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Longitudinal variation in cadmium influx in sunflower (Helianthus annuus L.) roots as depending on the growth substrate, root age and root order

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Abstract

Aims

In a previous work, we observed a longitudinal decrease in Cd2+ influx starting from the root tip in first order lateral roots of sunflower (Helianthus annuus L.) grown in hydroponics. This variable influx was expected to impact the total Cd2+ uptake depending on the root system architecture and on how steep was the decrease of the influx. Here, we examined the influence of the culture substrate, of the age and order of lateral roots on the longitudinal variation of Cd2+ influx.

Methods

By using short-term exposures to 109Cd-labelled solution (5 to 200 nM), we compared the longitudinal variations in Cd2+ roots influx depending on the growth substrate (hydroponics or sand), on the root age and order.

Results

In second order laterals, Cd2+ influx decreased from the apex to the root base, as for first order laterals. For sand cultures compared to hydroponics, the mean Cd2+ influx was lower and decreased more steeply with the distance from the apex. The influx also decreased with increasing root age and order, markedly in hydroponics but less for sand cultures.

Conclusion

Results suggested that for a given root surface area, the Cd2+ uptake by a root system should increase with increasing number of root tips and decreasing individual root length.

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References

  • Adriano DC (2001) Trace Elements in terrestrial environments : biochemistry, bioavailability, and risks of metals, New-York, USA

  • Aguirrezabal L (1993) Modélisation de l’allongement et de la ramification du système racinaire du tournesol (Helianthus annuus L.). Effet du rayonnement intercepté et de la température. p. 90. Blaise Pascal (Clermont-Ferrand II), Clemont-Ferrand

  • Aguirrezabal LAN, Deleens E, Tardieu F (1994) Root elongation rate is accounted for by intercepted Ppfd and source-sink relations in-field and laboratory-grown sunflower. Plant Cell and Environ 17:443–450

    Article  Google Scholar 

  • Ansari R, Kazi TG, Jamali MK, Arain MB, Wagan MD, Jalbani N, Afridi HI, Shah AQ (2009) Variation in accumulation of heavy metals in different verities of sunflower seed oil with the aid of multivariate technique. Food Chem 115:318–323

    Article  CAS  Google Scholar 

  • Berkelaar E, Hale B (2000) The relationship between root morphology and cadmium accumulation in seedlings of two durum wheat cultivars. Can J Bot-Rev Can Bot 78:381–387

    Article  CAS  Google Scholar 

  • Buckley WT, Buckley KE, Huang JZ (2010) Root cadmium desorption methods and their evaluation with compartmental modeling. New Phytol 188:280–290

    Article  CAS  PubMed  Google Scholar 

  • Cataldo DA, Garland TR, Wildung RE (1983) Cadmium uptake kinetics in intact soybean plants. Plant Physiol 73:844–848

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cholewa EM (2000) Calcium transport and delivery to the xylem in onion (Allium cepa L.) roots. In University of Waterloo, Waterloo, p 158

    Google Scholar 

  • Claassen N, Steingrobe B (1999) Mechanistic simulation models for a better understanding of nutrient uptake from soil. In: Rengel Z (ed) Mineral nutrition of crops: fundamental mechanisms and implications. Food Products Press, Haworth, pp 327–367

    Google Scholar 

  • Costa G, Morel JL (1993) Cadmium uptake by Lupinus albus (L)- Cadmium excretion, a possible mechanism of cadmium tolerance. J Plant Nutr 16:1921–1929

    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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Enstone DE, Peterson CA, Ma FS (2002) Root endodermis and exodermis: Structure, function, and responses to the environment. J Plant Growth Regul 21:335–351

    Article  CAS  Google Scholar 

  • Faessler E, Robinson BH, Stauffer W, Gupta SK, Papritz A, Schulin R (2010) Phytomanagement of metal-contaminated agricultural land using sunflower, maize and tobacco. Agric Ecosyst Environ 136:49–58

    Article  CAS  Google Scholar 

  • Farrell RE, McArthur DFE, Van Rees KCJ (2005) Net Cd2+ flux at the root surface of durum wheat (Triticum turgidum L. var. durum) cultivars in relation to cultivar differences in Cd accumulation. Can J Plant Sci 85:103–107

    Article  CAS  Google Scholar 

  • Ferguson IB, Clarkson DT (1976) Ion uptake in relation to development of a root hypodermis. New Phytol 77:11–14

    Article  CAS  Google Scholar 

  • Freixes S, Thibaud MC, Tardieu F, Muller B (2002) Root elongation and branching is related to local hexose concentration in Arabidopsis thaliana seedlings. Plant Cell Environ 25:1357–1366

    Article  CAS  Google Scholar 

  • Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310

    Article  CAS  PubMed  Google Scholar 

  • He JY, Ren YF, Wang FJ, Pan XB, Zhu C, Jiang DA (2009) Characterization of cadmium uptake and translocation in a cadmium-sensitive mutant of rice (Oryza sativa L. ssp japonica). Arch Environ Contam Toxicol 57:299–306

    Article  CAS  PubMed  Google Scholar 

  • He JL, Qin JJ, Long LY, Ma YL, Li H, Li K, Jiang XN, Liu TX, Polle A, Liang ZS, Luo ZB (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus x canescens. Physiol Plant 143:50–63

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Station 347:1–32

    Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere - a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Laporte MA, Denaix L, Pagès L, Sterckeman T, Flénet F, Dauguet S, Nguyen C (2013) Longitudinal variation in cadmium influx in intact first order lateral roots of sunflower (Helianthus annuus. L). Plant and Soil, 1–15

  • Lehmann H, Stelzer R, Holzamer S, Kunz U, Gierth M (2000) Analytical electron microscopical investigations on the apoplastic pathways of lanthanum transport in barley roots. Planta 211:816–822

    Article  CAS  PubMed  Google Scholar 

  • Li L, Liu X, Peijnenburg WJGM, Zhao J, Chen X, Yu J, Wu H (2012) Pathways of cadmium fluxes in the root of the halophyte Suaeda salsa. Ecotoxicol Environ Saf 75:1–7

    Article  PubMed  Google Scholar 

  • Lux A, Sottnikova A, Opatrna 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mullins GL, Sommers LE, Barber SA (1986) Modeling the plant uptake of cadmium and zinc from soils treated with sewage sludge. Soil Sci Soc Am J 50:1245–1250

    Article  CAS  Google Scholar 

  • Niu Z-x, L-n S, T-h S, Y-s L, Wang H (2007) Evaluation of phytoextracting cadmium and lead by sunflower, ricinus, alfalfa and mustard in hydroponic culture. J Environ Sci-China 19:961–967

    Article  CAS  Google Scholar 

  • Nye PH (1973) The relation between the radius of a root and its nutrient-absorbing power alpha. Some theoretical considerations. J Exp Bot 24:783–786

    Article  Google Scholar 

  • Pagès L, Moreau D, Sarlikioti V, Boukcim H, Nguyen C (2012) ArchiSimple: a parsimonious model of the root system architecture, In: Proceedings. Presented at the IEEE 4th International symposium on plant growth modeling, simulation, visualization and applications ShangHai (China)

  • Pellerin S, Pages L (1994) Evaluation of parameters describing the root system architecture of field grown maize plants (Zea mays L). 1. Elongation of seminal and nodal roots and extension of their branched zone. Plant Soil 164:155–167

    Article  CAS  Google Scholar 

  • Perumalla CJ, Peterson CA, Enstone DE (1990) A survey of angiosperm species to detect hypodermal Casparian bands.1. Roots with a uniseriate hypodermis and epidermis. Bot J Linn Soc 103:93–112

    Article  Google Scholar 

  • Pineros MA, Shaff JE, Kochian LV (1998) Development, characterization, and application of a cadmium-selective microelectrode for the measurement of cadmium fluxes in roots of Thlaspi species and wheat. Plant Physiol 116:1393–1401

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pinheiro J, Douglas Bates, Saikat DebRoy, Deepayan Sarkar and the R Development Core Team (2012) nlme: Linear and nonlinear mixed effects models. R package version 3.1-105

  • Rasmussen PE, Goulding KWT, Brown JR, Grace PR, Janzen HH, Korschens M (1998) Agroecosystem - Long-term agroecosystem experiments: Assessing agricultural sustainability and global change. Science 282:893–896

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Redjala T, Sterckeman T, Morel JL (2009) Cadmium uptake by roots: Contribution of apoplast and of high- and low-affinity membrane transport systems. Environ Exp Bot 67:235–242

    Article  CAS  Google Scholar 

  • Redjala T, Zelko I, Sterckeman T, Legue V, Lux A (2011) Relationship between root structure and root cadmium uptake in maize. Environ Exp Bot 71:241–248

    Article  CAS  Google Scholar 

  • Smolders E (2001) Cadmium uptake by plants. Int J Occup Med Environ Health 14:177–183

    CAS  PubMed  Google Scholar 

  • Sterckeman T, Perriguey J, Cael M, Schwartz C, Morel JL (2004) Applying a mechanistic model to cadmium uptake by Zea mays and Thlaspi caerulescens: consequences for the assessment of the soil quantity and capacity factors. Plant Soil 262:289–302

    Article  CAS  Google Scholar 

  • Tarradellas J, Bitton G, Rossel D (1997) Soil Ecotoxicology. Publisher CRC Lewis, Boca Ratón

    Google Scholar 

  • Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the funding ANR 2011 CESA 008 01 and by a research grant from the Technical Center for Oilseed Crops and Industrial Hemp (CETIOM) and from the French National Institute for Agricultural Research (INRA). The authors are grateful to S. Bussière, C. Coriou, and S. Thunot for their helpful technical contribution and to L. Pagès (INRA, Avignon) for providing the rhizoboxes.

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Correspondence to Christophe Nguyen.

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Responsible Editor: Fangjie Zhao.

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Laporte, M.A., Denaix, L., Dauguet, S. et al. Longitudinal variation in cadmium influx in sunflower (Helianthus annuus L.) roots as depending on the growth substrate, root age and root order. Plant Soil 381, 235–247 (2014). https://doi.org/10.1007/s11104-014-2123-8

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