Abstract
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.




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References
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 2:57–62
Arduinia I, Masonib A, Mariottib M, Ercoli L (2004) Low cadmium application increase miscanthus growth and cadmium translocation. Environ Exp Bot 52:89–100
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Bio-recovery 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
Belz RG, Cedergreen N (2010) Parthenin hormesis in plants depends on growth conditions. Environ Exp Bot 69:293–301
Calabrese EJ (2008) Hormesis: why it is important to toxicology and toxicologists. Environ Toxicol Chem 7:1451–1474
Calabrese EJ (2010) Hormesis is central to toxicology, pharmacology and risk assessment. Hum Exp Toxicol 29:249–261
Calabrese EJ, Baldwin LA (2001a) The frequency of U-shaped dose-responses in the toxicological literature. Toxicol Sci 62:330–338
Calabrese EJ, Baldwin LA (2001b) U-shaped dose–responses in biology, toxicology, and public health. Annu Rev Public Health 22:15–33
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, Baldwin LA, Holland CD (1999) Hormesis: a highly generalizable and reproducible phenomenon with important implications for risk assessment. Risk Anal 19:261–281
Cedergreen N, Olesen CF (2010) Can glyphosate stimulate photosynthesis? Pestic Biochem Physiol 96:140–148
Chaneva G, Parvanova P, Tzvetkova N, Tzvetkova A (2010) Photosynthetic response of maize plants against cadmium and paraquat impact. Water Air Soil Pollut 208:287–293
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
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 10:1281–1283
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 10:1020–1023
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 65:541–546
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
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 22:476–485
Kučera T, Horakova H, Šonska A (2008) Toxic metal ions in photoautotrophic organisms. Photosynthetica 46:481–489
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 175:655–674
Larson BMH, Catling PM, Waldron GE (2007) The biology of Canadian weeds. 135. Lonicera japonica Thunb. Can J Plant Sci 87:423–438
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 5:10–17
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 129:822–829
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 213–214:55–61
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
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
Liu ZL, Chen W, He XY (2012) Cadmium-induced physiological response in Lonicera japonica Thunb. CLEAN Soil Air Water 41:478–484
Mattson MP, Calabrese EJ (2010) Hormesis: what it is and why it matters. Hormesis. Springer, New York, pp 1–13
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
Milone MT, Sgherri C, Clijsters H, Navari-Izzo F (2003) Antioxidative responses of wheat treated with realistic concentration of cadmium. Environ Exp Bot 50:265–276
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
Nwugo CC, Huerta AJ (2008) Silicon-induced cadmium resistance in rice (Oryza sativa). J Plant Nutr Soil Sci 171:841–848
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 326:239–247
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
Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Scebba F, Arduini I, Ercoli L, Sebastiani L (2006) Cadmium effects on growth and antioxidant enzymes activities in Miscanthus sinensis. Biol Plant 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
Shi GR, Cai QS (2008) Photosynthetic and anatomic responses of peanut leaves to cadmium stress. Photosynthetica 46:627–630
Stebbing ARD (2003) A mechanism for hormesis-a problem in the wrong direction. Crit Rev Toxicol 33:463–467
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
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 66:126–134
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 38:26–38
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
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 259:181–189
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 167:81–87
Zhou WB, Qiu BS (2005) Effects of cadmium hyper-accumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae). Plant Sci 169:737–745
Zhou QX, Kong FX, Zhu L (2004) Ecotoxicology. Science Press, Beijing
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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.
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Jia, L., Liu, Z., Chen, W. et al. Hormesis Effects Induced by Cadmium on Growth and Photosynthetic Performance in a Hyperaccumulator, Lonicera japonica Thunb.. J Plant Growth Regul 34, 13–21 (2015). https://doi.org/10.1007/s00344-014-9433-1
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DOI: https://doi.org/10.1007/s00344-014-9433-1