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.
Similar content being viewed by others
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
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
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
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
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
Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486. doi:10.1007/s004250000458
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
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
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
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
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
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
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
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
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
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
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
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
Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613. doi:10.1093/jxb/erg303
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
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular. California Agricultural Experiment Station 347:1–32
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
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
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
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
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
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
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
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
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
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
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
Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545. doi:10.1016/0098-8472(95)00024-0
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
R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
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
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
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
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
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
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
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
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
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
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
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
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
EFSA (2011) Scientific opinion: statement on tolerable weekly intake for cadmium
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
Authors and Affiliations
Corresponding author
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
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-5782-y