Journal of Plant Growth Regulation

, Volume 34, Issue 1, pp 13–21 | Cite as

Hormesis Effects Induced by Cadmium on Growth and Photosynthetic Performance in a Hyperaccumulator, Lonicera japonica Thunb.

  • Lian Jia
  • Zhouli Liu
  • Wei Chen
  • Yin Ye
  • Shuai Yu
  • Xingyuan He


A soil experiment was designed to investigate the hormesis effect of cadmium (Cd) on the growth and the photosynthetic performance in a hyperaccumulator, Lonicera japonica Thunb. by measuring gas exchange, chlorophyll fluorescence parameters, and photosynthetic pigments. After 90 days of exposure to soil containing 25 mg kg−1 Cd, shoot Cd concentrations reached 168.27 ± 5.01 μg g−1 dry weight, without showing symptoms of visible damage to the plants. The results also show that Cd at low concentrations (≤10 mg kg−1) induced a significant increase in plant biomass, net photosynthetic rate (P n), content of chlorophyll (a, b, and a+b) and carotenoids, effective quantum yield ΦPSII and photochemical quenching coefficient q p, but inhibited them at high concentrations (>25 mg kg−1), confirming a hormetic response. The observed growth increases were closely related to the increase in net photosynthesis induced by Cd, though the causes of the P n increase are still not understood. The present study suggested that hormetic effects should be taken into consideration in phytoremediation of Cd-contaminated soil and the dose range of Cd inducing hormesis on L. japonica is proposed as 2.5–10 mg kg−1 in the soil.


Cadmium Hormesis Lonicera japonica Thunb. Photosynthesis Growth U-shaped curve 



This work was supported by the National Natural Science Foundation of China (41301340), the National Science & Technology Pillar Program (2012BAC05B05) and the major National Science & Technology project “water pollution control and management” (2012ZX07202008) of China.


  1. Amani AL (2008) Cadmium induced changes in pigment content, ion uptake, proline content and phosphoenolypyruvate carboxylase activity of Triticum aestivum seedlings. Aust J Basic Appl Sci 2:57–62Google Scholar
  2. Arduinia I, Masonib A, Mariottib M, Ercoli L (2004) Low cadmium application increase miscanthus growth and cadmium translocation. Environ Exp Bot 52:89–100CrossRefGoogle Scholar
  3. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Bio-recovery 1:81–126Google Scholar
  4. 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 212:696–709CrossRefPubMedGoogle Scholar
  5. Belz RG, Cedergreen N (2010) Parthenin hormesis in plants depends on growth conditions. Environ Exp Bot 69:293–301CrossRefGoogle Scholar
  6. Calabrese EJ (2008) Hormesis: why it is important to toxicology and toxicologists. Environ Toxicol Chem 7:1451–1474CrossRefGoogle Scholar
  7. Calabrese EJ (2010) Hormesis is central to toxicology, pharmacology and risk assessment. Hum Exp Toxicol 29:249–261CrossRefPubMedGoogle Scholar
  8. Calabrese EJ, Baldwin LA (2001a) The frequency of U-shaped dose-responses in the toxicological literature. Toxicol Sci 62:330–338CrossRefPubMedGoogle Scholar
  9. Calabrese EJ, Baldwin LA (2001b) U-shaped dose–responses in biology, toxicology, and public health. Annu Rev Public Health 22:15–33CrossRefPubMedGoogle Scholar
  10. Calabrese EJ, Baldwin LA (2003a) Toxicology rethinks its central belief: hormesis demands a reappraisal of the way risks are assessed. Nature 421:691–692CrossRefPubMedGoogle Scholar
  11. Calabrese EJ, Baldwin LA (2003b) The hormetic dose-response model is more common than the threshold model in toxicology. Toxicol Sci 71:246–250CrossRefPubMedGoogle Scholar
  12. Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157:42–48CrossRefPubMedGoogle Scholar
  13. Calabrese EJ, Baldwin LA, Holland CD (1999) Hormesis: a highly generalizable and reproducible phenomenon with important implications for risk assessment. Risk Anal 19:261–281PubMedGoogle Scholar
  14. Cedergreen N, Olesen CF (2010) Can glyphosate stimulate photosynthesis? Pestic Biochem Physiol 96:140–148CrossRefGoogle Scholar
  15. Chaneva G, Parvanova P, Tzvetkova N, Tzvetkova A (2010) Photosynthetic response of maize plants against cadmium and paraquat impact. Water Air Soil Pollut 208:287–293CrossRefGoogle Scholar
  16. Chen X, Wang J, Shi Y, Zhao MQ, Chi GY (2011) Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. Bot Stud 52:41–46Google Scholar
  17. Dai HP, Wei Y, Yang TX, Sa WQ, Wei AZ (2010) Influence of cadmium stress on chlorophyll fluorescence characteristics in Populus × canescens. J Food Agric Environ 10:1281–1283Google Scholar
  18. Dai HP, Yuan W, Zhang YZ et al (2012) Influence of photosynthesis and chlorophyll synthesis on Cd accumulation in Populus × canescens. J Food Agric Environ 10:1020–1023Google Scholar
  19. Han SH, Lee JC, Oh CY, Kim PG (2006) Alleviation of Cd toxicity by composted sewage sludge in Cd-treated Schmidt birch (Betula schmidtii) seedlings. Chemosphere 65:541–546CrossRefPubMedGoogle Scholar
  20. Jia L, Liu ZL, Chen W, He XY (2012) Stimulative effect induced by low-concentration Cadmium in Lonicera japonica Thunb. Afr J Microbiol Res 6:826–833Google Scholar
  21. Jia L, He XY, Chen W, Liu ZL, Huang YQ, Yu S (2013) Hormesis phenomena under Cd stress in a hyperaccumulator—Lonicera japonica Thunb. Ecotoxicology 22:476–485CrossRefPubMedGoogle Scholar
  22. Kučera T, Horakova H, Šonska A (2008) Toxic metal ions in photoautotrophic organisms. Photosynthetica 46:481–489CrossRefGoogle Scholar
  23. Kupper H, Aravind P, Leitenmaier B, Trtilek M, Šetlik I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to Cd-stress in the Cd Hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674CrossRefPubMedGoogle Scholar
  24. Larson BMH, Catling PM, Waldron GE (2007) The biology of Canadian weeds. 135. Lonicera japonica Thunb. Can J Plant Sci 87:423–438CrossRefGoogle Scholar
  25. Lefcort H, Freedman Z, House S, Pendleton M (2008) Hormetic effects of heavy metals in aquatic snails: is a little bit of pollution good? EcoHealth 5:10–17CrossRefPubMedGoogle Scholar
  26. Li P, Cai R, Gao H, Peng T, Wang Z (2007) Partitioning of excitation energy in two wheat cultivars with different grain protein contents grown under three nitrogen applications in the field. Physiol Plant 129:822–829CrossRefGoogle Scholar
  27. Li X, Bu N, Li Y, Ma L, Xin S, Zhang L (2012) Growth, photosynthesis and antioxidant responses of endophyte infected and non-infected rice under lead stress conditions. J Hazard Mater 213–214:55–61CrossRefPubMedGoogle Scholar
  28. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592Google Scholar
  29. Liu ZL, He XY, Chen W, Yuan FH, Yan K, Tao DL (2009) Accumulation and tolerance characteristics of cadmium in a potential hyperaccumulator—Lonicera japonica Thunb. J Hazard Mater 169:170–175CrossRefPubMedGoogle Scholar
  30. Liu ZL, He XY, Chen W (2011) Effects of cadmium hyperaccumulation on the concentrations of four trace elements in Lonicera japonica Thunb. Ecotoxicology 20:698–705CrossRefPubMedGoogle Scholar
  31. Liu ZL, Chen W, He XY (2012) Cadmium-induced physiological response in Lonicera japonica Thunb. CLEAN Soil Air Water 41:478–484CrossRefGoogle Scholar
  32. Mattson MP, Calabrese EJ (2010) Hormesis: what it is and why it matters. Hormesis. Springer, New York, pp 1–13CrossRefGoogle Scholar
  33. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefPubMedGoogle Scholar
  34. Milone MT, Sgherri C, Clijsters H, Navari-Izzo F (2003) Antioxidative responses of wheat treated with realistic concentration of cadmium. Environ Exp Bot 50:265–276CrossRefGoogle Scholar
  35. 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 164:601–610CrossRefPubMedGoogle Scholar
  36. Nwugo CC, Huerta AJ (2008) Silicon-induced cadmium resistance in rice (Oryza sativa). J Plant Nutr Soil Sci 171:841–848CrossRefGoogle Scholar
  37. 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
  38. Qiu RL, Zhao X, Tang YT, Yu FM, Hu PJ (2008) Antioxidative response to Cd in a newly discovered cadmium hyperaccumulator, Arabis paniculata F. Chemosphere 74:6–12CrossRefPubMedGoogle Scholar
  39. Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130CrossRefGoogle Scholar
  40. Scebba F, Arduini I, Ercoli L, Sebastiani L (2006) Cadmium effects on growth and antioxidant enzymes activities in Miscanthus sinensis. Biol Plant 50:688–692CrossRefGoogle Scholar
  41. Seth CS, Chaturvedi PK, Misra V (2008) The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotoxicol Environ Saf 71:76–85CrossRefPubMedGoogle Scholar
  42. Shi GR, Cai QS (2008) Photosynthetic and anatomic responses of peanut leaves to cadmium stress. Photosynthetica 46:627–630CrossRefGoogle Scholar
  43. Stebbing ARD (2003) A mechanism for hormesis-a problem in the wrong direction. Crit Rev Toxicol 33:463–467CrossRefPubMedGoogle Scholar
  44. Sun YB, Zhou QX, Wang L, Liu W (2009) Cadmium tolerance and accumulation characteristics of Bidens pilosa L. as a potential Cd-hyperaccumulator. J Hazard Mater 161:808–814CrossRefPubMedGoogle Scholar
  45. Tang YT, Qiu RL, Zeng XW, Ying RR, Yu FM, Zhou XY (2009a) Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ Exp Bot 66:126–134CrossRefGoogle Scholar
  46. Tang YT, Qiu RL, Zeng XW, Fang XH, Yu FM, Zhou XY (2009b) Zn and Cd hyperaccumulating characteristics of Picris divaricata Vant. Int J Environ Pollut 38:26–38CrossRefGoogle Scholar
  47. Wang CR, Tian Y, Wang XR, Yu HX, Lu XW, Wang C (2010) Hormesis effects and implicative application in assessment of lead-contaminated soils in roots of Vicia faba seedlings. Chemosphere 80:965–971CrossRefPubMedGoogle Scholar
  48. Wu SC, Cheung KC, Luo YM, Wong MH (2006) Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 140:124–135CrossRefPubMedGoogle Scholar
  49. Yang XE, Long XX, Ye HB, He ZL, Calver DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189CrossRefGoogle Scholar
  50. Ying RR, Qiu RL, Tang YT, Hu PJ, Qiu H, Chen HR, Shi TH, Morel JL (2010) Cadmium tolerance of carbon assimilation enzymes and chloroplast in Zn/Cd hyperaccumulator Picris divaricata. J Plant Physiol 167:81–87CrossRefPubMedGoogle Scholar
  51. Zhou WB, Qiu BS (2005) Effects of cadmium hyper-accumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae). Plant Sci 169:737–745CrossRefGoogle Scholar
  52. Zhou QX, Kong FX, Zhu L (2004) Ecotoxicology. Science Press, BeijingGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Lian Jia
    • 1
    • 2
  • Zhouli Liu
    • 1
  • Wei Chen
    • 1
  • Yin Ye
    • 1
  • Shuai Yu
    • 1
  • Xingyuan He
    • 1
  1. 1.State Key Laboratory of Forest and Soil Ecology, Institute of Applied EcologyChinese Academy of SciencesShenyangPeople’s Republic of China
  2. 2.College of Chemistry and Life ScienceAnshan Normal UniversityAnshanPeople’s Republic of China

Personalised recommendations