Abstract
The objective of this study was to assess the effect of different Cd and Si concentrations on the maize plants. The following Cd and/or Si treatments were used: 5 Cd; 10 Cd; 100 Cd; 5 Cd + 0.08 Si; 10 Cd + 0.08 Si; 100 Cd + 5 Si treatments (Cd concentration in μM, Si concentration in mM). The plant growth, photosynthetic pigments content, antioxidant enzymes activities (POX, SOD, CAT), Cd and Si accumulation, translocation and cell wall deposition of the maize plants was observed. Changes in the endodermal cell walls development and late metaxylem elements lignification due to Cd and/or Si treatment were also evaluated. The negative effect of Cd (5 and 10 μM) on the growth parameters was alleviated by Si at 0.08 mM. The positive effect of Si was not observed at higher Cd and Si concentrations. This indicates that the alleviating effect of Si on Cd toxicity depends on the Cd and Si concentrations. Plants responded to Cd toxicity by an increase of antioxidant enzyme activity. Silicon addition in Cd + Si treatment stimulated an increase in the activity of antioxidant enzymes in comparison with the Cd treatment. Chlorophyll and carotenoid content in the Cd treated plants was not significantly affected by Si. The young maize plants retained much more Cd in their roots as they translocated into the shoots. 5 Cd + 0.08 Si and 10 Cd + 0.08 Si treatments correlated with an increase in Cd concentration in the roots and shoots, and in the cell walls. Silicon caused a slight decrease of the Cd translocation into the shoots in 5 Cd + 0.08 Si and 10 Cd + 0.08 Si treatments. Negative correlation between the root Cd cell wall deposition and Cd translocation was observed. Cadmium and/or Si altered root anatomy. Cadmium enhanced suberin lamellae development and late metaxylem lignification; silicon in Cd + Si treatments accelerated suberin lamellae deposition and enhanced the tertiary endodermal cell walls formation in comparison with Cd treatments. Negative correlation between the endodermal cell walls development and Cd translocation was observed.
Similar content being viewed by others
References
Alscher G, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341
Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principles of protein-dye-binding. Ann Biochem 72:248–254
Cataldo CD, Garland TR, Wildung RE (1983) Cadmium uptake, kinetics in intact soybean plants. Plant Physiol 73:844–848
Chaneva G, Parvanova P, Tzvetkova N, Uzunova A (2010) Photosynthetic response of maize plants against cadmium and Paraquat impact. Water Air Soil Pollut 208:287–293
Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) CRS handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 283–284
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochemie 88:1707–1719
Ďurčeková K, Huttová J, Mistrík I, Olle M, Tamás L (2007) Cadmium induces premature xylogenesis in barley roots. Plant Soil 290:61–68
Ekmekçi Y, Tanyolac 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
Epstein E (1994) The anomaly of silicon in plant biology. Proc Natl Acad Sci USA 91:11–17
Feng J, Shi Q, Wang X, Wei M, Yang F, Xu H (2010) Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic 123:521–530
Frič F, Fuchs WH (1970) Veränderungen der Aktivität einiger enzyme im Weizenblatt in Abhängigkeit von Puccinia graministritici. Phytopathol 67:161–174
Fu X, Dou Ch, Chen Y, Chen X, Shi J, Yu M, Xu J (2011) Subcellular distribution and chemical forms of cadmium in Phytolacca americana L. J Hazard Mater 186:103–107
Greger M, Landberg T, Lux A, Singh BR (2011) Influence of Si on Cd uptake and accumulation in wheat. Proceedings of the 5th international conference on silicon in agriculture, Beijing, China, September 13–18, 2011
Guo ZG, Liu HX, Tian FP, Zhang ZH, Wang SM (2006) Effect of silicon on the morphology of shoots and roots of alfalfa (Medicago sativa). Aust J Exp Agric 46:1161–1166
Gzyl J, Rymer K, Gwozdz A (2009) Differential response of antioxidant enzymes to cadmium stress in tolerant and sensitive cell line of cucumber (Cucumis sativus L.). Acta Biochim Pol 56:723–727
Harkin JM, Obst JR (1973) Lignification in trees: indication of exclusive peroxidase participation. Science 180:296–298
Hattori T, Inanaga S, Tanimoto E, Lux A, Luxová M, Sugimoto Y (2003) Silicon—induced changes in viscoelastic properties of sorghum root cell walls. Plant Cell Physiol 44:743–749
Hodges DM, Andrews CJ, Johnson DA, Hamilton RI (1997) Antioxidant enzyme and compound responses to chilling stress and their combining abilities in differentially sensitive maize hybrids. Crop Sci 37:857–863
Kim YH, Kim CY, Song WK, Park DS, Kwon SY, Lee HS, Bang JW, Kwak SS (2008) Overexpression of sweetpotato swpa4 peroxidase results in increased hydrogen peroxide production and enhances stress tolerance in tobacco. Planta 227:867–881
Kollárová K, Vatehová Z, Slováková L, Lišková D (2010) Interaction of galactoglucomannan oligosaccharides with auxin in mung bean primary root. Plant Physiol Biochem 48:401–406
Kummerová M, Zezulka Š, Kráľová K, Masarovičová E (2010) Effect of zinc and cadmium on physiological and production characteristics in Matricaria recutita. Biol Plant 2:308–314
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lagrimini LM (1991) Wound-induced deposition of polyphenols in transgenic plants overexpressing peroxidase. Plant Physiol 96:577–583
Liang YC, Wong JWC, Wei L (2005) Silicon-mediated enhancement of cadmium tolerance in maize (Zea mays L.) grown in cadmium contaminated soil. Chemosphere 58:475–483
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382
Liu J, Qian M, Cai G (2007) Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain. J Hazard Mater 143:443–447
Lukačová Kuliková Z, Lux A (2010) Silicon influence on maize, Zea mays L., hybrids exposed to cadmium treatment. Bull Environ Contam Toxicol 85:243–250
Lux A, Luxová M, Abe J, Tanimoto E, Hattori T, Inanaga S (2003) The dynamics of silicon deposition in the sorghum root endodermis. New Phytol 158:437–441
Lux A, Šottníková A, Opatrná J, Greger M (2004) Differences in structure of adventitious roots in Salix clones with contrasting characteristics of cadmium accumulation and sensitivity. Physiol Plant 120:537–545
Lux A, Morita S, Abe J, Ito K (2005) An improved method for clearing and staining free-hand sections and whole-mount samples. Ann Bot 96:989–996
Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37
Madamanchi NR, Donahue JL, Cramer CL, Alscher RG, Pedersen K (1994) Differential response of Cu, Zn superoxide dismutases in two pea cultivars during a short-term exposure to sulphur dioxide. Plant Mol Biol 26:95–103
Martinka M, Lux A (2004) Response of roots of three populations of Silene dioica to cadmium treatment. Biologia 59:185–189
Masarovič D, Slováková Ľ, Bokor B, Bujdoš M, Lux A (2012) Effect of silicon application on Sorghum bicolor exposed to toxic concentration of zinc. Biologia. doi:10.2478/s11756-012-0054-5
Masarovičová E, Cicák A, Štefančík I (1999) Plant responses to air pollution and heavy metal stresses. In: Pessarakli M (ed) Handbook of plant and crop stress, 2nd edn, Marcel Dekker, New York, Basel, pp 569–598
Matoh T, Ishigaki K, Ohno K, Azuma J (1993) Isolation and characterization of boron–polysaccharide complex from radish roots. Plant Cell Physiol 34:639–642
Neuman D, zur Neiden U (2001) Silicon and heavy metal tolerance of higher plants. Phytochemistry 56:685–692
Olmos E, Martinez-Solano JR, Piqueras A, Hellín E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). J Exp Bot 54:291–301
Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540
Pavlovič A, Masarovičová E, Kráľová K, Kubová J (2006) Response of chamomile plants (Matricaria recutita L.) to cadmium treatment. Bull Environ Contam Toxicol 77:763–771
Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. Plant Physiol 133:830–837
Piršelová B, Kuna R, Libantová J, Moravčíková J, Matušíková I (2011) Biochemical and physiological comparison of heavy metal-triggered defense responses in the monocot maize and dicot soybean roots. Mol Biol Rep 38:3437–3446
Redjala T, Zelko I, Sterckeman T, Legué V, Lux A (2011) Relationship between root structure and root cadmium uptake in maize. Environ Exp Bot 71:241–248
Schreiber L (2010) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15:546–553
Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127:887–898
Seregin IV, Shpigun LK, Ivanov VB (2004) Distribution and toxic effects of cadmium and lead on maize roots. Russ J Plant Physiol 51:525–533
Shi X, Chaochun Z, Wang H, Zhang F (2005) Effect of Si on the distribution of Cd in rice seedlings. Plant Soil 272:53–60
Shi X, Quingsheng C, Liu C (2010) Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. Plant Growth Regul 61:45–52
Šimonová E, Henselová M, Masarovičová E, Kohanová J (2007) Comparison of tolerance of Brassica juncea and Vigna radiata to cadmium. Biol Plant 51:488–492
Sobkowiak R, Rymer K, Rucińska R, Deckert J (2004) Cadmiuminduced changes in antioxidant enzymes in suspension culture of soybean cells. Acta Biochim Pol 51:219–222
Song A, Li Z, Zhanga J, Xueb G, Fanb F, Liang Y (2009) Silicon-enhanced resistance to cadmium toxicity in Brassica chinensis L. is attributed to Si-suppressed cadmium uptake and transport and Si-enhanced antioxidant defense capacity. J Hazard Mater 172:74–83
Vaculík M, Lux A, Luxová M, Tanimoto E, Lichtscheidl I (2009) Silicon mitigates cadmium inhibitory effects in young maize plants. Environ Exp Bot 67:52–58
Vaculík M, Landberg T, Greger M, Luxová M, Stoláriková M, Lux A (2012) Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize plants. Ann Bot 110:433–443
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
Vázquez S, Fernandez-Pascaul M, Sanchez-Pardo B, Carpena RO, Zornoza P (2007) Subcellular compartmentalisation of cadmium in white lupine determined by energy-dispersive X-ray microanalysis. J Plant Physiol 164:1235–1238
Wagner JG (1993) Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51:173–210
Wang L, Wang W, Chen Q, Cao W, Li M, Zhang F (2000) Silicon—induced cadmium tolerance of rice seedlings. J Plant Nutr 23:1397–1406
Weigel HJ, Jäger HJ (1980) Subcellular distribution and chemical form of cadmium in bean plants. Plant Physiol 65:480–482
White PJ (2001) The pathways of calcium movement to the xylem. J Exp Bot 52:891–899
Wierzbicka MH, Przedpełska E, Ruzik R, Ouerdane L, Połeć-Pawlak K, Jarosz M, Szpunar J, Szakiel A (2007) Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma 231:99–111
Young AJ (1991) The photoprotective role of carotenoids in higher plants. Physiol Plant 83:702–708
Zelko I, Lux A (2004) Effect of cadmium on Karwinskia humboldtiana roots. Biologia 59:205–209
Zhang CH, Wang L, Nie Q, Zhang W, Zhang F (2008) Long-term effects of exogenous silicon on cadmium translocation and toxicity in rice (Oryza sativa L.). Environ Exp Bot 62:300–307
Zornoza P, Vázquez S, Esteban E, Fernández-Pascual M, Carpena R (2002) Cadmium—stress in nodulated white lupin: strategies to avoid toxicity. Plant Physiol Biochem 40:1003–1009
Acknowledgments
The work was supported by Slovak Research and Development Agency under the contract Nr. APVV-0140-10, COST 0004-06 and APVV SK-FR-0020-11; by Grant VEGA 1/0817/12 and is a part of COST FA 0905 Action. Especially we thank to Dipl. Ing. B. Rysava, Ph.D., Sempol spol. s.r.o. for providing seeds of Zea mays hybrids.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lukačová, Z., Švubová, R., Kohanová, J. et al. Silicon mitigates the Cd toxicity in maize in relation to cadmium translocation, cell distribution, antioxidant enzymes stimulation and enhanced endodermal apoplasmic barrier development. Plant Growth Regul 70, 89–103 (2013). https://doi.org/10.1007/s10725-012-9781-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-012-9781-4