Effects of calcium at toxic concentrations of cadmium in plants

Abstract

Main conclusion

This review provides new insight that calcium plays important roles in plant growth, heavy metal accumulation and translocation, photosynthesis, oxidative damage and signal transduction under cadmium stress.

Increasing heavy metal pollution problems have raised word-wide concerns. Cadmium (Cd), being a highly toxic metal, poses potential risks both to ecosystems and human health. Compared with conventional technologies, phytoremediation, being cost-efficient, highly stable and environment-friendly, is believed to be a promising green technology for Cd decontamination. However, Cd can be easily taken up by plants and may cause severe phytotoxicity to plants, thus limiting the efficiency of phytoremediation. Various researches are being done to investigate the effects of exogenous substances on the mitigation of Cd toxicity to plants. Calcium (Ca) is an essential plant macronutrient that involved in various plant physiological processes, such as plant growth and development, cell division, cytoplasmic streaming, photosynthesis and intracellular signaling transduction. Due to the chemical similarity between Ca and Cd, Ca may mediate Cd-induced physiological or metabolic changes in plants. Recent studies have shown that Ca could be used as an exogenous substance to protect plants against Cd stress by the alleviation of growth inhibition, regulation of metal uptake and translocation, improvement of photosynthesis, mitigation of oxidative damages and the control of signal transduction in the plants. The effects of Ca on toxic concentrations of Cd in plants are reviewed. This review also provides new insight that plants with enhanced Ca level have improved resistance to Cd stress.

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References

  1. Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran LS (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS One 10(1):e0114571

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  2. Ajm B, Whiting SN (2002) In search of the Holy Grail—a further step in understanding metal hyperaccumulation? New Phytol 155(1):1–4

    Article  Google Scholar 

  3. Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91(7):869–881

    CAS  PubMed  Article  Google Scholar 

  4. Andosch A, Affenzeller MJ, Lutz C, Lutz-Meindl U (2012) A freshwater green alga under cadmium stress: ameliorating calcium effects on ultrastructure and photosynthesis in the unicellular model Micrasterias. J Plant Physiol 169(15):1489–1500

    CAS  PubMed  Article  Google Scholar 

  5. Ansari MM, Neha, Khan HA (2015) Effect of cadmium chloride exposure during the induction of collagen induced arthritis. Chem Biol Interact 238:55–65

    CAS  PubMed  Article  Google Scholar 

  6. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  PubMed  Article  Google Scholar 

  7. Baliardini C, Meyer CL, Salis P, Saumitoulaprade P, Verbruggen N (2015) CATION EXCHANGER1 cosegregates with cadmium tolerance in the metal hyperaccumulator Arabidopsis halleri and plays a role in limiting oxidative stress in Arabidopsis spp. Plant Physiol 169(1):549–559

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  8. Bartlett JE, Baranov SV, Ananyev GM, Dismukes GC (2008) Calcium controls the assembly of the photosynthetic water-oxidizing complex: a cadmium(II) inorganic mutant of the Mn4Ca core. Philos Trans R Soc Lond B Biol Sci 363(1494):1253–1261

    CAS  PubMed  Article  Google Scholar 

  9. Bhargava A, Carmona FF, Bhargava M, Srivastava S (2012) Approaches for enhanced phytoextraction of heavy metals. J Environ Manag 105:103–120

    CAS  Article  Google Scholar 

  10. Brand JJ, Becker DW (1984) Evidence for direct roles of calcium in photosynthesis. J Bioenerg Biomembr 16(4):239–249

    CAS  PubMed  Article  Google Scholar 

  11. Brodziak-Dopierała B, Kwapuliński J, Sobczyk K, Wiechuła D (2015) Analysis of the content of cadmium and zinc in parts of the human hip joint. Biol Trace Elem Res 163(1–2):73–80

    PubMed  Article  CAS  Google Scholar 

  12. Brunetti P, Zanella L, Proia A, De PA, Falasca G, Altamura MM, Sanità DTL, Costantino P, Cardarelli M (2011) Cadmium tolerance and phytochelatin content of Arabidopsis seedlings over-expressing the phytochelatin synthase gene AtPCS1. J Exp Bot 62(15):5509–5519

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. Buhlungu BP, Ntoni NJ (2002) Phytoremediation of cadmium-contaminated soils using Leonotis leonurus. Folia Cardiol 9(6):545–551

    Google Scholar 

  14. Cao D-j, X-d Shi, Li H, P-p Xie, H-m Zhang, J-w Deng, Y-g Liang (2015) Effects of lead on tolerance, bioaccumulation, and antioxidative defense system of green algae, Cladophora. Ecotox Environ Safe 112:231–237

    CAS  Article  Google Scholar 

  15. Chang Y-S, Chang Y-J, Lin C-T, Lee M-C, Wu C-W, Lai Y-H (2013) Nitrogen fertilization promotes the phytoremediation of cadmium in Pentas lanceolata. Int Biodeter Biodegr 85:709–714

    CAS  Article  Google Scholar 

  16. Chao Y-Y, Hong C-Y, Chen C-Y, Kao CH (2011) The importance of glutathione in defence against cadmium-induced toxicity of rice seedlings. Crop Environ Bioinform 8:217–228

    CAS  Google Scholar 

  17. Cheng K, Tian HZ, Zhao D, Lu L, Wang Y, Chen J, Liu XG, Jia WX, Huang Z (2014) Atmospheric emission inventory of cadmium from anthropogenic sources. Int J Environ Sci Technol 11(3):605–616

    CAS  Article  Google Scholar 

  18. Cho S-C, Chao Y-Y, Kao CH (2012) Calcium deficiency increases Cd toxicity and Ca is required for heat-shock induced Cd tolerance in rice seedlings. J Plant Physiol 169(9):892–898

    CAS  PubMed  Article  Google Scholar 

  19. Choi Y-E, Harada E (2005) Roles of calcium and cadmium on Cd-containing intra-and extracellular formation of Ca crystals in tobacco. J Plant Biol 48(1):113–119

    CAS  Article  Google Scholar 

  20. Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14(6):1347–1357

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. Dayod M, Tyerman SD, Leigh RA, Gilliham M (2010) Calcium storage in plants and the implications for calcium biofortification. Protoplasma 247(3–4):215–231

    CAS  PubMed  Article  Google Scholar 

  22. Degl’Innocenti E, Castagna A, Ranieri A, Guidi L (2014) Combined effects of cadmium and ozone on photosynthesis of Lycopersicon esculentum. Photosynthetica 52(2):179–185

    Article  CAS  Google Scholar 

  23. Deng G, Li M, Li H, Yin L, Li W (2014) Exposure to cadmium causes declines in growth and photosynthesis in the endangered aquatic fern (Ceratopteris pteridoides). Aquat Bot 112:23–32

    CAS  Article  Google Scholar 

  24. Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2012) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plan 35(4):1281–1289

    Article  CAS  Google Scholar 

  25. El-Beltagi HS, Mohamed HI (2013) Alleviation of cadmium toxicity in Pisum sativum L. seedlings by calcium chloride. Not Bot Hortic Agrobot 41(1):157–168

    CAS  Google Scholar 

  26. El-Enany AE (1995) Alleviation of cadmium toxicity on maize seedlings by calcium. Biol Plant 37(1):93–99

    CAS  Article  Google Scholar 

  27. Eller F, Brix H (2016) Influence of low calcium availability on cadmium uptake and translocation in a fast-growing shrub and a metal-accumulating herb. Aob Plants 8. doi:10.1093/aobpla/plv143

  28. Fagerberg B, Barregard L, Sallsten G, Forsgard N, Östling G, Persson M, Borné Y, Engström G, Hedblad B (2015) Cadmium exposure and atherosclerotic carotid plaques—results from the Malmö diet and Cancer study. Environ Res 136:67–74

    CAS  PubMed  Article  Google Scholar 

  29. Faller P, Kienzler K, Krieger-Liszkay A (2005) Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of photosystem II by competitive binding to the essential Ca2+ site. Biochim Biophys Acta 1706(1–2):158–164

    CAS  PubMed  Article  Google Scholar 

  30. Farzadfar S, Zarinkamar F, Modarres-Sanavy S, Hojati M (2013) Exogenously applied calcium alleviates cadmium toxicity in Matricaria chamomilla L. plants. Environ Sci Pollut Res 20(3):1413–1422

    CAS  Article  Google Scholar 

  31. Gallego SM, Benavídes MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121(2):151–159

    CAS  Article  Google Scholar 

  32. Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19(10):623–630

    CAS  PubMed  Article  Google Scholar 

  33. Gong X, Liu Y, Huang D, Zeng G, Liu S, Tang H, Zhou L, Hu X, Zhou Y, Tan X (2016) Effects of exogenous calcium and spermidine on cadmium stress moderation and metal accumulation in Boehmeria nivea (L.) Gaudich. Environ Sci Pollut Res 23:8699–8708

    CAS  Article  Google Scholar 

  34. Hashimoto K, Kudla J (2011) Calcium decoding mechanisms in plants. Biochimie 93(12):2054–2059

    CAS  PubMed  Article  Google Scholar 

  35. Hayakawa N, Tomioka R, Takenaka C (2011) Effects of calcium on cadmium uptake and transport in the tree species Gamblea innovans. Soil Sci Plant Nutr 57(5):691–695

    CAS  Article  Google Scholar 

  36. Hayat S, Ahmad A, Wani AS, Alyemeni MN, Ahmad A (2015) Regulation of growth and photosynthetic parameters by salicylic acid and calcium in Brassica juncea under cadmium stress. Z Naturforsch 69:452–458

    Article  CAS  Google Scholar 

  37. Heyno E, Klose C, Krieger-Liszkay A (2008) Origin of cadmium-induced reactive oxygen species production: mitochondrial electron transfer versus plasma membrane NADPH oxidase. New Phytol 179(3):687–699

    CAS  PubMed  Article  Google Scholar 

  38. Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136(1):2438–2442

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. Hochmal AK, Schulze S, Trompelt K, Hippler M (2015) Calcium-dependent regulation of photosynthesis. Biochim Biophys Acta 1847(9):993–1003

    CAS  PubMed  Article  Google Scholar 

  40. Hong Y, Yan S (2015) Cadmium transporters in the kidney and cadmium-induced nephrotoxicity. Int J Mol Sci 16(1):1484–1494

    Article  CAS  Google Scholar 

  41. Huang DL, Zeng GM, Feng CL, Hu S, Jiang XF, Tang L, Su FF, Zhang Y, Zeng W, Liu HL (2008) Degradation of lead-contaminated lignocellulosic waste by Phanerochaete chrysosporium and the reduction of lead toxicity. Environ Sci Technol 42:4946–4951

    CAS  PubMed  Article  Google Scholar 

  42. Huang DL, Wang RZ, Liu YG, Zeng GM, Lai C, XuP LuBA, Xu JJ, Wang C, Huang C (2015) Application of molecularly imprinted polymers in wastewater treatment: a review. Environ Sci Pollut Res 22(2):963–977

    CAS  Article  Google Scholar 

  43. Huang DL, Xue WJ, Zeng GM, Wan J, Chen GM, Huang C, Zhang C, Cheng M, Xu P (2016) Immobilization of Cd in river sediments by sodium alginate modified nanoscale zero-valent iron: impact on enzyme activities and microbial community diversity. Water Res 106:15–25

    CAS  PubMed  Article  Google Scholar 

  44. Huda KM, Banu MS, Tuteja R, Tuteja N (2013) Global calcium transducer P-type Ca2+-ATPases open new avenues for agriculture by regulating stress signalling. J Exp Bot 64(11):3099–3109

    CAS  PubMed  Article  Google Scholar 

  45. Iannelli MA, Pietrini F, Fiore L, Petrilli L, Massacci A (2002) Antioxidant response to cadmium in Phragmites australis plants. Plant Physiol Biochem 40(11):977–982

    CAS  Article  Google Scholar 

  46. Islam MM, Munemasa S, Hossain MA, Nakamura Y, Mori IC, Murata Y (2010) Roles of AtTPC1, vacuolar two pore channel 1. Arabidopsis stomatal closure. Plant Cell Physiol 51(2):302–311

    CAS  PubMed  Article  Google Scholar 

  47. Islam MS, Ahmed MK, Raknuzzaman M, Habibullah-Al-Mamun M, Islam MK (2015) Heavy metal pollution in surface water and sediment: a preliminary assessment of an urban river in a developing country. Ecol Indic 48:282–291

    CAS  Article  Google Scholar 

  48. Jarup L (2003) Hazards of heavy metal contamination. Brit Med Bull 68(1):167–182

    PubMed  Article  Google Scholar 

  49. Jiali H, Hong L, Jie L, Chaofeng M, Shaojun L, Long Q, Ying G, Xiangning J, Janz D, Polle A, Tyree M, Zhi-Bin L (2013) A transcriptomic network underlies microstructural and physiological responses to cadmium in Populus × canescens. Plant Physiol 162(1):424–439

    Article  CAS  Google Scholar 

  50. Jiang JH, Ge G, Gao K, Pang Y, Chai RC, Jia XH, Kong JG, Yu AC-H (2015) Calcium signaling involvement in cadmium-induced astrocyte cytotoxicity and cell death through activation of MAPK and PI3K/Akt signaling pathways. Neurochem Res 40(9):1929–1944

    CAS  PubMed  Article  Google Scholar 

  51. Jones RGW, Lunt OR (1967) The function of calcium in plants. Bot Rev 33(4):407–426

    CAS  Article  Google Scholar 

  52. Kärkönen A, Kuchitsu K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112:22–32

    PubMed  Article  CAS  Google Scholar 

  53. Kastori R, Petrović M, Petrović N (1992) Effect of excess lead, cadmium, copper, and zinc on water relations in sunflower. J Plant Nutr 15(11):2427–2439

    CAS  Article  Google Scholar 

  54. Kesseler A, Brand M (1995) The mechanism of the stimulation of state 4 respiration by cadmium in potato tuber (Solanum tuberosum) mitochondria. Plant Physiol Biochem 33(4):519–528

    CAS  Google Scholar 

  55. Kim YY, Yang YY, Lee Y (2002) Pb and Cd uptake in rice roots. Physiol Plant 116(3):368–372

    CAS  Article  Google Scholar 

  56. Kinraid TB (1998) Three mechanisms for the calcium alleviation of mineral toxicities. Plant Physiol 118(2):513–520

    Article  Google Scholar 

  57. Koptsik GN (2014) Problems and prospects concerning the phytoremediation of heavy metal polluted soils: a review. Eurasian Soil Sci 47(9):923–939

    CAS  Article  Google Scholar 

  58. Kováčik J (2013) Hyperaccumulation of cadmium in Matricaria chamomilla: a never-ending story? Acta Physiol Plant 35(5):1721–1725

    Article  CAS  Google Scholar 

  59. Kumar M, Kumari P, Gupta V, Anisha PA, Reddy CRK, Jha B (2010) Differential responses to cadmium induced oxidative stress in marine macroalga Ulva lactuca (Ulvales, Chlorophyta). Biometals 23(2):315–325

    CAS  PubMed  Article  Google Scholar 

  60. Kurtyka R, Małkowski E, Kita A, Karcz W (2008) Effect of Calcium and Cadmium on Growth and Accumulation of Cadmium, Calcium, Potassium and Sodium in Maize Seedlings. Polish J Environ Stud 17:51–56

  61. Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171(2):249–269

    CAS  PubMed  Article  Google Scholar 

  62. Lehmann S, Serrano M, L’Haridon F, Tjamos SE, Metraux J-P (2015) Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry 112:54–62

    CAS  PubMed  Article  Google Scholar 

  63. Li H, Liu Y, Zeng G, Zhou L, Wang X, Wang Y, Wang C, Hu X, Xu W (2014) Enhanced efficiency of cadmium removal by Boehmeria nivea (L.) Gaud. in the presence of exogenous citric and oxalic acids. J Environ Sci 26(12):2508–2516

    Article  Google Scholar 

  64. Li P, Zhao C, Zhang Y, Wang X, Wang X, Wang J, Wang F, Bi Y (2015a) Calcium alleviates cadmium-induced inhibition on root growth by maintaining auxin homeostasis in Arabidopsis seedlings. Protoplasma 253:185–200

    PubMed  Article  CAS  Google Scholar 

  65. Li S, Yang W, Yang T, Chen Y, Ni W (2015b) Effects of cadmium stress on leaf chlorophyll fluorescence and photosynthesis of Elsholtzia argyi—a cadmium accumulating plant. Int J Phytoremed 17(1):85–92

    CAS  Article  Google Scholar 

  66. Li X, Zhou Q, Sun X, Ren W (2016) Effects of cadmium on uptake and translocation of nutrient elements in different welsh onion (Allium fistulosum L.) cultivars. Food Chem 194:101–110

    CAS  PubMed  Article  Google Scholar 

  67. Liu Y, Xin W, Zeng G, Dan Q, Gu J, Ming Z, Chai L (2007) Cadmium-induced oxidative stress and response of the ascorbate–glutathione cycle in Bechmeria nivea (L.) Gaud. Chemosphere 69(1):99–107

    CAS  PubMed  Article  Google Scholar 

  68. Liu W, Shang S, Feng X, Zhang G, Wu F (2015) Modulation of exogenous selenium in cadmium-induced changes in antioxidative metabolism, cadmium uptake, and photosynthetic performance in the 2 tobacco genotypes differing in cadmium tolerance. Environ Toxicol Chem 34(1):92–99

    PubMed  Article  CAS  Google Scholar 

  69. López ML, Peralta-Videa JR, Benitez T, Gardea-Torresdey JL (2005) Enhancement of lead uptake by alfalfa (Medicago sativa) using EDTA and a plant growth promoter. Chemosphere 61(4):595–598

    PubMed  Article  CAS  Google Scholar 

  70. López ML, Peralta-videa JR, Parsons JG, Benitez T, Gardea-Torresdey JL (2007) Gibberellic acid, kinetin, and the mixture indole—3-acetic acid—kinetin assisted with EDTA-induced lead hyperaccumulation in alfalfa plants. Environ Sci Technol 41(23):8165–8170

    PubMed  Article  CAS  Google Scholar 

  71. Lopez-Climent MF, Arbona V, Perez-Clemente RM, Zandalinas SI, Gomez-Cadenas A (2013) Effect of cadmium and calcium treatments on phytochelatin and glutathione levels in citrus plants. Plant Biol 16(1):79–87

    PubMed  Article  CAS  Google Scholar 

  72. Luo J, Qi S, Peng L, Xie X (2015) Phytoremediation potential of cadmium-contaminated soil by Eucalyptus globulus under different coppice systems. Bull Environ Contam Toxicol 94(3):321–325

    CAS  PubMed  Article  Google Scholar 

  73. Marchetti C (2013) Role of calcium channels in heavy metal toxicity. ISRN Toxicol 2013:184360

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  74. Miqyass M, van Gorkom HJ, Yocum CF (2007) The PSII calcium site revisited. Photosynth Res 92(3):275–287

    CAS  PubMed  Article  Google Scholar 

  75. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410

    CAS  PubMed  Article  Google Scholar 

  76. Mleczek M, Kozlowska M, Kaczmarek Z, Chadzinikolau T, Golinski P (2012) Influence of Ca/Mg ratio on phytoextraction properties of Salix viminalis I. The effectiveness of Cd, Cu, Pb, and Zn bioaccumulation and plant growth. Int J Phytoremed 14(1):75–88

    Article  Google Scholar 

  77. Mohamed FI (2012) Protective effects of some antioxidant metals against chromosomal damage induced by cadmium in Vicia faba plants. Int J Agric Res 7:376–387

    Article  Google Scholar 

  78. Molinier J, Ramos C, Fritsch O, Hohn B (2004) CENTRIN2 modulates homologous recombination and nucleotide excision repair in arabidopsis. Plant Cell 16(6):1633–1643

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. Nedjimi B, Daoud Y (2009) Cadmium accumulation in Atriplex halimus subsp. schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. Flora Morphol Distrib Funct Ecol Plants 204(4):316–324

    Article  Google Scholar 

  80. Obata H, Umebayashi M (1997) Effects of cadmium on mineral nutrient concentrations in plants differing in tolerance for cadmium. J Plant Nutr 20(1):97–105

    CAS  Article  Google Scholar 

  81. Parvaiz A, Abdel LAA, Abd Allah EF, Abeer H, Maryam S, Anjum NA, Salih G (2016) Calcium and potassium supplementation enhanced growth, osmolyte secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Front Plant Sci 7:347

    Google Scholar 

  82. Perez-Chaca MV, RodrÍGuez-Serrano M, Molina AS, Pedranzani HE, Zirulnik F, Sandalio LM, Romero-Puertas MC (2014) Cadmium induces two waves of reactive oxygen species in Glycine max (L.) roots. Plant Cell Environ 37(7):1672–1687

    CAS  PubMed  Article  Google Scholar 

  83. Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32(32):539–548

    CAS  PubMed  Article  Google Scholar 

  84. Piterková J, Luhová L, Navrátilová B, Sedlářová M, Petřivalský M (2015) Early and long-term responses of cucumber cells to high cadmium concentration are modulated by nitric oxide and reactive oxygen species. Acta Physiol Plant 37(2):1–12

    Article  CAS  Google Scholar 

  85. Qiao Z, Jing T, Jin Z, Liang Y, Zhang L, Liu Z, Liu D, Pei Y (2016) CDPKs enhance Cd tolerance through intensifying H2S signal in Arabidopsis thaliana. Plant Soil 398(1–2):99–110

    CAS  Article  Google Scholar 

  86. Rahman A, Mostofa MG, Nahar K, Hasanuzzaman M, Fujita M (2016) Exogenous calcium alleviates cadmium-induced oxidative stress in rice (Oryza sativa L.) seedlings by regulating the antioxidant defense and glyoxalase systems. Braz J Bot 39(2):393–407

    Article  Google Scholar 

  87. Ramalho JC, Rebelo MC, Santos ME, Antunes ML, Nunes M (1994) Effects of calcium deficiency on Coffea arabica. Nutrient changes and correlation of calcium levels with some photosynthetic parameters. Plant Soil 172(1):87–96

    Article  Google Scholar 

  88. Rodriguez-Hernandez MC, Bonifas I, Alfaro-De la Torre MC, Flores-Flores JL, Bañuelos-Hernández B, Patiño-Rodríguez O (2015) Increased accumulation of cadmium and lead under Ca and Fe deficiency in Typha latifolia: a study of two pore channel (TPC1) gene responses. Environ Exp Bot 115:38–48

    CAS  Article  Google Scholar 

  89. Rodriguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueno MC, Del Rio LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150(1):229–243

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  90. Ruta LL, Popa VC, Nicolau I, Danet AF, Iordache V, Neagoe AD, Farcasanu IC (2014) Calcium signaling mediates the response to cadmium toxicity in Saccharomyces cerevisiae cells. FEBS Lett 588(17):3202–3212

    CAS  PubMed  Article  Google Scholar 

  91. Saed-Moucheshi A, Shekoofa A, Pessarakli M (2014) Reactive oxygen species (ROS) generation and detoxifying in plants. J Plant Nutr 37(10):1573–1585

    CAS  Article  Google Scholar 

  92. Sakan SM, Dević GJ, Relić DJ, Anđelković IB, Sakan NM, Đorđević DS (2015) Environmental assessment of heavy metal pollution in freshwater sediment, Serbia. Clean Soil Air Water 43(6):838–845

    CAS  Article  Google Scholar 

  93. Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109(4):1427–1433

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  94. Sasaki A, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24(5):2155–2167

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. Shahid M, Austruy A, Echevarria G, Arshad M, Sanaullah M, Aslam M, Nadeem M, Nasim W, Dumat C (2014) EDTA-enhanced phytoremediation of heavy metals: a review. Soil Sediment Contam 23(4):389–416

    CAS  Article  Google Scholar 

  96. Shi HP, Zhu YF, Wang YL, Tsang PK (2014) Effect of cadmium on cytogenetic toxicity in hairy roots of Wedelia trilobata L. and their alleviation by exogenous CaCl2. Environ Sci Pollut Res Int 21(2):1436–1443

    CAS  PubMed  Article  Google Scholar 

  97. Siddiqui MH, Al-Whaibi MH, Sakran AM, Basalah MO, Ali HM (2012) Effect of calcium and potassium on antioxidant system of Vicia faba L. under cadmium stress. Int J Mol Sci 13(6):6604–6619

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. Singh A, Prasad SM (2014) Remediation of heavy metal contaminated ecosystem: an overview on technology advancement. Int J Environ Sci Technol 12(1):353–366. doi:10.1007/s13762-014-0542-y

    Article  CAS  Google Scholar 

  99. Skórzyńska-Polit E, Tukendorf A, Selstam E, Baszyński T (1998) Calcium modifies Cd effect on runner bean plants. Environ Exp Bot 40(3):275–286

    Article  Google Scholar 

  100. Spirlandeli AL, Deminice R, Jordao AA (2014) Plasma malondialdehyde as biomarker of lipid peroxidation: effects of acute exercise. Int J Sports Med 35(1):14–18

    CAS  PubMed  Google Scholar 

  101. Srivastava RK, Pandey P, Rajpoot R, Rani A, Gautam A, Dubey RS (2015) Exogenous application of calcium and silica alleviates cadmium toxicity by suppressing oxidative damage in rice seedlings. Protoplasma 252(4):959–975

    CAS  PubMed  Article  Google Scholar 

  102. Steinhorst L, Kudla J (2014) Signaling in cells and organisms—calcium holds the line. Curr Opin Plant Biol 22:14–21

    CAS  PubMed  Article  Google Scholar 

  103. Stockinger EJ, Skinner JS, Gardner KG, Francia E, Pecchioni N (2007) Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J 51(2):308–321

    CAS  PubMed  Article  Google Scholar 

  104. Stravinskienė V, Račaitė M (2014) Impact of cadmium and zinc on the growth of white clover (Trifolium repens L.) shoots and roots. Pol J Environ Stud 23(4):1355–1359

    Google Scholar 

  105. Suzuki N (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnol 22(1):19–25

    CAS  Article  Google Scholar 

  106. Talukdar D (2012) Exogenous calcium alleviates the impact of cadmium-induced oxidative stress in Lens culinaris Medic. seedlings through modulation of antioxidant enzyme activities. J Crop Sci Biotechnol 15(4):325–334

    Article  Google Scholar 

  107. Tang H, Liu Y, Gong X, Zeng G, Zheng B, Wang D, Sun Z, Zhou L, Zeng X (2015) Effects of selenium and silicon on enhancing antioxidative capacity in ramie (Boehmeria nivea (L.) Gaud.) under cadmium stress. Environ Sci Pollut Res 22(13):9999–10008

    CAS  Article  Google Scholar 

  108. Tian S, Lu L, Zhang J, Wang K, Brown P, He Z, Liang J, Yang X (2011) Calcium protects roots of Sedum alfredii H. against cadmium-induced oxidative stress. Chemosphere 84(1):63–69

    CAS  PubMed  Article  Google Scholar 

  109. Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37(1):1–13

    CAS  Google Scholar 

  110. Wan G, Najeeb U, Jilani G, Naeem MS, Zhou W (2011) Calcium invigorates the cadmium-stressed Brassica napus L. plants by strengthening their photosynthetic system. Environ Sci Pollut Res 18(9):1478–1486

    CAS  Article  Google Scholar 

  111. Wang CL, Liu YG, Zeng GM, Xin-Jiang HU, Ying YC, Xi HU, Zhou L, Wang YQ, Hua-Ying LI (2014) Mechanism of exogenous selenium alleviates cadmium induced toxicity in Bechmeria nivea (L.) Gaud (Ramie). Trans Nonferr Metal Soc 24(12):3964–3970

    CAS  Article  Google Scholar 

  112. Wang D, Liu Y, Tan X, Liu H, Zeng G, Hu X, Jian H, Gu Y (2015) Effect of exogenous nitric oxide on antioxidative system and S-nitrosylation in leaves of Boehmeria nivea (L.) Gaud under cadmium stress. Environ Sci Pollut Res 22(5):3489–3497

    CAS  Article  Google Scholar 

  113. Xu P, Liu L, Zeng G, Huang D, Lai C, Zhao M, Huang C, Li N, Wei Z, Wu H, Zhang C, Lai M, He Y (2014) Heavy metal-induced glutathione accumulation and its role in heavy metal detoxification in Phanerochaete chrysosporium. Appl Microbiol Biotechnol 98(14):6409–6418

    CAS  PubMed  Article  Google Scholar 

  114. Xu P, Zeng G, Huang D, Dong H, Lai C, Chen M, Tang W, Li F, Leng Y, Cheng M, He X, He Y (2015) Cadmium induced hydrogen peroxide accumulation and responses of enzymatic antioxidants in Phanerochaete chrysosporium. Ecol Eng 75:110–115

    Article  Google Scholar 

  115. Yang CM, Juang KW (2015) Alleviation effects of calcium and potassium on cadmium rhizotoxicity and absorption by soybean and wheat roots. J Plant Nutr Soil Sci 178(5):748–754

    CAS  Article  Google Scholar 

  116. Yang J, Kim E-C, Shin D-C, Jo S-J, Lim Y-W (2015a) Human exposure and risk assessment of cadmium for residents of abandoned metal mine areas in Korea. Environ Geochem Health 37(2):321–332

    CAS  PubMed  Article  Google Scholar 

  117. Yang X, Duan J, Wang L, Li W, Guan J, Beecham S, Mulcahy D (2015b) Heavy metal pollution and health risk assessment in the Wei River in China. Environ Monit Assess 187(3):1–11

    Google Scholar 

  118. Zhang W, Zhou R-G, Gao Y-J, Zheng S-Z, Xu P, Zhang S-Q, Sun D-Y (2009) Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in arabidopsis. Plant Physiol 149(4):1773–1784

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  119. Zhang L, Chen Z, Zhu C (2012) Endogenous nitric oxide mediates alleviation of cadmium toxicity induced by calcium in rice seedlings. J Environ Sci 24(5):940–948

    CAS  Article  Google Scholar 

  120. Zhang SJ, Li TX, Huang HG, Zhang XZ, Yu HY, Zheng ZC, Wang YD, Zou TJ, Hao XQ, Pu Y (2014a) Phytoremediation of cadmium using plant species of Athyrium wardii (Hook.). Int J Environ Sci Technol 11(3):757–764

    CAS  Article  Google Scholar 

  121. Zhang X, Gao B, Xia H (2014b) Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of bana grass and vetiver grass. Ecotox Environ Safe 106:102–108

    CAS  Article  Google Scholar 

  122. Zhang M, Zhang J, Lu LL, Zhu ZQ, Yang XE (2015) Functional analysis of CAX2-like transporters isolated from two ecotypes of Sedum alfredii. Biol Plant 60(1):37–47

    Article  CAS  Google Scholar 

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Acknowledgements

This article was financially supported by the Program for the National Natural Science Foundation of China (51579098, 51378190, 51278176, 51408206, 51521006), the National Program for Support of Top-Notch Young Professionals of China (2014), the Program for New Century Excellent Talents in University (NCET-13-0186), the Program for Changjiang Scholars and Innovative Research Team in University (IRT-13R17), Scientific Research Fund of Hunan Provincial Education Department (No. 521293050) and Hunan Provincial Science and Technology Plan Project (No. 2016RS3026).

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Correspondence to Danlian Huang or Yunguo Liu.

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Huang, D., Gong, X., Liu, Y. et al. Effects of calcium at toxic concentrations of cadmium in plants. Planta 245, 863–873 (2017). https://doi.org/10.1007/s00425-017-2664-1

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Keywords

  • Metal accumulation
  • Oxidative stress
  • Photosynthesis
  • Signal transduction