Plant Growth Regulation

, Volume 75, Issue 3, pp 695–706 | Cite as

Effects of application of salicylic acid alleviates cadmium toxicity in perennial ryegrass

  • Xiaoying Bai
  • Yuanjie Dong
  • Jing Kong
  • Linlin Xu
  • Shuang Liu
Original Paper


To study the exogenous salicylic acid (SA) to alleviate the cadmium (Cd) toxicity in ryegrass (Lolium perenne L.), ryegrass plants subjected to 100 μM CdCl2 exposure were treated with different concentrations of SA, and Cd toxicity was evaluated by the decreases in plant growth and chlorophyll content. In Cd-treated plants, the activities of antioxidant enzymes, such as superoxide dismutase, peroxidase and catalase, decreased dramatically in both shoots and roots, whereas the accumulation of superoxide anion (O 2 ·- ), hydrogen peroxide (H2O2) and malondialdehyde (MDA) increased significantly. Excess Cd also decreased soluble protein and ascorbic acid (AsA) contents, increased accumulation of Cd in both shoots and roots; furthermore, the absorption of micronutrients was inhibited. Addition of 200 μM SA had the most significant alleviating effect against Cd toxicity while the addition of 400 μM SA had no significant effect with Cd treatment. Addition of 100, 200, 300 μM SA considerably increased chlorophyll content and the activities of antioxidant enzymes, increased the uptake and translocation of mineral elements, and decreased H2O2 and MDA accumulation in both shoots and roots of Cd-stressed plants. Addition of 200 μM SA not only decreased the Cd uptake in ryegrass, but also decreased the root-to-shoot translocation of Cd and changed its subcellular distribution in plants. Addition of 200 μM SA increased Cd concentrations in soluble fraction and cell wall in both shoots and roots markedly, with the majority of Cd associated with the cell wall and the soluble fraction and a minor part of Cd present in the cell organelle. Based on these results, we conclude that the optimal concentrations of exogenous SA could alleviate Cd-induced stress and promote ryegrass plant growth.


Ryegrass Cd SA Antioxidative systems Ion accumulation Subcellular distribution 



Salicylic acid




Superoxide dismutase






Superoxide anion radical


Reactive oxygen species




Ascorbic acid





The authors thank Pingping Yang (College of Animal Science and Technology, Shandong Agricultural University, China) for her supplying instruments and patient guidance. The authors also thank English Lecturer Mr Stuart Craig MA (England, Taishan University of china) and Dr. G. Jones (University of Florida, USA), for their critical reading and revision of the manuscript. Special acknowledgements are given to the editors and reviewers. This research work was financially supported by the Shandong Provincial Natural Science Foundation of China (ZR2013CM003) and a Project of Shandong Province Higher Educational Science and Technology Program (J14LF08).


  1. Ali NA, Bernal MP, Ater M (2002) Tolerance and bioaccumulation of copper in Phragmites australis and Zea mays. Plant Soil 239:103–111CrossRefGoogle Scholar
  2. Ananieva EA, Alexieva VS, Popova LP (2002) Treatment with salicylic acid decreases the effects of paraquat on photosynthesis. J Plant Physiol 159:685–693CrossRefGoogle Scholar
  3. Arienzo M, Adamo P, Cozzolino V (2004) The potential of Lolium perenne for revegetation of contaminated soil from a metallur-gical site. Sci Total Environ 319:13–25CrossRefPubMedGoogle Scholar
  4. Barceló J, Poschenrieder CH (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37CrossRefGoogle Scholar
  5. 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 126:1024–1030CrossRefPubMedCentralPubMedGoogle Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizating the principle of protein dyes binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  7. Chao YY, Chen CY, Huang WD, Kao CH (2010) Salicylic acid-mediated hydrogen peroxide accumulation and protection against Cd toxicity in rice leaves. Plant Soil 329:327–337CrossRefGoogle Scholar
  8. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719CrossRefPubMedGoogle Scholar
  9. Davies CS, Nielsen SS, Nielsen NC (1987) Flavor improvement of soybean preparations by genetic removal of lipoxygenase-2. J Am Oil Chem Soc 64:1428–1433CrossRefGoogle Scholar
  10. De DN (2000) Plant Cell Vacuoles. CSIRO Publishing, CollingwoodGoogle Scholar
  11. Djebali W, Zarrouk M, Brouquisse R, El Kahoui S, Limam F, Ghorbel MH, Chaïbi W (2005) Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes. Plant Biol 7:258–268CrossRefGoogle Scholar
  12. Drazic G, Mihailovic N (2005) Modification of cadmium toxicity in soybean seedlings by salicylic acid. Plant Sci 168:511–517CrossRefGoogle Scholar
  13. Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxyl ammonium-chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620CrossRefPubMedGoogle Scholar
  14. Ericson MC, Alfinito AE (1984) Proteins produced during salt stress in tobacco cell cultures. Plant Physiol 74:506–509CrossRefPubMedCentralPubMedGoogle Scholar
  15. Ernst WHO, Verkleij JAC, Schat H (1992) Metal tolerance in plants. Acta Bot Neerl 41:229–248Google Scholar
  16. Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46CrossRefGoogle Scholar
  17. Gordon LK, Minibayeva FV, Rakhmatullina DF, Alyabyev AJ, Ogorodnikova TI, Loseva NL, Valitova YN (2004) Heat production of wheat roots induced by the disruption of proton gradient by salicylic acid. Thermoch Acta 422:101–104CrossRefGoogle Scholar
  18. 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 147:743–749CrossRefPubMedGoogle Scholar
  19. Guo Q, Meng L, Mao PC, Jia YQ, Shi YJ (2013) Role of exogenous salicylic acid in alleviating cadmium-induced toxicity in Kentucky bluegrass. Biochem Syst Ecol 50:269–276CrossRefGoogle Scholar
  20. Hall J (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11CrossRefPubMedGoogle Scholar
  21. Hannaway D, Fransen S, Cropper J, Teel M, Chaney M, Griggs T, Halse R, Hart J, Cheeke P, Hansen D, Klinger R, Lane W (1999) Perennial ryegrass (Lolium perenne L.). In: A pacific northwest extension publication, vol PNW 502. Oregon State University, Washington State University, University of IdahoGoogle Scholar
  22. Hayat S, Ali B, Ahmad A (2007) Salicylic acid: biosynthesis, metabolism and physiological role in plants. Salicylic acid: a plant hormone, pp 1–14Google Scholar
  23. Hayens RJ (1980) Ion exchange properties of roots and ionic interactions within the root POPLsn: their role in ion accumulation by plants. Bot Rev 46:75–99CrossRefGoogle Scholar
  24. He JY, Ren YF, Pan XB, Yan YP, Zhu C, Jiang D (2010) Salicylic acid alleviates the toxicity effect of cadmium on germination, seedling growth, and amylase activity of rice. J Nutr Soil Sci 173(2):300–305CrossRefGoogle Scholar
  25. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I: kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefPubMedGoogle Scholar
  26. Hernandez LE, Cooke DT (1997) Modifications of the root plasma membrane lipid composition of cadmium-treated Pisum sativum. J Exp Bot 48:1375–1381CrossRefGoogle Scholar
  27. Horváth E, Szalai G, Janda T (2007) Induction of Abiotic Stress Tolerance by Salicylic Acid Signaling. J Plant Growth Regul 26:290–300CrossRefGoogle Scholar
  28. Hsu Y, Kao C (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238CrossRefGoogle Scholar
  29. Jonak C, Őkrész L, Bögre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5:415–424CrossRefPubMedGoogle Scholar
  30. Kang HM, Saltviet M (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576CrossRefPubMedGoogle Scholar
  31. Knudson LL, Tibbitts TW, Edwards GE (1977) Measurement of ozone injury by determination of leaf chlorophyll concentration. Plant Physiol 60:606–608CrossRefPubMedCentralPubMedGoogle Scholar
  32. Kováčik J, Grúz J, Bačkor M, Strnad M, Repčák M (2009) Salicylic acid-induced changes to growth and phenolic metabolism in Matricaria chamomilla plants. Plant Cell Rep 28:135–143CrossRefPubMedGoogle Scholar
  33. Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330CrossRefGoogle Scholar
  34. Leita L, De Nobili M, Mondini C, Baca-García MT (1993) Response of leguminosae to cadmium exposure. J Plant Nutr 16:2001–2012CrossRefGoogle Scholar
  35. Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–736CrossRefPubMedGoogle Scholar
  36. Maslenkova L, Toncheva S (1998) Salicylic acid induced changes in photosystem II reactions in barley plants. Compt Rend Acad Bulg Sci 51:101–104Google Scholar
  37. Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281CrossRefPubMedCentralPubMedGoogle Scholar
  38. Mostofa MG, Fujita M (2013) Salicylic acid alleviates copper toxicity in rice (Oryza sativa L.) seedlings by up-regulating antioxidative and glyoxalase systems. Ecotoxicology 22:959–973CrossRefPubMedGoogle Scholar
  39. Nickel RS, Cunningham BA (1969) Improved peroxidase assay method using Ieuco 2, 3, 6-trichlcroindophenol and application to comparative measurements of peroxidase catalysis. Anal Biochem 27:292–299CrossRefPubMedGoogle Scholar
  40. Palmgren MG, Harper JF (1999) Pumping with plant P-type ATPases. J Exp Bot 50:883–893CrossRefGoogle Scholar
  41. Patra HL, Kar M, Mishre D (1978) Catalase activity in leaves and cotyledons during plant development and senescence. Biochem Pharmacol 172:385–390Google Scholar
  42. Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492CrossRefPubMedGoogle Scholar
  43. Pinto AP, Mota AM, de Varennes A, Pinto FC (2004) Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants. Sci Total Environ 326:239–247CrossRefPubMedGoogle Scholar
  44. Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224–231CrossRefPubMedGoogle Scholar
  45. Prasad KVSK, Saradhi PP, Sharmila P (1999) Concerted action of antioxidant enzymes and curtailed growth under zinc toxicity in Brassica juncea. Environ Exp Bot 42:1–10CrossRefGoogle Scholar
  46. Raza SH, Shafiq F (2013) Exploring the role of salicylic acid to attenuate cadmium accumulation in radish (Raphanus sativus). Int J Agric Biol 15(3):547–552Google Scholar
  47. Reinheckel T, Noack H, Lorenz S, Wiswedel I, Augustin W (1998) Comparison of protein oxidation and aldehyde formation during oxidative stress in isolated mitochondria. Free Radic Res 29:297–305CrossRefPubMedGoogle Scholar
  48. Saidi I, Ayouni M, Dhieb A, Chtourou Y, Chaïbi W, Djebali W (2013) Oxidative damages induced by short-term exposure to cadmium in bean plants:protective role of salicylic acid. S Afr J Bot 85:32–38CrossRefGoogle Scholar
  49. Schützendübel A, Nikolova P, Rudolf C, Polle A (2002) Cadmium and H2O2-induced oxidative stress in populus canescens roots. Plant Physiol Biochem 40:577–584CrossRefGoogle Scholar
  50. Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50CrossRefPubMedGoogle Scholar
  51. Shi GR, Cai QS, Liu QQ, Wu L (2009) Salicylic acid-mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake, photosynthesis, and antioxidant enzymes. Acta Physiol Plant 31:969–977CrossRefGoogle Scholar
  52. Stewart RC, Bewley JD (1980) Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 65:245–248CrossRefPubMedCentralPubMedGoogle Scholar
  53. Tonamura B (1978) Test reactions for a stopped flow apparatus regulation of 2, 6-D and potassium ferricyanide by L-ascorbic acid. Anal Biochem 84:370–383CrossRefGoogle Scholar
  54. Wagner GJ (1993) Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51:173–212CrossRefGoogle Scholar
  55. Wang QH, Liang X, Dong YJ, Xu LL, Zhang XW, Hou J, Fan ZY (2013) Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regul 69:11–20CrossRefGoogle Scholar
  56. Weigel HJ, Jäger HJ (1980) Subcellular distribution and chemical form of cadmium in bean plants. Plant Physiol 65:480–482CrossRefPubMedCentralPubMedGoogle Scholar
  57. Xiong J, An L, Lu H, Yhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765CrossRefPubMedGoogle Scholar
  58. Xu J, Wang WY, Yin HX, Liu XJ, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxindegradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330CrossRefGoogle Scholar
  59. Xu LL, Dong YJ, Kong J, Liu S (2013) Effects of root and foliar applications of exogenous NO on alleviating cadmium toxicity in lettuce seedlings. Plant Growth Regul. doi: 10.1007/s10725-013-9834-3 Google Scholar
  60. Zawoznik MS, Groppa MD, Tomaro ML, Benavides MP (2007) Endogenous salicylic acid potentiates cadmium-induced oxidative stress in Arabidopsis thaliana. Plant Sci 173:190–197CrossRefGoogle Scholar
  61. Zhang ZL, Di WJ (2003) Laboratory guide for plant physiology [M]. Higher Education Press, BeijingGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Xiaoying Bai
    • 1
  • Yuanjie Dong
    • 1
    • 2
  • Jing Kong
    • 1
  • Linlin Xu
    • 1
  • Shuang Liu
    • 1
  1. 1.College of Resources and EnvironmentShandong Agricultural UniversityTai’anPeople’s Republic of China
  2. 2.Chinese National Engineering Laboratory for Efficient Utilization of Soil and Fertilizer ResourcesTai’anPeople’s Republic of China

Personalised recommendations