Acta Physiologiae Plantarum

, Volume 31, Issue 5, pp 969–977 | Cite as

Salicylic acid-mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake, photosynthesis, and antioxidant enzymes

Original Paper


To assess the role of salicylic acid (SA) in alleviating cadmium (Cd) toxicity in hemp (Cannabis sativa L.) plants, the growth parameters, Cd accumulation, photosynthetic performance and activities of major antioxidant enzymes were investigated in hemp seedlings treated with 500 μM SA, under 0, 25, 50, and 100 mg Cd kg−1 sands (DW) conditions, respectively. Cd exposure resulted in a small reduction in biomass (12.0–26.9% for root, and 8.7–29.4% for shoot, respectively), indicating hemp plants have innate capacity to tolerant Cd stress. This was illustrated by little inhibition in photosynthetic performance, unchanged malondialdehyde content, and enhancement of superoxide dismutase (SOD) and peroxidases (POD) activities in hemp plants. Cd content in root is 25.0–29.5 times’ higher than that in shoot, suggesting the plant can be classified as a Cd excluder. It is concluded that SA pretreatment counteracted the Cd-induced inhibition in plant growth. The beneficial effects of SA in alleviating Cd toxicity can be attributed to the SA-induced reduction of Cd uptake, improvement of photosynthetic capacity, and enhancement of SOD and POD activities.


Antioxidant enzyme Cadmium Cannabis sativa Photosynthesis Salicylic acid 









Intercellular CO2 concentration


Transpiration rate


Steady-state chlorophyll fluorescence yield


The minimal fluorescence


The maximal fluorescence


The maximal fluorescence of light-adapted leaf


The variable fluorescence


Maximal quantum yield of PS II


Stomatal conductance




Photosystem II


Photosystem I


Net-photosynthetic rate




The effective quantum yield of PS II


Dark respiration


Reactive-oxygen species


Superoxide dismutase


Translocation factor



Financial support from the natural science foundation of Jiangsu province (BK2006148) and the natural science foundation for college of Anhui province (KJ2008B66ZC, KJ2009B073) is gratefully acknowledged.


  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. doi: 10.1016/S0076-6879(84)05016-3 PubMedCrossRefGoogle Scholar
  2. Alvarez ME (2000) Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol Biol 44:429–442. doi: 10.1023/A:1026561029533 PubMedCrossRefGoogle Scholar
  3. Azevedo Neto AD, Prisco JT, Eneas-Filho J, Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94. doi: 10.1016/j.envexpbot.2005.01.008 CrossRefGoogle Scholar
  4. Baker AJM (1987) Metal tolerance. New Phytol 106:93–111Google Scholar
  5. Barcelo J, Poschenrieder C (1990) Plant water relations as affected by heavy metal Stress: A review. J Plant Nutr 13:1–37. doi: 10.1080/01904169009364057 CrossRefGoogle Scholar
  6. Beauchamp C, Fridovich I (1971) Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. doi: 10.1016/0003-2697(71)90370-8 PubMedCrossRefGoogle Scholar
  7. Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030. doi: 10.1104/pp.126.3.1024 PubMedCrossRefGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi: 10.1016/0003-2697(76)90527-3 PubMedCrossRefGoogle Scholar
  9. Chaoui A, Mazhoudi S, Ghorbal M, El Ferjani E (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci 127:139–147. doi: 10.1016/S0168-9452(97)00115-5 CrossRefGoogle Scholar
  10. Chartzoulakisa K, Patakasb A, Kofidisc G, Bosabalidisc A, Nastoub A (2002) Water stress affects leaf anatomy, gas exchange, water relations and growth of two avocado cultivars. Sci Hortic (Amsterdam) 95:39–50. doi: 10.1016/S0304-4238(02)00016-X CrossRefGoogle Scholar
  11. Chen Z, Iyer S, Caplan A, Klessig DF, Fan B (1997) Differential accumulation of salicylic acid and salicylic acid-sensitive catalase in different rice tissues. Plant Physiol 114:193–201. doi: 10.1104/pp.114.1.265 PubMedCrossRefGoogle Scholar
  12. Chien H, Wang J, Lin C, Kao C (2001) Cadmium toxicity of rice leaves is mediated through lipid peroxidation. Plant Growth Regul 33:205–213. doi: 10.1023/A:1017539616793 CrossRefGoogle Scholar
  13. Choudhury S, Panda SK (2004) Role of salicylic acid in regulating cadmium induced oxidative stress in Oryza sativa. Bulg J Plant Physiol 30:95–110Google Scholar
  14. Citterio S, Santagostino A, Fumagalli P, Prato N, Ranalli P, Sgorbati S (2003) Heavy metal tolerance and accumulation of Cd, Cr and Ni by Cannabis sativa L. Plant Soil 256:243–252. doi: 10.1023/A:1026113905129 CrossRefGoogle Scholar
  15. Dahmani-Muller H, van Oort F, Gélie B, Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. New Phytol 109:231–238Google Scholar
  16. Dat JF, Foyer CH, Scott IM (1998a) Changes in salicylic acid and antioxidants during induced thermo tolerance in mustard seedlings. Plant Physiol 118:1455–1461. doi: 10.1104/pp.118.4.1455 PubMedCrossRefGoogle Scholar
  17. Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998b) Parallel changes in H2O2 and catalase during thermo tolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357. doi: 10.1104/pp.116.4.1351 PubMedCrossRefGoogle Scholar
  18. De Filippis LF, Ziegler H (1993) Effect of sublethal concentrations of zinc, cadmium and mercury on the photosynthetic carbon reduction cycle of Euglena. J Plant Physiol 142:167–172Google Scholar
  19. Drazic G, Mihailovic N (2005) Modification of cadmium toxicity in soybean seedlings by salicylic acid. Plant Sci 168:511–517. doi: 10.1016/j.plantsci.2004.09.019 CrossRefGoogle Scholar
  20. Dražić G, Mihailović N, Lojić M (2006) Cadmium accumulation in Medicago sativa seedlings treated with salicylic acid. Biol Plant 50:239–244. doi: 10.1007/s10535-006-0013-5 CrossRefGoogle Scholar
  21. 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
  22. Durner J, Shah J, Klessig DF (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2:266–274. doi: 10.1016/S1360-1385(97)86349-2 CrossRefGoogle Scholar
  23. Durnford DG, Price JA, McKim SM, Sarchfield ML (2003) Light harvesting complex gene expression is controlled by both transcriptional and post-transcriptional mechanisms during photoacclimation in Chlamydomonas reinhardtii. Physiol Plant 118:193–205. doi: 10.1034/j.1399-3054.2003.00078.x CrossRefGoogle Scholar
  24. Ekmekçi Y, Tanyolaç 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
  25. Foyer C, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071. doi: 10.1111/j.1365-3040.2005.01327.x CrossRefGoogle Scholar
  26. Gallego S, Benavides M, Tomaro M (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159. doi: 10.1016/S0168-9452(96)04528-1 CrossRefGoogle Scholar
  27. Greger M, Ogren E (1991) Direct and indirect effects of Cd2+ on photosynthesis in sugar beet (Beta vulgaris). Physiol Plant 83:129–135. doi: 10.1111/j.1399-3054.1991.tb01291.x CrossRefGoogle Scholar
  28. Guo B, Liang YC, Zhu YG, Zhao FJ (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 147:743–749. doi: 10.1016/j.envpol.2006.09.007 PubMedCrossRefGoogle Scholar
  29. Guo B, Liang Y, Zhu Y (2009) Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice? J Plant Physiol 166:20–31. doi: 10.1016/j.jplph.2008.01.002 PubMedCrossRefGoogle Scholar
  30. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11. doi: 10.1093/jexbot/53.366.1 PubMedCrossRefGoogle Scholar
  31. Horvath G, Droppa M, Oraveez A, Raskin V, Marder JB (1996) Formation of the photosynthetic apparatus during greening of cadmium poisoned barley leaves. Planta 199:238–243. doi: 10.1007/BF00196564 CrossRefGoogle Scholar
  32. Hura T, Hura K, Grzesiak M, Rzepka A (2007) Effect of long-term drought stress on leaf gas exchange and fluorescence parameters in C3 and C4 plants. Acta Physiol Plant 29:103–113. doi: 10.1007/s11738-006-0013-2 CrossRefGoogle Scholar
  33. Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling in maize (Zea mays L.) plants. Planta 208:175–180. doi: 10.1007/s004250050547 CrossRefGoogle Scholar
  34. Kang HM, Saltveit M (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576. doi: 10.1034/j.1399-3054.2002.1150411.x PubMedCrossRefGoogle Scholar
  35. Klessig DF, Malamy J (1994) The salicylic acid signal in plants. Plant Mol Biol 26:1439–1458. doi: 10.1007/BF00016484 PubMedCrossRefGoogle Scholar
  36. Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931. doi: 10.1016/j.jplph.2006.11.014 PubMedCrossRefGoogle Scholar
  37. Li HS (2000) Principles and techniques of plant physiological biochemical experiment. Higher Education Press, Beijing, pp 260–263Google Scholar
  38. Liao YC, Chang Chien SW, Wang MC, Shen Y, Hung PL, Das B (2006) Effect of transpiration on Pb uptake by lettuce and on water soluble low molecular weight organic acids in rhizosphere. Chemosphere 65:343–351. doi: 10.1016/j.chemosphere.2006.02.010 PubMedCrossRefGoogle Scholar
  39. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic membranes. Methods Enzymol 148:350–382. doi: 10.1016/0076-6879(87)48036-1 CrossRefGoogle Scholar
  40. Lichtenthaler HK, Miehe JA (1997) Fluorescence imaging as a diagnostic tool for plant stress. Trends Plant Sci 2:316–320. doi: 10.1016/S1360-1385(97)89954-2 CrossRefGoogle Scholar
  41. Linger P, Müssig J, Fischer H, Kobert J (2002) Industrial hemp (Cannabis sativa L.) growing on heavy metal contaminated soil: fibre quality and phytoremediation potential. Ind Crops Prod 16:33–42. doi: 10.1016/S0926-6690(02)00005-5
  42. Linger P, Ostwald A, Haensler J (2005) Cannabis sativa L growing on heavy metal contaminated soil: growth, cadmium uptake and photosynthesis. Biol Plant 49:567–576. doi: 10.1007/s10535-005-0051-4 CrossRefGoogle Scholar
  43. Lozano-Rodriguez E, Hernàndez L, Bonay P, Carpena-Ruiz R (1997) Distribution of cadmium in shoot and root tissues of maize and pea plants: physiological disturbances. J Exp Bot 48:123–128. doi: 10.1093/jxb/48.1.123 CrossRefGoogle Scholar
  44. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. doi: 10.1093/jexbot/51.345.659 PubMedCrossRefGoogle Scholar
  45. Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281. doi: 10.1104/pp.102.018457 PubMedCrossRefGoogle Scholar
  46. Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178PubMedGoogle Scholar
  47. Mishra A, Choudhuri MA (1999) Effects of salicylic acid on heavy metal-induced membrane deterioration mediated lipoxygenase in rice. Biol Plant 42:409–415. doi: 10.1023/A:1002469303670 CrossRefGoogle Scholar
  48. 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 164:601–610. doi: 10.1016/j.jplph.2006.03.003 PubMedCrossRefGoogle Scholar
  49. Novák V, Vidovič J (2003) Transpiration and nutrient uptake dynamics in maize (Zea mays L.). Ecol Modell 166:99–107. doi: 10.1016/S0304-3800(03)00102-9 CrossRefGoogle Scholar
  50. Pál M, Szalai G, Horváth E, Janda T, Páldi E (2002) Effect of salicylic acid during heavy metal stress. Acta Biol Szeged 46:119–120Google Scholar
  51. Pál M, Leskó K, Janda T, Páldi E, Szalai G (2007) Cadmium-induced changes in the membrane lipid composition of maize plants. Cereal Res Commun 35:1631–1642. doi: 10.1556/CRC.35.2007.4.10 CrossRefGoogle Scholar
  52. Putter J (1974) Peroxidases. In: Bergmeyer HU (ed) Methods of enzymatic analysis: II. Academic Press, New York, pp 685–690Google Scholar
  53. Radwan DEM, Fayez AK, Mahmoud SY, Hamad A, Lu GQ (2006) Salicylic acid alleviates growth inhibition and oxidative stress caused by zucchini yellow mosaic virus infection in Cucurbita pepo leaves. Physiol Mol Plant Pathol 69:172–181. doi: 10.1016/j.pmpp.2007.04.004 CrossRefGoogle Scholar
  54. Rai VK, Sharma SS, Sharma S (1986) Reversal of ABA-induced stomatal closure by phenolic compounds. J Exp Bot 37:129–134. doi: 10.1093/jxb/37.1.129 CrossRefGoogle Scholar
  55. Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433PubMedGoogle Scholar
  56. Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plant. J Exp Bot 52:2115–2126PubMedGoogle Scholar
  57. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365. doi: 10.1093/jexbot/53.372.1351 PubMedCrossRefGoogle Scholar
  58. Senaratna T, Touchell D, Bunns E, Dixon K (2000) Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:157–161. doi: 10.1023/A:1006386800974 CrossRefGoogle Scholar
  59. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant response and adaptation to heavy metal stress. J Exp Bot 57:711–726. doi: 10.1093/jxb/erj073 PubMedCrossRefGoogle Scholar
  60. Sharma YK, Leon J, Raskin I, Davis KR (1996) Ozone-induced responses in Arabidopsis thaliana—the role of salicylic acid in the accumulation of defence-related transcripts and induced resistance. Proc Natl Acad Sci USA 93:5099–5104. doi: 10.1073/pnas.93.10.5099 PubMedCrossRefGoogle Scholar
  61. Siedlecka A, Krupa Z (2002) Functions of enzymes in heavy metal treated plants. In: Prasad MNV, Kazimierz S (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer, The Netherlands, pp 314–317Google Scholar
  62. Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85:85–89. doi: 10.1111/j.1399-3054.1992.tb05267.x CrossRefGoogle Scholar
  63. Sudhakar C, Lakshmi A, Giridarakumar S (2001) Changes in the antioxidant enzymes efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci 161:613–619. doi: 10.1016/S0168-9452(01)00450-2 CrossRefGoogle Scholar
  64. Tani FH, Barrington S (2005) Zinc and copper uptake by plants under two transpiration rates Part I. Wheat (Triticum aestivum L.). Environ Pollut 138:538–547PubMedGoogle Scholar
  65. Tasgin E, Attici O, Nalbantogly B (2003) Effect of salicylic acid and cold on freezing tolerance in winter wheat leaves. Plant Growth Regul 41:231–236. doi: 10.1023/B:GROW.0000007504.41476.c2 CrossRefGoogle Scholar
  66. Vaillant N, Monnet F, Hitmi A, Sallanon H, Coudret A (2005) Comparative study of responses in four Datura species to a zinc stress. Chemosphere 59:1005–1013. doi: 10.1016/j.chemosphere.2004.11.030 PubMedCrossRefGoogle Scholar
  67. Vaŕadi G, Polyańka H, Darkó È, Lehoczki E (2003) Atrazine resistance entails a limited xanthophylls cycle activity, a lower PS II efficiency and altered pattern of excess excitation dissipation. Physiol Plant 118:47–56. doi: 10.1034/j.1399-3054.2003.00089.x PubMedCrossRefGoogle Scholar
  68. Venendaal R, Jorgensen U, Foster CA (1997) European energy crops: a synthesis. Biomass Bioenergy 13:147–185. doi: 10.1016/S0961-9534(97)00029-9 CrossRefGoogle Scholar
  69. Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189. doi: 10.1023/B:PLSO.0000020956.24027.f2 CrossRefGoogle Scholar
  70. Zawoznik MS, Groppa MD, Tomaro ML, Benavides MP (2007) Endogenous salicylic acid potentiates cadmium-induced oxidative stress in Arabidopsis thaliana. Plant Sci 173:190–197. doi: 10.1016/j.plantsci.2007.05.004 CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2009

Authors and Affiliations

  1. 1.College of Life SciencesNanjing Agricultural UniversityNanjingPeople’s Republic of China
  2. 2.The Anui Provincial Key Laboratory of the Resource Plant Biology, Department of BiologyHuaibei Coal Industry Teachers CollegeHuaibeiPeople’s Republic of China

Personalised recommendations