Abstract
A hydroponic experiment was carried out to investigate possible hormetic response induced by cadmium (Cd) in a potential hyperaccumulator-Lonicera japonica Thunb. The results showed that Cd at low concentrations induced a significant increase in plant growth, leaf water content and content of photosynthetic pigments in L. japonica, but decreased them at high concentrations, displayed inverted U-shaped dose response curves, confirming a typical biphasic hormetic response. The U-shaped dose response curves were displayed in malondialdehyde (MDA) and electrolyte leakage in leaves at low doses of Cd, indicating reduce oxidative stress and toxic effect. The increase of superoxide dismutase (SOD) and catalase (CAT) activities was observed along with the increased Cd concentration, indicative of increase in anti-oxidative capacity that ensures redox homeostasis is maintained. After 28 days exposure to 10 mg L−1 Cd, stem and leaf Cd concentrations reached 502.96 ± 28.90 and 103.22 ± 5.62 mg kg−1 DW, respectively and the plant had high bioaccumulation coefficient (BC) and translocation factor (TF′). Moreover, the maximum TF value was found at 2.5 mg L−1 Cd treatment, implying that low Cd treatment improved the ability to transfer Cd from medium via roots to aerial structures. Taking together, L. japonica could be considered as a new plant to investigate the underlying mechanisms of hormesis and Cd tolerance. Our results suggest that hormetic effects should be taken into consideration in phytoremediation of Cd-contaminated soil.
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References
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126
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 212:696–709
Belkhadi A, Hediji H, Abbes Z, Nouairi I, Barhoumi Z, Zarrouk M, Chaïbi W, Djebal W (2010) Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linum usitatissimum L. Ecotox Environ Saf 73:1004–1011
Booker FL, Fiscus EL (2005) The role of ozone flux and antioxidants in the suppression of ozone injury by elevated CO2 in soybean. J Exp Bot 56:2139–2151
Bowler C, Montagu MV, Inzé D (1992) Superoxide dismutase and stress tolerance. Plant Physiol Plant Mol Biol 43:83–116
Calabrese EJ, Baldwin LA (1999) Chemical hormesis: its historical foundations as biological hypothesis. Toxicol Pathol 27:195–216
Calabrese EJ, Baldwin LA (2001) The frequency of U-shaped dose-responses in the toxicological literature. Toxicol Sci 62:330–338
Calabrese EJ, Baldwin LA (2003a) Toxicology rethinks its central belief: hormesis demands a reappraisal of the way risks are assessed. Nature 421:691–692
Calabrese EJ, Baldwin LA (2003b) The hormetic dose-response model is more common than the threshold model in toxicology. Toxicol Sci 71:246–250
Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157:42–48
Calabrese EJ, Staudenmayer JW, Stanek EJ, Hoffmann GR (2006) Hormesis outperforms threshold model in NCI anti-tumor drug screening data. Toxicol Sci 94:368–378
Calabrese EJ, Stanek EJ, Nascarella MA, Hoffmann GR (2008) Hormesis predicts low-dose responses better than threshold models. Int J Toxicol 27:369–378
Calabrese EJ, Hoffmann GR, Stanek EJ, Nascarella MA (2010) Hormesis in high-throughput screening of antibacterial compounds in E coli. Hum Exp Toxicol 29:667–677
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 52:41–46
de la Rosa G, Peralta-Videa JR, Montes M, Parsons JG, Cano-Aguilera I, Gardea-Torresdey JL (2004) Cadmium uptake and translocation in tumbleweed (Salsolakali), a potential Cd-hyperaccumulator desert plant species: ICP/OES and XAS studies. Chemosphere 55:1159–1168
di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–32
Jia L, Liu ZL, Chen W, He XY (2012) Stimulative effect induced by low-concentration cadmium in Lonicera japonica Thunb. Afr J Microbiol Res 6:826–833
Kovalchuk I, Filkowski J, Smith K, Kovalchuk O (2003) Reactive oxygen species stimulate homologous recombination in plants. Plant Cell Environ 26:1531–1539
Krivosheeva A, Tao DL, Ottander C, Wingsle G, Dube SL, Oquist G (1996) Cold acclimation and photoinhibition of photosynthesis in Scots pine. Planta 200:296–305
Larson BMH, Catling PM, Waldron GE (2007) The biology of Canadian weeds.135. Lonicera japonica Thunb. Can J Plant Sci 87:423–438
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592
Lin RZ, Wang XR, Luo Y, Du WC, Guo HY, Yin DQ (2007) Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings (Triticum aestivum L.). Chemosphere 69:89–98
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 169:170–175
Liu ZL, He XY, Chen W (2011) Effects of cadmium hyperaccumulation on the concentrations of four trace elements in Lonicera japonica Thunb. Ecotoxicology 20:698–705
Mattina MJI, Lannucci-Berger W, Musante C, White JC (2003) Concurrent plant uptake of heavy metals and persistent organic pollutants from soil. Environ Pollut 124:375–378
Mattson MP, Calabrese EJ (2010) Hormesis: what it is and why it matters. Hormesis. Springer, New York, pp 1–13
Parson PA (2003) Metabolic efficiency in response to environmental agents predicts hormesis and invalidates the linear no-threshold premise: ionizing radiation as a case study. Crit Rev Toxicol 33:443–450
Poschenrieder C, Gense B, Barcelo J (1989) Influence of cadmium on water relations, stomatal resistance and abscisic acid content in expanding bean leaves. Plant Physiol 90:1365–1371
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 74:6–12
Roosens N, Verbruggen N, Meerts P, Ximenez-Embun P, Smith J (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from Western Europe. Plant Cell Environ 10:1657–1672
Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668
Scebba F, Arduini I, Ercoli L, Sebastiani L (2006) Cadmium effects on growth and antioxidant enzymes activities in Miscanthus sinensis. Biol Plantarum 50:688–692
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 71:76–85
Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedling. Plant Sci 161:1135–1144
Shan SH, Liu F, Li CJ, Wan SB (2012) Effects of cadmium on growth, oxidative stress and antioxidant enzyme activities in peanut (Arachis hypogaea L.) seedlings. J Agric Sci 4:142–151
Skórzyńska-Polit E, Drażkiewicz M, Krupa Z (2010) Lipid peroxidation and antioxidative response in Arabidopsis thaliana exposed to cadmium and copper. Acta Physiol Plant 32:169–175
Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260
Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58
Stebbing ARD (1998) A theory for growth hormesis. Mutat Res 403:249–258
Strzałka K, Kostecka-Gugała A, Latowski D (2003) Carotenoids and environmental stress in plants: significance of carotenoid-mediated modulation of membrane physical properties. Russ J Plant Physiol 50:168–172
Sun YB, Zhou QX, Diao CY (2008) Effects of cadmium and arsenic on growth and metal accumulation of Cd-hyperaccumulator Solanum nigrum L. Bioresour Technol 99:1103–1110
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 161:808–814
Susana RZ, Enrique MN, Luis AM (2010) Accumulation and tolerance characteristics of cadmium in a halophytic Cd-hyperaccumulator, Arthrocnemum macrostachyum. J Hazard Mater 184:299–307
Tang YT, Qiu RL, Zeng XW, Ying RR, Yu FM, Zhou XY (2009) Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ Exp Bot 66:126–134
Tanhan MKP, Pokethitiyook P, Chaiyarat R (2007) Uptake and accumulation of cadmium lead and zinc by Siam weed [Chromolaena odorata (L.) King & Robinson]. Chemosphere 68:323–329
Vig K, Megharaj M, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135
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 80:965–971
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 140:124–135
Wu F, Yang W, Zhang J, Zhou L (2010) Cadmium accumulation and growth responses of a poplar (Populus deltoids×Populus nigra) in cadmium contaminated purple soil and alluvial soil. J Hazard Mater 177:268–273
Zhou WB, Qiu BS (2005) Effects of cadmium hyper-accumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae). Plant Sci 169:737–745
Acknowledgments
The authors are very thankful to Dr. Dali Tao, for his help in improving the manuscript. This work was funded by the National Science and Technology Pillar Program (2012BAC05B05) and the major National Science and Technology project “Water Pollution Control and Management” (2012ZX07202008) of China.
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Jia, L., He, X., Chen, W. et al. Hormesis phenomena under Cd stress in a hyperaccumulator—Lonicera japonica Thunb. Ecotoxicology 22, 476–485 (2013). https://doi.org/10.1007/s10646-013-1041-5
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DOI: https://doi.org/10.1007/s10646-013-1041-5