Abstract
One of the major reasons why cadmium is toxic in plants is because it disturbs their nutrient balance. The aim of this work is to investigate the effects of cadmium (Cd) and/or silicon (Si) on the nutrient status of poplar callus cells after 3 and after 9 weeks of Cd exposure and to study its possible relationship with the changes in the fresh and dry mass, the plasma membrane integrity, and cadmium tolerance patterns. A principal component analysis (PCA) was performed to reveal the associations among the elements, and the variability between both treatments, and between the 3- and 9-week stages. Cadmium reduced the fresh and dry mass, the plasma membrane integrity, and the concentration of all nutrients except for P. After 9 weeks of exposure, the Cd concentration in callus cells had almost doubled, in spite of an improvement in all studied parameters. These changes may be due to the callus acclimatizing to the Cd stress. In the Cd + Si treatment, the fresh and dry mass, the plasma membrane integrity, and the concentration of nutrients, as well as the growth tolerance index, increased in comparison with the Cd treatment. We assumed that the enhancement in the plasma membrane integrity mediated by Si under Cd stress had caused the improvement in the uptake of nutrients and, consequently, the fresh and dry mass of callus cells had increased. The reduction in Cd concentration due to the Si impact also contributed to the increase in fresh and dry mass.
Similar content being viewed by others
References
Abdi H, Williams LJ (2010) Principal component analysis. WIREs Comp Stat 2:433–459. https://doi.org/10.1002/wics.101
Adrees M, Ali S, Rizwan M, Zia-ur-Rehman M, Ibrahim M, Abbas F, Farid M, Qayyum F, Irshad MK (2015) Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: A review. Ecotox Environ Safe 119:186–197. https://doi.org/10.1016/j.ecoenv.2015.05.011
Amiri J, Enteshary S, Delavary K (2011) The effect of silicon on membrane integrity and antioxidative pigments on Echium amoenum that exposed to cadmium stress. Planta Med 77-PI5. https://doi.org/10.1055/s-0031-1282598
Azevedo H, Pinto CGG, Santos C (2005a) Cadmium effects in sunflower: nutritional imbalances in plants and calluses. J Plant Nutr 28:2221-2231 https://doi.org/10.1080/01904160500324808
Azevedo H, Pinto CGG, Santos C (2005b) Cadmium effects in sunflower: membrane permeability and changes in catalase and peroxidase activity in leaves and calluses. J Plant Nutr 28:2233–2241. https://doi.org/10.1080/01904160500324816
Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34. https://doi.org/10.1590/S1677-04202005000100003
Bokor B, Vaculík V, Slováková Ľ, Masarovič D, Lux A (2014) Silicon does not always mitigate zinc toxicity in maize. Acta Physiol Plant 36:733–743. https://doi.org/10.1007/s11738-013-1451-2
Bolan NS, Adriano DC, Mani S, Duraisamy P, Arulmozhiselvan S (2003) Immobilization and phytoavailability of cadmium in variable charge soils: I. Effect of phosphate addition. Plant Soil 250:83–94. https://doi.org/10.1023/A:1022826014841
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719. https://doi.org/10.1016/j.biochi.2006.07.003
Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99. https://doi.org/10.1016/j.tplants.2012.08.003
Diaz-Colon JD, Bonny RW, Dawis FS, Bauer JR (1972) Comparative effects and concentrations of Picloran, 2,4,5-T and Dicamba in tissues culture. Physiol Plant 27:60–64. https://doi.org/10.1111/j.1399-3054.1972.tb01137.x
Ekmekçi Y, Tanyolaç D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611. https://doi.org/10.1016/j.jplph.2007.01.017
Emamverdian A, Ding Y, Xie Y, Sangari S (2018) Silicon mechanisms to ameliorate heavy metal stress in plants. Biomed Res Int 2018:8492898. https://doi.org/10.1155/2018/8492898
Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z (2013) Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotox Environ Safe 96:242–249. https://doi.org/10.1016/j.ecoenv.2013.07.006
Golan-Goldhirsh A, Barazani O, Nepovim A, Soudek P, Smrcek S, Dufkova L, Krenkova S, Yrjala K, Schröder P, Vanek T (2005) Plant response to heavy metals and organic pollutants in cell culture and at whole plant level. J Soils Sediments 4:133–140. https://doi.org/10.1007/BF02991058
Gong HJ, Randall DP, Flowers TJ (2006) Silicon deposition in the root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow. Plant Cell Environ 29:1970–1979 https://doi.org/10.1111/j.1365-3040.2006.01572.x
Greger M, Landberg T, Vaculík M (2018) Silicon influences soil availability and accumulation of mineral nutrients in various plant species. Plants 7:41. https://doi.org/10.3390/plants7020041
Gussarson M, Jensen P (1992) Effects of copper and cadmium on uptake and leakage of K+ in birch (Betula pendula) roots. Tree Physiol 11:305–313. https://doi.org/10.1093/treephys/11.3.305
Hannan F, Ali S, Ahmad R, Rizwan M, Iqbal M, Rizvi H, Zia-ur-Rehman M (2016) Silicon and cadmium toxicity in plants: an overview. In: Tripathi DK, Singh VP, Ahmad P, Chauhan DK, Prasad SM (eds) Silicon in plants, advances and future prospects. Taylor and Francis Group, Boca Raton, pp 245–264
Hasan SA, Fariduddin Q, Ali B, Hayat S, Ahmad A (2009) Cadmium: toxicity and tolerance in plants. J Environ Biol 30:165–174
Hattab S, Dridi B, Chouba L, Kheder MB, Bousetta H (2009) Photosynthesis and growth responses of pea Pisum sativum L. under heavy metals stress. J Environ Sci 21:1552–1556. https://doi.org/10.1016/S1001-0742(08)62454-7
Huang D, Gong X, Liu Y, Zeng G, Lai C, Bashir H, Zhou L, Wang D, Xu P, Cheng M, Wan J (2017) Effects of calcium at toxic concentrations of cadmium in plants. Planta 245:863–873. https://doi.org/10.1007/s00425-017-2664-1
Kaya C, Tuna LA, Sonmez O, Ince F, Higgs D (2009) Mitigation effects of silicon on maize plants grown at high zinc. J Plant Nutr 32:1788–1798. https://doi.org/10.1080/01904160903152624
Küpper H, Andresen E (2016) Mechanisms of metal toxicity in plants. Metallomics 8:269–285. https://doi.org/10.1039/c5mt00244c
Küpper H, Küpper F, Spiller M (1998) In situ detection of heavy metal substituted chlorophylls in water plants. Photosynth Res 58:123–133. https://doi.org/10.1023/A:1006132608181
Lux A, Masarovičová E, Lišková D, Kráľová K, Varga L (2000) Study of woody plants utilizable for phytoremediation in Slovakia. 379-391. Ecosystem Service and Sustainable Watershed Management in North China International Conference, Beijing, P.R. China
May MJ, Vernoux T, Leaver C, Van Montagu M, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667. https://doi.org/10.1093/jxb/49.321.649
Mehrabanjoubani P, Abdolzadeh A, Sadeghipour HR, Aghdasi M (2015) Silicon affects transcellular and apoplastic uptake of some nutrients in plants. Pedosphere 25:192–201. https://doi.org/10.1016/S1002-0160(15)60004-2
Nazar R, Iqbal N, Masood A, Khan MIR, Khan N (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489. https://doi.org/10.4236/ajps.2012.310178
Neumann D, zur Nieden U (2001) Silicon and heavy metal tolerance of higher plants. Phytochemistry 56:685–692. https://doi.org/10.1016/S0031-9422(00)00472-6
Obata H, Umebayashi M (1997) Effects of cadmium on mineral nutrient concentrations in plants differing in tolerance for cadmium. J Plant Nutr 20:97–105. https://doi.org/10.1080/01904169709365236
Rezvani M, Zaefarian F, Miransari M, Nematzadeh GA (2011) Uptake and translocation of cadmium and nutrients by Aeluropus littoralis. Arch Agron Soil Sci 58:1413–1425. https://doi.org/10.1080/03650340.2011.591385
Roosta HR, Estaji A, Niknam F (2018) Effect of iron, zinc and manganese shortage-induced change on photosynthetic pigments, some osmoregulators and chlorophyll fluorescence parameters in lettuce. Photosynthetica 56:606–615. https://doi.org/10.1007/s11099-017-0696-1
Salt DE, Rauser WE (1995) MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol 107:1293–1301. https://doi.org/10.1104/pp.107.4.1293
Sarwar N, Saifullah MSS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937. https://doi.org/10.1002/jsfa.3916
Shao G, Chen M, Wang W, Mou R, Zhang G (2007) Iron nutrition affects cadmium accumulation and toxicity in rice plants. Plant Growth Regul 53:33–42. https://doi.org/10.1007/s10725-007-9201-3
Shekhawat GS, Verma K, Jana S, Singh K, Teotia P, Prasad A (2010) In vitro biochemical evaluation of cadmium tolerance mechanism in callus and seedlings of Brassica juncea. Protoplasma 239:31–38. https://doi.org/10.1007/s00709-009-0079-y
Shi Y, Zhang Y, Han W, Feng R, Hu Y, Guo J, Gong H (2016) Silicon enhances water stress tolerance by improving root hydraulic conductance in Solanum lycopersicum L. Front Plant Sci 7:196. https://doi.org/10.3389/fpls.2016.00196
Shirazi SS, Ronaghi AM, Karimian N, Yasrebi J, Emam Y (2012) Influence of cadmium toxicity on nitrogen and phosphorus uptake and some vegetative growth parameters in shoot of seven rice cultivars. J Sci Technol Greenhouse Cult 3:107–118
Singh UM, Sareen P, Sengar RS, Kumar A (2013) Plant ionomics: a newer approach to study mineral transport and its regulation. Acta Physiol Plant 35:2641–2653. https://doi.org/10.1007/s11738-013-1316-8
Singh VP, Tripathi DK, Kumar D, Chauhan DK (2011) Influence of exogenous silicon addition on aluminium tolerance in rice seedlings. Biol Trace Elem Res 144:1260–1274. https://doi.org/10.1007/s12011-011-9118-6
Solti A, Gáspár L, Mészáros I, Szigeti Z, Lévai L, Sárvári E (2008) Impact of iron supply on the kinetics of recovery of photosynthesis in Cd-stressed poplar (Populus glauca). Ann Bot 102:771–782. https://doi.org/10.1093/aob/mcn160
Sun JY, Shen ZG (2007) Effects of Cd stress on photosynthetic characteristics and nutrient uptake of cabbages with different Cd-tolerance. Ying Yong Sheng Tai Xue Bao 18:2605–2610 (in Chinese)
Tripathi DK, Singh VP, Prasad SM, Chauhan DK, Dubey NK (2015) Silicon nanoparticles (SiNp) alleviate chromium (VI) phytotoxicity in Pisum sativum (L.) seedlings. Plant Physiol Biochem 96:189–198. https://doi.org/10.1016/j.plaphy.2015.07.026
Tsyganov V, Belimov A, Borisov AY, Safronova V, Georgi M, Dietz K-J, Tikhonovich IA (2007) A chemically induced new pea (Pisum sativum) mutant SGECd with increased tolerance to, and accumulation of, cadmium. Ann Bot 99:227–237. https://doi.org/10.1093/aob/mcl261
Vatehová Z, Kollárová K, Zelko I, Richterová-Kučerová D, Bujdoš M, Lišková D (2012) Interaction of silicon and cadmium in Brassica juncea and Brassica napus. Biologia 67:498–504. https://doi.org/10.2478/s11756-012-0034-9
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372. https://doi.org/10.1016/j.pbi.2009.05.001
Wang S, Wang F, Gao S (2015) Foliar application with nano-silicon alleviates Cd toxicity in rice seedlings. Environ Sci Pollut Res 22:2837–2845. https://doi.org/10.1007/s11356-014-3525-0
Wang H, Wang PF, Zhang H (2010) Use of phosphorus to alleviate stress induced by cadmium and zinc in two submerged macrophytes. Afr J Biotechnol 8:2176–2183
Wiszniewska A, Hanus-Fajerska E, Muszyńska E, Smoleń S (2017) Comparative assessment of response to cadmium in heavy metal-tolerant shrubs cultured in vitro. Water Air Soil Pollut 228:304. https://doi.org/10.1007/s11270-017-3488-0
Xue ZC, Gao HY, Zhang LT (2013) Effects of cadmium on growth, photosynthetic rate and chlorophyll content in leaves of soybean seedlings. Biol Plant 57:587–590. https://doi.org/10.1007/s10535-013-0318-0
Zayed A, Gowthaman S, Terry N (1998) Phytoaccumulation of trace elements by wetland plants: I Duckweed. J Environ Qual 27:715–721. https://doi.org/10.2134/jeq1998.00472425002700030032x
Zhang X, Zhang W, Lang D, Cui J, Li Y (2018) Silicon improves salt tolerance of Glycyrrhiza uralensis Fisch. by ameliorating osmotic and oxidative stresses and improving phytohormonal balance. Environ Sci Pollut Res 25:25916–25932. https://doi.org/10.1007/s11356-018-2595-9
Funding
This work was financially supported by the Scientific Grant Agency of the Ministry of Education of the Slovak Republic and the Academy of Sciences VEGA no. 2/0105/18.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 14 kb)
Rights and permissions
About this article
Cite this article
Kučerová, D., Labancová, E., Vivodová, Z. et al. The modulation of ion homeostasis by silicon in cadmium treated poplar callus cells. Environ Sci Pollut Res 27, 2857–2867 (2020). https://doi.org/10.1007/s11356-019-07054-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-07054-1