Advertisement

Plant and Soil

, Volume 372, Issue 1–2, pp 581–595 | Cite as

Longitudinal variation in cadmium influx in intact first order lateral roots of sunflower (Helianthus annuus. L)

  • Marie A. Laporte
  • Laurence Denaix
  • Loïc Pagès
  • Thibault Sterckeman
  • Francis Flénet
  • Sylvie Dauguet
  • Christophe Nguyen
Regular Article

Abstract

Aims

Contamination of sunflower (Helianthus annuus L.) by cadmium (Cd) is a concern for food and feed safety as this species accumulates Cd to a greater extent than other crops. We examined the relationships between root architecture and Cd2+ uptake by roots.

Methods

We determined and mathematically modelled the longitudinal variation of Cd2+ influx in first order roots of sunflower grown in hydroponics by using short-term exposure to 109Cd-labelled solutions (0.8 to 500 nM). Thereafter, by taking into account the longitudinal variation of the influx, we simulated the uptake of Cd2+ for 24 h by cohorts of roots characterised by various architectural characteristics.

Results

Cd2+ influx at the root tip was on average 2.9 times that of the basal region close to the taproot. The simulations indicated that the total Cd2+ uptake by root cohorts mainly depends on 1/ the root diameter and the number of roots, 2/ the value of the Cd2+ influx at the basal region 3/ the stronger influx at the root tip.

Conclusion

Considering a higher Cd2+ influx at the root tip may be important to understand the relationship between root architecture and Cd2+ uptake by the root system.

Keywords

Cadmium Influx Longitudinal variation Root architecture Sunflower 

Notes

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.

Supplementary material

11104_2013_1756_MOESM1_ESM.doc (34 kb)
Online Resource 1 (DOC 34 kb)

References

  1. Adriano DC (2001) Trace elements in terrestrial environments: biochemistry, bioavailability, and risks of metals, 2nd edn. Springer, New YorkCrossRefGoogle Scholar
  2. 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., Blaise Pascal (Clermont-Ferrand II), Clemont-FerrandGoogle Scholar
  3. 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(1):318–323. doi: 10.1016/j.foodchem.2008.11.051 CrossRefGoogle Scholar
  4. Assuncao AGL, Martins PD, De Folter S, Vooijs R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 24(2):217–226. doi: 10.1046/j.1365-3040.2001.00666.x CrossRefGoogle Scholar
  5. Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach. Soil nutrient bioavailability: a mechanistic approach., vol Ed. 2Google Scholar
  6. 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(3):381–387CrossRefGoogle Scholar
  7. Buckley WT, Buckley KE, Huang JZ (2010) Root cadmium desorption methods and their evaluation with compartmental modeling. New Phytol 188(1):280–290. doi: 10.1111/j.1469-8137.2010.03354.x PubMedCrossRefGoogle Scholar
  8. Cholewa EM (2000) Calcium transport and delivery to the xylem in onion (Allium cepa L.) roots.Google Scholar
  9. Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212(4):475–486. doi: 10.1007/s004250000458 PubMedCrossRefGoogle Scholar
  10. Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7(7):309–315. doi: 10.1016/s1360-1385(02)02295-1 PubMedCrossRefGoogle Scholar
  11. Costa G, Morel JL (1994) Efficiency of H +−atpase activity on cadmium uptake by 4 cultivars of lettuce. J Plant Nutr 17(4):627–637CrossRefGoogle Scholar
  12. Dong B, Rengel Z, Graham RD (1995) Root morphology of wheat genotypes differing in zinc efficiency. J Plant Nutr 18(12):2761–2773. doi: 10.1080/01904169509365098 CrossRefGoogle Scholar
  13. Durmaz E, Coruh C, Dinler G, Grusak MA, Peleg Z, Saranga Y, Fahima T, Yazici A, Ozturk L, Cakmak I, Budak H (2011) Expression and cellular localization of ZIP1 transporter under zinc deficiency in wild emmer wheat. Plant Mol Biol Rep 29(3):582–596. doi: 10.1007/s11105-010-0264-3 CrossRefGoogle Scholar
  14. Enstone DE, Peterson CA (2005) Suberin lamella development in maize seedling roots grown in aerated and stagnant conditions. Plant Cell Environ 28(4):444–455CrossRefGoogle Scholar
  15. Enstone DE, Peterson CA, Ma FS (2002) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21(4):335–351. doi: 10.1007/s00344-003-0002-2 CrossRefGoogle Scholar
  16. 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(1):103–107CrossRefGoogle Scholar
  17. Ferguson IB, Clarkson DT (1976) Ion uptake in relation to development of a root hypodermis. New Phytol 77(1):11–14CrossRefGoogle Scholar
  18. Fujimaki S, Suzui N, Ishioka NS, Kawachi N, Ito S, Chino M, Nakamura S-i (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(4):1796–1806. doi: 10.1104/pp. 109.151035 PubMedCrossRefGoogle Scholar
  19. Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390(2–3):301–310. doi: 10.1016/j.scitotenv.2007.10.038 PubMedCrossRefGoogle Scholar
  20. Harrison-Murray RS, Clarkson DT (1973) Relationship between structural development and the absorption of ions by the root system of Cucurbita pepo. Planta 114(1):1–16. doi: 10.1007/bf00390280 Google Scholar
  21. 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(4):1413–1420PubMedCrossRefGoogle Scholar
  22. He JY, Zhu C, Ren YF, Jiang DA, Sun ZX (2007) Root morphology and cadmium uptake kinetics of the cadmium-sensitive rice mutant. Biol Plant 51(4):791–794. doi: 10.1007/s10535-007-0162-1 CrossRefGoogle Scholar
  23. 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(2):299–306. doi: 10.1007/s00244-008-9273-8 PubMedCrossRefGoogle Scholar
  24. 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(1):50–63. doi: 10.1111/j.1399-3054.2011.01487.x PubMedCrossRefGoogle Scholar
  25. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Station 347:1–32Google Scholar
  26. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162(1):9–24. doi: 10.1111/j.1469-8137.2004.01015.x CrossRefGoogle Scholar
  27. Ishikawa S, Suzui N, Ito-Tanabata S, Ishii S, Igura M, Abe T, Kuramata M, Kawachi N, Fujimaki S (2011) Real-time imaging and analysis of differences in cadmium dynamics in rice cultivars (Oryza sativa) using positron-emitting Cd-107 tracer. BMC Plant Biol 11. doi: 10.1186/1471-2229-11-172
  28. Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205(1):25–44. doi: 10.1023/a:1004356007312 CrossRefGoogle Scholar
  29. 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(6):816–822. doi: 10.1007/s004250000346 PubMedCrossRefGoogle Scholar
  30. 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. doi: 10.1016/j.ecoenv.2011.09.007 PubMedCrossRefGoogle Scholar
  31. 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(4):537–545PubMedCrossRefGoogle Scholar
  32. Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62(1):21–37. doi: 10.1093/jxb/erq281 PubMedCrossRefGoogle Scholar
  33. McLaughlin MJ, Parker DR, Clarke JM (1999) Metals and micronutrients—food safety issues. Field Crops Res 60(1–2):143–163. doi: 10.1016/s0378-4290(98)00137-3 CrossRefGoogle Scholar
  34. Nwoke OC, Diels J, Abaidoo R, Nziguheba G, Merckx R (2008) Organic acids in the rhizosphere and root characteristics of soybean (Glycine max) and cowpea (Vigna unguiculata) in relation to phosphorus uptake in poor savanna soils. Afr J Biotechnol 7(20):3617–3624Google Scholar
  35. Nye PH (1973) The relation between the radius of a root and its nutrient-absorbing power alpha. Some theoretical considerations. J Exp Bot 24(82):783–786. doi: 10.1093/jxb/24.5.783 CrossRefGoogle Scholar
  36. 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)Google Scholar
  37. 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(2):93–112. doi: 10.1111/j.1095-8339.1990.tb00176.x CrossRefGoogle Scholar
  38. 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(4):1393–1401PubMedCrossRefGoogle Scholar
  39. Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2012) nlme: linear and nonlinear mixed effects models. R package version 3.1-105Google Scholar
  40. 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
  41. 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(5390):893–896. doi: 10.1126/science.282.5390.893 PubMedCrossRefGoogle Scholar
  42. 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(1):235–242. doi: 10.1016/j.envexpbot.2009.05.012 CrossRefGoogle Scholar
  43. 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(6):935–945. doi: 10.1002/jpln.201000003 CrossRefGoogle Scholar
  44. 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(2):241–248. doi: 10.1016/j.envexpbot.2010.12.010 CrossRefGoogle Scholar
  45. Rubio G, Sorgona A, Lynch JP (2004) Spatial mapping of phosphorus influx in bean root systems using digital autoradiography. J Exp Bot 55(406):2269–2280. doi: 10.1093/jxb/erh246 PubMedCrossRefGoogle Scholar
  46. Smolders E (2001) Cadmium uptake by plants. Int J Occup Med Environ Health 14(2):177–183PubMedGoogle Scholar
  47. Weber M, Harada E, Vess C, von Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37(2):269–281. doi: 10.1046/j.1365-313X.2003.01960.x PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Marie A. Laporte
    • 1
    • 2
  • Laurence Denaix
    • 1
    • 2
  • Loïc Pagès
    • 3
  • Thibault Sterckeman
    • 4
  • Francis Flénet
    • 5
  • Sylvie Dauguet
    • 6
  • Christophe Nguyen
    • 1
    • 2
  1. 1.INRA, UMR1220 TCEMVillenave d’OrnonFrance
  2. 2.Univ. Bordeaux, UMR1220 TCEMVillenave d’OrnonFrance
  3. 3.INRA - UR 1115 PSHAvignon cedex 9France
  4. 4.Laboratoire Sols et EnvironnementUniversité de Lorraine - INRAVandœuvre-lès-Nancy cedexFrance
  5. 5.CETIOMThiverval GrignonFrance
  6. 6.CETIOMPessacFrance

Personalised recommendations