg in freshwater environments: a literature review. Environ Pollut 71:91–130PubMedCrossRefGoogle Scholar
  32. Pál M, Horváth E, Jand T, Páldi E, Szalai G (2006) Physiological changes and defense mechanisms induced by cadmium stress in maize. J Plant Nutr Soil Sci 169:239–246CrossRefGoogle Scholar
  33. Papoyan A, Pineros M, Kochian LV (2007) Plant Cd2+ and Zn2+ status effects on root and shoot heavy metal accumulation in Thlaspi caerulescens. New Phytol 175:51–58PubMedCrossRefGoogle Scholar
  34. 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 133:829–837PubMedCrossRefGoogle Scholar
  35. Podazza G, Rosa M, González JA, Hilal M, Prado FE (2006) Cadmium induces changes in sucrose partitioning, invertase activities and membrane functionality in roots of Rangpur lime (Citrus limonia L. Osbeck). Plant Biol 8:706–714PubMedCrossRefGoogle Scholar
  36. Rod M, Liu M, Qi H, Zhang ZP, Song ZW, Kou TJ (2012) Response of photosynthesis and chlorophyll fluorescence to drought stress in two maize cultivars. African J Agri Res 34:4751–4760Google Scholar
  37. Roh KS, Choi BY (2004) Sucrose regulates growth and activation of rubisco in tobacco leaves in vitro. Biotech Bioprocess Eng 9:229–235CrossRefGoogle Scholar
  38. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signalling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709PubMedCrossRefGoogle Scholar
  39. Roth U, Von Roepenack-Lahaye E, Clemens S (2006) Proteome changes in Arabidopsis thaliana roots upon exposure to Cd2+. J Exp Bot 57:4003–4013PubMedCrossRefGoogle Scholar
  40. Sandalio L, Dalurzo H, Gomes M, Romero-Puertas M, del Rio L (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Botany 52:2115–2126Google Scholar
  41. Santos C, Monteiro M, Dias MC (2010) Cadmium toxicity in crops: a review. Environmental science, engineering and technology. Nova Publishers, NovinkaGoogle Scholar
  42. Siedlecka A, Krupa Z, Samuelsson G, Öquist G, Gardeström P (1997) Primary carbon metabolism in Phaseolus vulgaris plants under Cd/Fe interaction. Plant Physiol Biochem 35:951–957Google Scholar
  43. Sims DA, Gamon JA (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sens Environ 81:337–354CrossRefGoogle Scholar
  44. Singh RP, Agrawal M (2007) Effects of sewage sludge amendment on heavy metal accumulation and consequent responses of Beta vulgaris plants. Chemosphere 67:2229–2240PubMedCrossRefGoogle Scholar
  45. Vassilev A, Lidon FC, Matos MC, Ramalho JC, Yordanov I (2002) Photosynthetic performance and content of some nutrients in cadmium and copper treated barley plants. J Plant Nut 25:2343–2360CrossRefGoogle Scholar
  46. Wang C, Fan X, Wang G, Niu J, Zhou B (2011) Differential expression of rubisco in sporophytes and gametophytes of some marine macroalgae. PLoS One 6:e16351PubMedCrossRefGoogle Scholar
  47. Wójcik M, Tukiendorf A (2005) Cadmium uptake, localization and detoxification in Zea mays. Biol Plant 49:237–245CrossRefGoogle Scholar
  48. Young AJ (1991) The photoprotective role of carotenoids in higher plants. Physiol Plant 83:702–708CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2012

Authors and Affiliations

  • Maria Celeste Dias
    • 1
  • Cristina Monteiro
    • 1
  • José Moutinho-Pereira
    • 2
  • Carlos Correia
    • 2
  • Berta Gonçalves
    • 2
  • Conceição Santos
    • 1
  1. 1.Department of Biology and Centre for Environmental and Marine Studies (CESAM)University of Aveiro, Campus Universitário de SantiagoAveiroPortugal
  2. 2.Department of Biology and Environment, Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB)University of Trás-os-Montes e Alto DouroVila RealPortugal

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