Physiological and Biochemical Characteristics of Cinnamomum camphora in Response to Cu- and Cd-Contaminated Soil

  • Jihai ZhouEmail author
  • Kun Cheng
  • Jiyong Zheng
  • Zaiqun Liu
  • Weibo ShenEmail author
  • Houbao Fan
  • Zhinong Jin


Copper (Cu) and cadmium (Cd) are ordinary heavy metals. Unreasonable development and utilization of these heavy metals will cause severe pollution to the soils and consequently bring damage to human health. Therefore, recovering soils polluted by heavy metals is crucial. An indoor pot experiment was carried out involving seven treatments, namely, low-concentration Cu stress (Cu1), high-concentration Cu stress (Cu2), low-concentration Cd stress (Cd1), high-concentration Cd stress (Cd2), low-concentration Cu–Cd combined stress (Cu1Cd1), and high-concentration Cu–Cd combined stress (Cu2Cd2), and an uncontaminated soil as a control. Results demonstrated that the net photosynthetic rate and chlorophyll content are approximately 8.36–72.51% and 7.22–36.50%, respectively, lower under the Cu, Cd, and Cu–Cd combined stresses than under the control. The net photosynthetic rates are higher under Cu2 and Cd2 than under Cu1 and Cd1; by contrast, the net photosynthetic rate of leaves is lower under Cu2Cd2 than under Cu1Cd1. The net photosynthesis rate of Cinnamomum camphora is significantly positively correlated with superoxide dismutase activity but is significantly negatively correlated with the total chlorophyll, malondialdehyde, soluble sugar, and proline contents. Young Cinnamomum camphora grows well under Cu, Cd, and Cu–Cd combined stresses and is applicable in ecologically restoring heavy metal–contaminated soils.


Young Cinnamomum camphora Heavy-metal stress Combined pollution Physiology Biochemistry 


Funding Information

This work was financially supported by the Science and Technology Key Project of Jiangxi Provincial Department of Education (GJJ20180921), National Natural Science Foundation of China (31460149), Key Project of Jiangxi Provincial Department of Science and Technology (20171ACH80016), Special Graduate Student Innovation Fund of Jiangxi Province in 2017 (YJSCX20170008), and the fund of State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau (K318009902-1414).


  1. Ali, H., Khan, E., & Sajad, M. A. (2013). Phytoremediation of heavy metals-concepts and applications. Chemosphere, 91, 869–881.CrossRefGoogle Scholar
  2. Andresen, E., & Kupper, H. (2013). Cadmium toxicity in plants. Metal Ions in Life Sciences, 11, 395–413.CrossRefGoogle Scholar
  3. Batool, R., Hameed, M., Ashraf, M., Fatima, S., Nawaz, T., & Ahmad, M. S. A. (2014). Structural and functional response to metal toxicity in aquatic Cyperus alopecuroides Rottb. Limnologica – Ecol and Manag Inland Waters, 48, 46–56.CrossRefGoogle Scholar
  4. Bharwana, S. A., Ali, S., Farooq, M. A., Ali, B., Iqbal, N., Abbas, F., & Ahmad, M. S. A. (2014). Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environmental Science and Pollution Research, 21, 717–731.CrossRefGoogle Scholar
  5. Bolan, N., Kunhikrishnan, A., Thangarajan, R., Kumpiene, J., Park, J., Makino, T., Kirkham, M. B., & Scheckel, K. (2014). Remediation of heavy metal(loid)s contaminated soils – to mobilize or to immobilize? Journal of Hazardous Materials, 266, 141–166.CrossRefGoogle Scholar
  6. Capuana, M. (2011). Heavy metals and woody plants - biotechnologies for phytoremediation. iForest, 4, 7–15.CrossRefGoogle Scholar
  7. Chen, G. C., Liu, Y. Q., Wang, R. M., Zhang, J. F., & Owens, G. (2013). Cadmium adsorption by willow root: the role of cell walls and their subfractions. Environmental Science and Pollution Research, 20, 5665–5672.CrossRefGoogle Scholar
  8. Chen, J., Yan, Z., & Li, X. (2014). Effect of methyl jasmonate on cadmium uptake and antioxidative capacity in Kandelia obovata seedlings under cadmium stress. Ecotoxicology and Environmental Safety, 104, 349–356.CrossRefGoogle Scholar
  9. Choppala, G., Saifullah, Bolan, N., Bibi, S., Iqbal, M., Rengel, Z., Kunhikrishnan, A., Ashwath, N., & Ok, Y. S. (2014). Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Critical Reviews in Plant Sciences, 33, 374–391.CrossRefGoogle Scholar
  10. Di Baccio, D., Castagna, A., Tognetti, R., Ranieri, A., & Sebastiani, L. (2014). Early responses to cadmium of two poplar clones that differ in stress tolerance. Journal of Plant Physiology, 171, 1693–1705.CrossRefGoogle Scholar
  11. Etesami, H. (2018). Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicology and Environmental Safety, 147, 175–191.CrossRefGoogle Scholar
  12. Fan, S. K., Fang, X. Z., Guan, M. Y., Ye, Y. Q., Lin, X. Y., Du, S. T., & Jin, C. W. (2014). Exogenous abscisic acid application decreases cadmium accumulation in Arabidopsis plants, which is associated with the inhibition of IRT1-mediated cadmium uptake. Frontiers in Plant Science, 5, 1–8.CrossRefGoogle Scholar
  13. Guarino, C., Conte, B., Spada, V., Arena, S., Sciarrillo, R., & Scaloni, A. (2014). Proteomic analysis of eucalyptus leaves unveils putative mechanisms involved in the plant response to a real condition of soil contamination by multiple heavy metals in the presence or absence of mycorrhizal/rhizobacterial additives. Environmental Science & Technology, 48, 11487–11496.CrossRefGoogle Scholar
  14. Guerrier, G. (1997). Proline accumulation in leaves of NaCl-sensitive and NaCl-tolerant tomatoes. Biologia Plantarum, 40, 623–628.CrossRefGoogle Scholar
  15. Han, R. M., Lefèvre, I., Albacete, A., Pérez-Alfocea, F., Barba-Espín, G., Díaz-Vivancos, P., Quinet, M., Ruan, C. J., Hernandez, J. A., & Cantero-Navarro, E. (2013). Antioxidant enzyme activities and hormonal status in response to Cd stress in the wetland halophyte Kosteletzkya virginica under saline conditions. Physiologia Plantarum, 147, 352–368.CrossRefGoogle Scholar
  16. Hassan, Z., & Aarts, M. G. M. (2011). Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environmental and Experimental Botany, 72, 53–63.CrossRefGoogle Scholar
  17. Ho, J. R., Ma, H. W., Wang, Y. C., Ko, C. H., Chang, F. C., Feng, F. L., & Wang, Y. N. (2014). Extraction of heavy metals from contaminated soil by Cinnamomum camphora. Ecotoxicology, 23(10), 1987–1995.CrossRefGoogle Scholar
  18. Hu, Y. F., Zhou, G. Y., Na, X. F., Yang, L. J., Nan, W. B., Liu, X., Zhang, Y. Q., Li, J. L., & Bi, Y. R. (2013). Cadmium interferes with maintenance of auxin homeostasis in Arabidopsis seedlings. Journal of Plant Physiology, 170, 965–975.CrossRefGoogle Scholar
  19. Iannone, M. F., Groppa, M. D., & Benavides, M. P. (2015). Cadmium induces different biochemical responses in wild type and catalase-deficient tobacco plants. Environmental and Experimental Botany, 109, 201–211.CrossRefGoogle Scholar
  20. Leitenmaier, B., & Kupper, H. (2013). Compartmentation and complexation of metals in hyperaccumulator plants. Frontiers in Plant Science, 4, 1–13.CrossRefGoogle Scholar
  21. Li, H. S. (2000). Principles and techniques of plant physiological biochemical experiment (pp. 164–169). Beijing: Higher Education Press (in Chinese).Google Scholar
  22. Llugany, M., Tolrà, R., Martín, S. R., Poschenrieder, C., & Barceló, J. (2013). Cadmium-induced changes in glutathione and phenolics of Thlaspi and Noccaea species differing in Cd accumulation. Journal of Plant Nutrition and Soil Science, 176, 851–858.CrossRefGoogle Scholar
  23. Lu, K., Yang, X., Gielen, G., & Bolan, N. (2017). Effect of bamboo and rice straw biochars on the mobility and redistribution of heavy metals (Cd, Cu, Pb and Zn) in contaminated soil. Journal of Environmental Management, 186, 285–292.CrossRefGoogle Scholar
  24. Luo, Z. B., Wu, C. H., Zhang, C., Li, H., Lipka, U., & Polle, A. (2014). The role of ectomycorrhizas in heavy metal stress tolerance of host plants. Environmental and Experimental Botany, 108, 47–62.CrossRefGoogle Scholar
  25. Ma, Y. L., He, J. L., Ma, C. F., Luo, J., Li, H., Liu, T. X., Polle, A., Peng, C. F., & Luo, Z. B. (2014). Ectomycorrhizas with Paxillus involutus enhance cadmium uptake and tolerance in Populus × canescens. Plant, Cell & Environment, 37, 627–642.CrossRefGoogle Scholar
  26. Mao, X., Jiang, R., Xiao, W., & Yu, J. (2015). Use of surfactants for the remediation of contaminated soils: a review. Journal of Hazardous Materials, 285, 419–435.CrossRefGoogle Scholar
  27. Marmiroli, M., Pietrini, F., Maestri, E., Zacchini, M., Marmiroli, N., & Massacci, A. (2011). Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree Physiology, 31, 1319–1334.CrossRefGoogle Scholar
  28. Marmiroli, M., Imperiale, D., Maestri, E., & Marmiroli, N. (2013). The response of Populus spp. to cadmium stress: chemical, morphological and proteomics study. Chemosphere, 93, 1333–1344.CrossRefGoogle Scholar
  29. Medas, D., De Giudici, G., Pusceddu, C., Casu, M. A., Birarda, G., Vaccari, L., Gianoncelli, A., & Meneghini, C. (2017). Impact of Zn excess on biomineralization processes in Juncus acutus grown in mine polluted sites. Journal of Hazardous Materials.
  30. Ovecka, M., & Takac, T. (2014). Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnology Advances, 32, 73–86.CrossRefGoogle Scholar
  31. Pizarro, I., Gómez-Gómez, M., León, J., Román, D., & Palacios, M. A. (2016). Bioaccessibility and arsenic speciation in carrots, beets and quinoa from a contaminated area of Chile. Science of the Total Environment, 565, 557–563.CrossRefGoogle Scholar
  32. Poonam, S., Kaur, H., & Geetika, S. (2013). Effect of jasmonic acid on photosynthetic pigments and stress markers in Cajanus cajan (L.) Mill sp. seedlings under copper stress. American Journal of Plant Sciences, 4, 817–823.CrossRefGoogle Scholar
  33. Rajkumar, M., Prasad, M. N. V., Freitas, H., & Ae, N. (2009). Biotechnological applications of serpentine bacteria for phytoremediation of heavy metals. Critical Reviews in Biotechnology, 29, 120–130.CrossRefGoogle Scholar
  34. Shi, W. G., Li, H., Liu, T. X., Polle, A., Peng, C. H., & Luo, Z. B. (2015). Exogenous abscisic acid alleviates zinc uptake and accumulation in Populus × canescens exposed to excess zinc. Plant, Cell & Environment, 38, 207–223.CrossRefGoogle Scholar
  35. Stolarikova-Vaculikova, M., Romeo, S., Minnocci, A., Luxova, M., Vaculik, M., Lux, A., & Sebastiani, L. (2015). Anatomical, biochemical and morphological responses of poplar Populus deltoides clone Lux to Zn excess. Environmental and Experimental Botany, 109, 235–243.CrossRefGoogle Scholar
  36. Suthar, V., Memon, K. S., & Mahmood-UI-Hassan, M. (2014). EDTA-enhanced phytoremediation of contaminated calcareous soils: heavy metal bioavailability, extractability, and uptake by maize and sesbania. Environmental Monitoring and Assessment, 186, 3957–3968.CrossRefGoogle Scholar
  37. Tao, S., Sun, L., Ma, C., Li, L., Li, G., & Hao, L. (2013). Reducing basal salicylic acid enhances Arabidopsis tolerance to lead or cadmium. Plant and Soil, 372, 309–318.CrossRefGoogle Scholar
  38. Tuzen, M., Sesli, E., & Soylak, M. (2007). Trace element levels of mushroom species from East Black Sea region of Turkey. Food Control, 18(7), 806–810.CrossRefGoogle Scholar
  39. Upadhyay, R. K. (2014). Metal stress in plants: Its detoxification in natural environment. Brazilian Journal of Botany, 37, 377–382.CrossRefGoogle Scholar
  40. Wang, B., Wang, C., Li, J., Sun, H., & Xu, Z. (2014). Remediation of alkaline soil with heavy metal contamination using tourmaline as a novel amendment. Journal of Environmental Chemical Engineering, 2, 1281–1286.CrossRefGoogle Scholar
  41. Wang, R., Wang, J., Zhao, L., Yang, S., & Song, Y. (2015). Impact of heavy metal stresses on the growth and auxin homeostasis of Arabidopsis seedlings. Biometals, 28, 123–132.CrossRefGoogle Scholar
  42. Wu, G., Kang, H. B., Zhang, X. Y., Shao, H. B., Chu, L. Y., & Ruan, C. J. (2010). A critical review on the bio-removal of hazardous heavy metals from contaminated soils: issues, progress, eco-environmental concerns and opportunities. Journal of Hazardous Materials, 174, 1–8.CrossRefGoogle Scholar
  43. Xie, Y., Li, X., Liu, X., Amombo, E., Chen, L., & Fu, J. (2017). Application of aspergillus aculeatus, to rice roots reduces cd concentration in grain. Plant and Soil, 1, 1–14.Google Scholar
  44. Zhan, J., & Sun, Q. Y. (2011). Diversity of free-living nitrogen-fixing microorganisms in wastelands of copper mine tailings during the process of natural ecological restoration. Journal of Environmental Sciences (China), 23, 476–487.CrossRefGoogle Scholar
  45. Zhu, X. F., Wang, Z. W., Dong, F., Lei, G. J., Shi, Y. Z., Li, G. X., & Zheng, S. J. (2013). Exogenous auxin alleviates cadmium toxicity in Arabidopsis thaliana by stimulating synthesis of hemicellulose 1 and increasing the cadmium fixation capacity of root cell walls. Journal of Hazardous Materials, 263, 398–403.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Jiangxi Key Laboratory for Restoration of Degraded Ecosystems & Watershed Ecohydrology, National and Local Joint Engineering Laboratory of Water Engineering Safety and Effective Utilization of Water Resources in Poyang Lake WatershedNanchang Institute of TechnologyNanchangChina
  2. 2.College of Life SciencesAnhui Normal UniversityWuhuChina
  3. 3.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation, Institute of Soil and Water ConservationNorthwest A&F UniversityYanglingChina

Personalised recommendations