Skip to main content

Accumulation of Cd, Cu and Zn in shoots of maize (Zea mays L.) exposed to 0.8 or 20 nM Cd during vegetative growth and the relation with xylem sap composition

Environmental Science and Pollution Research volume 23, pages 3152–3164 (2016)Cite this article

Abstract

This work focuses on the exposure of maize plants to nanomolar concentrations of Cd, which is relevant for agricultural soils cropped with food and feed plants. Maize plants were cultivated in nutrient solution at 0.8 or 20 nM Cd during the vegetative growth stages. No significant hormesis or toxic effects of Cd were observed on maize growth, but a decrease in the allocation of Cd to shoots between the 0.8 and 20 nM Cd exposures revealed that the plants already responded to these low concentrations of Cd according to a shoot Cd excluder strategy. The Cd, Cu and Zn concentrations in shoots decreased with time as the result of an early decrease in the root/shoot ratio and of a decrease in the coefficient of allocation to aboveground for Zn and Cd at 20 nM. As a consequence, shoots of young plants were richer in micronutrients Cu and Zn but also in toxic Cd. The rate of delivery of Cd, Cu and Zn from xylem sap was successfully used to predict the time course of concentrations of Cd, Cu and Zn in the shoot. However, it overestimated the actual concentrations of Cd in the shoot, presumably because the reallocation of this trace element from shoots back to roots was not taken into account.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Akhter MF, McGarvey B, Macfie SM (2012) Reduced translocation of cadmium from roots is associated with increased production of phytochelatins and their precursors. J Plant Physiol 169:1821–1829. doi:10.1016/j.jplph.2012.07.011

    Article  CAS  Google Scholar 

  • Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654. doi:10.1080/01904168109362867

    Article  CAS  Google Scholar 

  • Belanger G, Ziadi N (2008) Phosphorus and nitrogen relationships during spring growth of an aging timothy sward. Agron J 100:1757–1762. doi:10.2134/agronj2008.0132

    Article  CAS  Google Scholar 

  • Bloom AJ, Caldwell RM (1988) Root excision decreases nutrient absorption and gas fluxes. Plant Physiol 87:794–796. doi:10.1104/pp.87.4.794

    Article  CAS  Google Scholar 

  • Cakmak I, Welch RM, Hart J et al (2000) Uptake and retranslocation of leaf‐applied cadmium (109Cd) in diploid, tetraploid and hexaploid wheats. J Exp Bot 51:221–226. doi:10.1093/jexbot/51.343.221

    Article  CAS  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486. doi:10.1007/s004250000458

    Article  CAS  Google Scholar 

  • Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99. doi:10.1016/j.tplants.2012.08.003

    Article  CAS  Google Scholar 

  • Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330. doi:10.1016/j.pbi.2006.03.015

    Article  CAS  Google Scholar 

  • Degryse F, Smolders E, Merckx R (2006) Labile Cd complexes increase Cd availability to plants. Environ Sci Technol 40:830–836. doi:10.1021/es050894t

    Article  CAS  Google Scholar 

  • Degryse F, Shahbazi A, Verheyen L, Smolders E (2012) Diffusion limitations in root uptake of cadmium and zinc, but not nickel, and resulting bias in the Michaelis constant. Plant Physiol 160:1097–1109. doi:10.1104/pp.112.202200

    Article  CAS  Google Scholar 

  • der Vliet LV, Peterson C, Hale B (2007) Cd accumulation in roots and shoots of durum wheat: the roles of transpiration rate and apoplastic bypass. J Exp Bot 58:2939–2947. doi:10.1093/jxb/erm119

    Article  CAS  Google Scholar 

  • Else MA, Hall KC, Arnold GM et al (1995) Export of abscisic acid, 1-aminocyclopropane-1-carboxylic acid, phosphate, and nitrate from roots to shoots of flooded tomato plants (accounting for effects of xylem sap flow rate on concentration and delivery). Plant Physiol 107:377–384. doi:10.1104/pp.107.2.377

    CAS  Google Scholar 

  • Enstone D, Peterson C, Ma F (2002) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351. doi:10.1007/s00344-003-0002-2

    Article  CAS  Google Scholar 

  • Florijn PJ, Nelemans JA, Beusichem MLV (1993) Evaluation of structural and physiological plant characteristics in relation to the distribution of cadmium in maize inbred lines. Plant Soil 154:103–109. doi:10.1007/BF00011078

    Article  CAS  Google Scholar 

  • Fujimaki S, Suzui N, Ishioka NS et al (2010) Tracing cadmium from culture to spikelet: noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant. Plant Physiol 152:1796–1806. doi:10.1104/pp.109.151035

    Article  CAS  Google Scholar 

  • Gastal F, Lemaire G (2002) N uptake and distribution in crops: an agronomical and ecophysiological perspective. J Exp Bot 53:789–799. doi:10.1093/jexbot/53.370.789

    Article  CAS  Google Scholar 

  • Goodger JQD, Sharp RE, Marsh EL, Schachtman DP (2005) Relationships between xylem sap constituents and leaf conductance of well-watered and water-stressed maize across three xylem sap sampling techniques. J Exp Bot 56:2389–2400. doi:10.1093/jxb/eri231

    Article  CAS  Google Scholar 

  • Grusak MA, Pearson J, Marentes E (1999) The physiology of micronutrient homeostasis in field crops. Field Crop Res 60:41–56. doi:10.1016/S0378-4290(98)00132-4

    Article  Google Scholar 

  • Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613. doi:10.1093/jxb/erg303

    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. doi:10.1034/j.1399-3054.2002.1160109.x

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular. California Agricultural Experiment Station 347:1–32

    Google Scholar 

  • Jia L, Liu Z, Chen W et al (2015) Hormesis effects induced by cadmium on growth and photosynthetic performance in a hyperaccumulator, Lonicera japonica Thunb. J Plant Growth Regul 34:13–21

    Article  CAS  Google Scholar 

  • Kobayashi NI, Tanoi K, Hirose A, Nakanishi TM (2013) Characterization of rapid intervascular transport of cadmium in rice stem by radioisotope imaging. J Exp Bot 64:507–517. doi:10.1093/jxb/ers344

    Article  CAS  Google Scholar 

  • Kochian LV (1991) Mechanisms of micronutrient uptake and translocation in plants. Micronutrient in agriculture. Soil Science Society of America, pp 229–296

  • Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37. doi:10.1093/jxb/erq281

    Article  CAS  Google Scholar 

  • McLaughlin M, Parker D, Clarke J (1999) Metals and micronutrients—food safety issues. Field Crop Res 60:143–163. doi:10.1016/S0378-4290(98)00137-3

    Article  Google Scholar 

  • McLaughlin MJ, Hamon RE, McLaren RG et al (2000) Review: a bioavailability-based rationale for controlling metal and metalloid contamination of agricultural land in Australia and New Zealand. Soil Res 38:1037–1086

    Article  CAS  Google Scholar 

  • Meers E, Samson R, Tack FMG et al (2007) Phytoavailability assessment of heavy metals in soils by single extractions and accumulation by Phaseolus vulgaris. Environ Exp Bot 60:385–396. doi:10.1016/j.envexpbot.2006.12.010

    Article  CAS  Google Scholar 

  • Nguyen C, Denaix L, Bussiere S et al (2011) Dilution of As, Cd, Pb, Cu, Zn concentration in shoot biomass during the growth of field-grown maize and the correlation with the concentration in the grain, 11th ICOBTE Adsorption-Desorption and Transport of Trace Elements in Multicomponent Systems: Experimental Evidence and Modeling Approaches. Firenze, Italy

    Google Scholar 

  • Palmgren MG, Clemens S, Williams LE et al (2008) Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13:464–473. doi:10.1016/j.tplants.2008.06.005

    Article  CAS  Google Scholar 

  • Parkhurst DL., Appelo CAJ., 1999. User’s guide to Phreeqc (version 2). A computer program for speciation, batch-reaction, one-dimensional transport, and inverse geochemical calculations, Water-Resources Investigations Report 99–4259. U.S. Department of the interior, U.S. Geological survey, 326p

  • Peuke AD (2010) Correlations in concentrations, xylem and phloem flows, and partitioning of elements and ions in intact plants. A summary and statistical re-evaluation of modelling experiments in Ricinus communis. J Exp Bot 61:635–655. doi:10.1093/jxb/erp352

    Article  CAS  Google Scholar 

  • Pinto E, Almeida AA, Ferreira IMPLVO (2015) Assessment of metal(loid)s phytoavailability in intensive agricultural soils by the application of single extractions to rhizosphere soil. Ecotox Environ Safe 113:418–424. doi:10.1016/j.ecoenv.2014.12.026

    Article  CAS  Google Scholar 

  • Plénet D, Lemaire G (1999) Relationships between dynamics of nitrogen uptake and dry matter accumulation in maize crops. Determination of critical N concentration. Plant Soil 216:65–82. doi:10.1023/A:1004783431055

    Article  Google Scholar 

  • Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545. doi:10.1016/0098-8472(95)00024-0

    Article  CAS  Google Scholar 

  • Puig S, Peñarrubia L (2009) Placing metal micronutrients in context: transport and distribution in plants. Curr Opin Plant Biol 12:299–306. doi:10.1016/j.pbi.2009.04.008

    Article  CAS  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/

    Google Scholar 

  • Redjala T, Sterckeman T, Louis Morel J (2010) Determination of the different components of cadmium short-term uptake by roots. J Plant Nutr Soil Sci 173:935–945. doi:10.1002/jpln.201000003

    Article  CAS  Google Scholar 

  • Rengel Z, Batten G, Crowley D (1999) Agronomic approaches for improving the micronutrient density in edible portions of field crops. Field Crop Res 60:27–40. doi:10.1016/S0378-4290(98)00131-2

    Article  Google Scholar 

  • Sanaeiostovar A, Khoshgoftarmanesh AH, Shariatmadari H (2011) Effects of zinc activity in nutrient solution on uptake, translocation, and root export of cadmium and zinc in three wheat genotypes with different zinc efficiencies. Soil Sci Plant Nutr 57:681–690. doi:10.1080/00380768.2011.617290

    Article  CAS  Google Scholar 

  • Sauvé S, Norvell WA, McBride M, Hendershot W (2000) Speciation and complexation of cadmium in extracted soil solutions. Environ Sci Technol 34:291–296. doi:10.1021/es990202z

    Article  CAS  Google Scholar 

  • Schurr U (1998) Xylem sap sampling—new approaches to an old topic. Trends Plant Sci 3:293–298. doi:10.1016/S1360-1385(98)01275-8

    Article  Google Scholar 

  • Shane MW, McCully ME, Canny MJ (2000) The vascular system of maize stems revisited: implications for water transport and xylem safety. Ann Bot 86:245–258. doi:10.1006/anbo.2000.1171

    Article  Google Scholar 

  • Siddhu G, Sirohi DS, Kashyap K et al (2008) Toxicity of cadmium on the growth and yield of Solanum melongena L. J Environ Biol 29:853–857

    CAS  Google Scholar 

  • Sogreah (2007) Bilan des flux de contaminants entrant sur les sols agricoles de France métropolitaine. Bilan qualitatif de la contamination par les éléments tracés métalliques et les composés tracés organiques et application quantitative pour les éléments tracés métalliques. Ademe

  • Waters BM, Sankaran RP (2011) Moving micronutrients from the soil to the seeds: genes and physiological processes from a biofortification perspective. Plant Sci 180:562–574. doi:10.1016/j.plantsci.2010.12.003

    Article  CAS  Google Scholar 

  • Welch RM, Hart JJ, Norvell WA et al (1999) Effects of nutrient solution zinc activity on net uptake, translocation, and root export of cadmium and zinc by separated sections of intact durum wheat (Triticum turgidum L. var durum) seedling roots. Plant Soil 208:243–250. doi:10.1023/A:1004598228978

    Article  CAS  Google Scholar 

  • Yamaguchi N, Ishikawa S, Abe T, et al. (2012) Role of the node in controlling traffic of cadmium, zinc, and manganese in rice. J Exp Bot err455. doi: 10.1093/jxb/err455

  • Ye X, Ma Y, Sun B (2012) Influence of soil type and genotype on Cd bioavailability and uptake by rice and implications for food safety. J Environ Sci 24:1647–1654. doi:10.1016/S1001-0742(11)60982-0

    Article  CAS  Google Scholar 

  • Yoneyama T, Gosho T, Kato M et al (2010) Xylem and phloem transport of Cd, Zn and Fe into the grains of rice plants (Oryza sativa L.) grown in continuously flooded Cd-contaminated soil. J Plant Nutr Soil Sci 56:445–453. doi:10.1111/j.1747-0765.2010.00481.x

    Article  CAS  Google Scholar 

  • Zarrouk S, Bermond A, Benzina NK et al (2014) Diffusive gradient in thin-film (DGT) models Cd and Pb uptake by plants growing on soils amended with sewage sludge and urban compost. Environ Chem Lett 12:191–199. doi:10.1007/s10311-013-0431-5

    Article  CAS  Google Scholar 

  • EFSA (2011) Scientific opinion: statement on tolerable weekly intake for cadmium

Download references

Acknowledgments

This work was supported by the French National Institute for Agricultural Research (INRA) and by the funding ANR 2011 CESA 008 01 from the Agence National de la Recherche. The authors are grateful to C. Coriou and S. Thunot for their technical help.

Author information

Affiliations

  1. INRA, UMR 1391 ISPA, 33140, Villenave d’Ornon, France

    C. Nguyen, A. J. Soulier, S. Bussière & J. Y. Cornu

  2. Bordeaux Sciences Agro, UMR 1391 ISPA, 33170, Gradignan, France

    C. Nguyen, A. J. Soulier, S. Bussière & J. Y. Cornu

  3. Unité de Services et de Recherche en Analyses Végétales et Environnementales (USRAVE), INRA, Centre de Bordeaux Aquitaine, 33140, Villenave d’Ornon, France

    P. Masson

Authors
  1. C. Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. J. Soulier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Masson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Bussière
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Y. Cornu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Nguyen.

Additional information

Responsible editor: Elena Maestri

Additional file

Below is the link to the electronic supplementary material.

ESM 1: Fig. SI 1

Actual concentrations of Cd, Cu and Zn measured in the nutrient solution of maize plants grown in hydroponics at two concentrations of Cd (n = 5). Growing degree days were calculated in basis 6. Vertical bars indicate one standard deviation. (DOC 56 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nguyen, C., Soulier, A.J., Masson, P. et al. Accumulation of Cd, Cu and Zn in shoots of maize (Zea mays L.) exposed to 0.8 or 20 nM Cd during vegetative growth and the relation with xylem sap composition. Environ Sci Pollut Res 23, 3152–3164 (2016). https://doi.org/10.1007/s11356-015-5782-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5782-y

Keywords

  • Cadmium
  • Copper
  • Dilution
  • Growth
  • Partitioning
  • Trace elements
  • Xylem sap
  • Zinc