Skip to main content

Advertisement

SpringerLink
Log in

Silicon alleviates Cd stress of wheat seedlings (Triticum turgidum L. cv. Claudio) grown in hydroponics

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

We investigated the potential role of silicon in improving tolerance and decreasing cadmium (Cd) toxicity in durum wheat (Triticum turgidum L. durum) either through a reduced Cd uptake or exclusion/sequestration in non-metabolic tissues. For this, plants were grown in hydroponic conditions for 10 days either in presence or absence of 1 mM Si and for 11 additional days in various Cd concentrations (0, 0.5, 5.0 and 50 μM). After harvesting, morphological and physiological parameters as well as elemental concentrations were recorded. Cadmium caused reduction in growth parameters, photosynthetic pigments and mineral nutrient concentrations both in shoots and roots. Shoot and root contents of malate, citrate and aconitate increased, while contents of phosphate, nitrate and sulphate decreased with increasing Cd concentrations in plants. Addition of Si to the nutrient solution mitigated these adverse effects: Cd concentration in shoots decreased while concentration of Cd adsorbed at the root cell apoplasmic level increased together with Zn uptake by roots. Overall, total Cd uptake decreased in presence of Si. There was no co-localisation of Cd and Si either at the shoot or at the root levels. No Cd was detected in leaf phytoliths. In roots, Cd was mainly detected in the cortical parenchyma and Si at the endodermis level, while analysis of the outer thin root surface of the plants grown in the 50 μM Cd + 1 mM Si treatment highlighted non-homogeneous Cd and Si enrichments. These data strongly suggest the existence of a root localised protection mechanism consisting in armoring the root surface by Si- and Cd-bearing compounds and in limiting root–shoot translocation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Adrees M, Ali S, Rizwan M, Rehman MZ, Ibrahim M, Abbas F, Farid M, Qayyum MK, Irshad MK (2015) Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol Environ Saf 119:186–197

    Article  CAS  Google Scholar 

  • Bavi K, Kholdebarin B, Moradshahi A (2011) Effect of cadmium on growth, protein content and peroxidase activity in pea plants. Pak J Bot 43:1467–1470

    CAS  Google Scholar 

  • Britton (1995) Structure and properties of carotenoids in relation to function. FASEB J 9:1551–1558

    CAS  Google Scholar 

  • Chaignon V, Di Malta D, Hinsinger P (2002) Fe-deficiency increases Cu acquisition by wheat cropped in a Cu-contaminated vineyard soil. New Phytol 154:121–130

    Article  CAS  Google Scholar 

  • Chaney RL, Ryan JA, Li YM, Welch RM, Reeves PG, Brown SL, Green CE (1996) Phyto-availability and bio-availability in risk assessment of cadmium in agricultural environments. In: Proceedings of sources of cadmium in the environment. Organization for Economic Co-Operation and Development, Paris, pp 49-78

  • Chaney R, Brown S, Angle J (1998) Soil-root interface: ecosystem health and human food-chain protection. Soil chemistry and ecosystem health. P. Huang. Madison, Wisconsin, Soil Sci Soc Am, pp 279-311

  • Ci D, Jiang D, Dai T, Jing Q, Cao W (2009) Effects of cadmium on plant growth and physiological traits in contrast wheat recombinant inbred lines differing in cadmium tolerance. Chemosphere 77:1620–1625

    Article  CAS  Google Scholar 

  • Ci D, Jiang D, Wollenweber B, Dai T, Jing Q, Cao W (2010) Cadmium stress in wheat seedlings: growth, cadmium accumulation and photosynthesis. Acta Physiol Plant 32:365–373

    Article  CAS  Google Scholar 

  • Cieslinski G, Van Rees KCJ, Szmigielska AM, Krishnamurti GSR, Huang PM (1998) Low-molecular-weight organic acids in rhizosphere soils of durum wheat and their effect on cadmium bioaccumulation. Plant Soil 203:109–117

    Article  CAS  Google Scholar 

  • Clemens S, Palmgren MG, Kramer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315

    Article  CAS  Google Scholar 

  • Cosio C, DeSantis L, Frey B, Diallo S, Keller C (2005) Distribution of cadmium in leaves of Thlaspi caerulescens. J Exp Bot 56:765–775

    Article  CAS  Google Scholar 

  • Currie HA, Perry CC (2007) Silica in plants: biological, biochemical and chemical studies. Ann Bot 100:1383–1389

    Article  CAS  Google Scholar 

  • da Cunha KPV, do Nascimento CWA (2009) Silicon effects on metal tolerance and structural changes in maize (Zea mays L.) grown on a cadmium and zinc enriched soil. Water Air Soil Pollut 197:323–330

    Article  Google Scholar 

  • da Cunha KPV, do Nascimento CWA, da Silva AJ (2008) Silicon alleviates the toxicity of cadmium and zinc for maize (Zea mays L.) grown on contaminated soil. J Plant Nutr Soil Sci 171:849–853

    Article  Google Scholar 

  • Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36

    Article  CAS  Google Scholar 

  • Doncheva SN, Poschenrieder C, Stoyanova ZI, Georgieva K, Velichkova M, Barcelo J (2009) Silicon amelioration of manganese toxicity in Mn-sensitive and Mn-tolerant maize varieties. Environ Exp Bot 65:169–197

    Article  Google Scholar 

  • El Kassis E, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian JC (2007) Characterization of a selenate-resistant Arabidopsis thaliana mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 143:1231–1241

    Article  Google Scholar 

  • Epstein E (1994) The anomaly of silicon in plant biology. Proc Natl Acad Sci U S A 91:11–17

    Article  CAS  Google Scholar 

  • 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. Scient Horti 123:521–530

    Article  CAS  Google Scholar 

  • Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    Article  CAS  Google Scholar 

  • Grant CA, Buckley WT, Bailey LD, Selles F (1998) Cadmium accumulation in crops. Can J Plant Sci 78:1–17

    Article  CAS  Google Scholar 

  • Greger M, Löfstedt M (2004) Comparison of uptake and distribution of cadmium in different cultivars of bread and durum wheat. Crop Sci 44:501–507

    Article  CAS  Google Scholar 

  • Guntzer F, Keller C, Meunier JD (2010) Determination of the silicon concentration in plant material using Tiron extraction. New Phytol 188:902–906

    Article  CAS  Google Scholar 

  • Haouari CC, Nasraoui AH, Bouthour D, Houda MD, Daieb CB, Mnai J, Gouia H (2012) Response of tomato (Solanum lycopersicon) to cadmium toxicity: growth, element uptake, chlorophyll content and photosynthesis rate. Afr J Plant Sci 6:1–7

    CAS  Google Scholar 

  • Harris NS, Taylor GJ (2001) Remobilization of cadmium in maturing shoots of near isogenic lines of durum wheat that differ in grain cadmium accumulation. J Exp Bot 52:1473–1481

    Article  CAS  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Sullivan LA, Kochian LV (1998) Characterization of cadmium binding, uptake and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116:1413–1420

    Article  CAS  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Kochian LV (2002) Transport interactions between cadmium and zinc in roots of bread and durum wheat seedlings. Physiol Plant 116:73–78

    Article  CAS  Google Scholar 

  • Hasan SA, Fariduddin Q, Ali B, Hayat S, Ahmad A (2009) Cadmium: toxicity and tolerance in plants. J Environ Biol 30:165–174

    CAS  Google Scholar 

  • Hernandez-Apaolaza L (2014) Can silicon partially alleviate micronutrient deficiency in plants? A review. Planta 240:447–458

    Article  CAS  Google Scholar 

  • Jalil A, Selles F, Clarke JM (1994) Effect of cadmium on growth and the uptake of cadmium and other elements by durum wheat. J Plant Nutr 17:1839–1858

    Article  CAS  Google Scholar 

  • Keller C, Hammer D, Kayser A, Richner W, Brodbeck M, Sennhauser M (2003) Root development and phytoextraction efficiency: comparison of different species. Plant Soil 249:67–81

    Article  CAS  Google Scholar 

  • Keller C, Rizwan M, Davidian JC, Pokrovsky OS, Bovet N, Chaurand P, Meunier JD (2015) Effect of silicon on wheat seedlings (Triticum turgidum L.) grown in hydroponics and exposed to 0 to 30 μM Cu. Planta 241:847–860

    Article  CAS  Google Scholar 

  • Küpper H, Küpper F, Spiller M (1998) In situ detection of heavy metal substituted chlorophylls in water plants. Photosyn Res 58:123–133

    Article  Google Scholar 

  • Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120

    Article  CAS  Google Scholar 

  • Liang YC, Wong JWC, Long W (2005) Silicon-mediated enhancement of cadmium tolerance in maize (Zea mays L.) grown in cadmium contaminated soil. Chemosphere 58:475–483

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids—pigments of photosynthetic biomembranes In: Colowick SP, Kaplan NO (ed.) Methods in enzymology. Academic Press, San Diego-New York-Berkeley-Boston-London-Sydney-Tokyo-Toronto, 148:350-382

  • Liu JG, Qian M, Cai GL, Yang JC, Zhu QS (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

    Article  CAS  Google Scholar 

  • Liu C, Li F, Luo C, Liu X, Wang S, Liu T, Li X (2009) Foliar application of two silica sols reduced cadmium accumulation in rice grains. J Hazard Mater 161:1466–1472

    Article  CAS  Google Scholar 

  • López-Millán AF, Sagardoy R, Solanas M, Abadía A, Abadía J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ Exp Bot 65:376–385

    Article  Google Scholar 

  • Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

    Article  CAS  Google Scholar 

  • Ma JF, Hiradate S, Matsumoto H (1998) High aluminium resistance in buckwheat. II. Oxalic acid detoxifies aluminium internally. Plant Physiol 117:753–759

    Article  CAS  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    Article  CAS  Google Scholar 

  • Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691

    Article  CAS  Google Scholar 

  • MacFarlane GR, Burchett MD (2000) Cellular distribution of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh. Aquatic Bot 68:45–59

    Article  CAS  Google Scholar 

  • Meyer MW, Fricke FL, Holmgren GGS, Kubota J, Chaney RL (1982) Cadmium and lead in wheat grain and associated surface soils of major wheat production areas of the United States. pp 34. In: Agronomy abstracts, the Am Soc Agron, Madison

  • Motomura H, Fujii T, Suzuki M (2000) Distribution of silicified cells in the leaf blades of Pleioblastus chino (Franchet et Savatier) Makino (Bambusoideae). Ann Bot 85:751–757

    Article  Google Scholar 

  • Naeem A, Saifullah, Ghafoor A, Farooq M (2015) Suppression of cadmium concentration in wheat grains by silicon is related to its application rate and cadmium accumulating abilities of cultivars. J Sci Food Agric 95:2467–2472

  • Nakamura SI, Akiyama C, Sasaki T, Hattori H, Chino M (2008) Effect of cadmium on the chemical composition of xylem exudates from oilseed rape plants (Brassica napus L.). Soil Sci Plant Nutr 54:118–127

    Article  CAS  Google Scholar 

  • Neumann DE, Zur Nieden U (2001) Silicon and heavy metal tolerance of higher plant. Phytochem 56:685–692

    Article  CAS  Google Scholar 

  • Norvell WA, Wu J, Hopkins DG, Welch RM (2000) Association of cadmium in durum wheat grain with soil chloride and chelate-extractable soil cadmium. Soil Sci Soc Am J 64:2162–2168

    Article  CAS  Google Scholar 

  • Nwugo CC, Huerta AJ (2008) Effects of silicon nutrition on cadmium uptake, growth and photosynthesis of rice plants exposed to low-level cadmium. Plant Soil 311:73–86

    Article  CAS  Google Scholar 

  • Ouzounidou G, Moustakas M, Eleftheriou EP (1997) Physiological and ultrastructural effects of cadmium on wheat (Triticum aestivum L.) leaves. Arch Environ Contam Toxicol 32:154–160

    Article  CAS  Google Scholar 

  • Parr JF, Lentfer CJ, Boyd WE (2001a) A comparative analysis of wet and dry ashing techniques for the extraction of phytoliths from plant material. J Archaeol Sci 28:875–886

    Article  Google Scholar 

  • Parr JF, Dolic V, Lancaster G, Boyd WE (2001b) A microwave digestion method for the extraction of phytoliths from herbarium specimens. Rev Palaeobot Palynol 116:203–212

    Article  Google Scholar 

  • Rizwan M, Meunier JD, Miche H, Keller C (2012) Effect of silicon on reducing cadmium toxicity in durum wheat (Triticum turgidum L. cv. Claudio W.) grown in a soil with aged contamination. J Hazard Mater 209–210:326–334

    Article  Google Scholar 

  • Rogalla L, Römheld V (2002) Role of leaf apoplast in silicon-mediated manganese tolerance of Cucumis sativus L. Plant Cell Environ 25:549–555

    Article  CAS  Google Scholar 

  • Saber NE, Abdel-Monein AM, Barakat SY (1999) Role of organic acids in sunflower tolerance to heavy metals. Biol Plant 42:65–73

    Article  CAS  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    CAS  Google Scholar 

  • Sanita di Toppi L, Gabrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Senden MHMN, Van Der Meer AJGM, Verburg TG, Wolterbeek HT (1995) Citric acid in tomato plant roots and its effect on cadmium uptake and distribution. Plant Soil 171:333–339

    Article  CAS  Google Scholar 

  • Shi X, Zhang C, Wang H, Zhang F (2005) Effect of Si on the distribution of Cd in rice seedlings. Plant Soil 272:53–60

    Article  CAS  Google Scholar 

  • Shi G, Cai Q, 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

    Article  CAS  Google Scholar 

  • Sommer M, Kaczorek D, Kuzyakov Y, Breuer J (2006) Silicon pools and fluxes in soils and landscapes: a review. J Plant Nutr Soil Sci 169:310–329

    Article  CAS  Google Scholar 

  • Song A, Li P, Li Z, Fan F, Nikolic M, Liang Y (2011) The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reactions in rice. Plant Soil 344:319–333

    Article  CAS  Google Scholar 

  • Sridhar BBM, Han FX, Diehl SV, Monts DL, Su Y (2007) Effects of Zn and Cd accumulation on structural and physiological characteristics of barley plants. Braz J Plant Physiol 19:15–22

    Article  CAS  Google Scholar 

  • Treder W, Cieslinski G (2005) Effect of silicon application on cadmium uptake and distribution in strawberry plants grown on contaminated soils. J Plant Nutr 28:917–929

    Article  CAS  Google Scholar 

  • Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688

    Article  CAS  Google Scholar 

  • Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T (2011) Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci U S A 108:20959–20964

    Article  CAS  Google Scholar 

  • Vaculík M, Lux A, Luxova M, Tanimoto E, Lichtscheid I (2009) Silicon mitigates cadmium inhibitory effects in young maize plants. Environ Exp Bot 67:52–58

    Article  Google Scholar 

  • Vaculík M, Landberg T, Greger M, Luxova M, Stolarikova M, Lux A (2012) Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize. Ann Bot 110:433–443

    Article  Google Scholar 

  • Vaculík M, Pavlovič A, Lux A (2015) Silicon alleviates cadmium toxicity by enhanced photosynthetic rate and modified bundle sheath’s cell chloroplasts ultrastructure in maize. Ecotoxicol Environ Saf 120:66–73

    Article  Google Scholar 

  • Voogt W, Sonneveld C, Datnoff LE, Korndrfer GHS (2001) Silicon in horticultural crops grown in soilless culture, chapter 6. In: Studies in plant science, Elsevier, pp 115–131

  • Wang LJ, Wang YH, Chen Q, Cao WD, Li M, Zhang FS (2000) Silicon induced cadmium tolerance of rice seedlings. J Plant Nutr 23:1397–1406

    Article  CAS  Google Scholar 

  • Wójcik M, Tukiendorf A (2005) Cadmium uptake, localization and detoxification in Zea mays. Biol Plant 49:237–245

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zorrig W, Rouached A, Shahzad Z, Abdelly C, Davidian JC, Berthomieu P (2010) Identification of three relationships linking cadmium accumulation to cadmium tolerance and zinc and citrate accumulation in lettuce. J Plant Physiol 167:1239–1247

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financed by the French Institut National des Sciences de l’Univers (INSU, CNRS) programme Ecosphère continentale et côtière (EC2CO). Muhammad Rizwan was financed by the Higher Education Commission (HEC) of Pakistan. We thank Stéphane Jézequel (Arvalis-Institut du Végétal, France) for his help in the selection of the durum wheat cultivar and for providing the seeds, Perrine Chaurand (Aix-Marseille University, France) for the XRF analysis and Wim Voogt (Wageningen University, NL) for providing Si(KOH)2 and expertise concerning Si in nutrient solution. Partial support from BIO-GEO-CLIM project (14.B25.31.0001) of the MinObrNauki is also acknowledged (OP).

Author information

Authors and Affiliations

  1. Department of Environmental Sciences and Engineering, Government College University, Faisalabad, 38000, Pakistan

    M. Rizwan

  2. Aix-Marseille Université, CNRS, IRD, CEREGE UM34, 13545, Aix en Provence, France

    M. Rizwan, J.-D. Meunier & C. Keller

  3. Biochimie & Physiologie Moléculaire des Plantes, UMR CNRS-INRA-Université Montpellier II-Montpellier SupAgro, Place Viala, 34060, Montpellier, Cedex 2, France

    J.-C. Davidian

  4. Geoscience and Environment Toulouse (GET), UMR 5563 CNRS, 14 Avenue Edouard Belin, 31400, Toulouse, France

    O. S. Pokrovsky

  5. BIO-GEO-CLIM Laboratory, Tomsk State University, Tomsk, Russia

    O. S. Pokrovsky

  6. Nano-Science Center, Department of Chemistry, University of Copenhagen, Universitetsparken 5, 2100, Copenhagen, Denmark

    N. Bovet

Authors
  1. M. Rizwan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J.-D. Meunier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J.-C. Davidian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. S. Pokrovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. Bovet
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Keller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Keller.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 27 kb)

ESM 2

(DOCX 41 kb)

ESM 3

(DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rizwan, M., Meunier, JD., Davidian, JC. et al. Silicon alleviates Cd stress of wheat seedlings (Triticum turgidum L. cv. Claudio) grown in hydroponics. Environ Sci Pollut Res 23, 1414–1427 (2016). https://doi.org/10.1007/s11356-015-5351-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5351-4

Keywords

Search

Navigation