Plant and Soil

, Volume 424, Issue 1–2, pp 591–606 | Cite as

Contribution of remobilization to the loading of cadmium in durum wheat grains: impact of post-anthesis nitrogen supply

  • Bo-Fang Yan
  • C. Nguyen
  • O. S. Pokrovsky
  • F. Candaudap
  • C. Coriou
  • S. Bussière
  • T. Robert
  • J. Y. Cornu
Regular Article



This study focuses on quantifying the contribution of remobilization to the amount of cadmium accumulated in durum wheat grains. The impact of post-anthesis N supply was tested in two cultivars that differ in their shoot biomass partitioning.


Two French durum wheat cultivars were grown hydroponically and exposed to 100 nM Cd. After anthesis, the plants were fed with a solution enriched in the stable isotope 111Cd to trace the Cd newly absorbed, and subjected or not to nitrogen deprivation. Plants were sampled at anthesis and grain maturity to assess the post-anthesis fluxes of Cd and N among organs.


Cd remobilized from pre-anthesis stores contributed to more than half of the Cd accumulated in mature grains. Cd was mainly remobilized from stem and poorly remobilized from leaves. Stopping N supply during grain filling enhanced N remobilization but had no impact on post-anthesis uptake and remobilization of Cd, and thereby, on Cd concentration in grains. No difference was observed between the two cultivars in the contribution of Cd remobilization and its dependence toward post-anthesis N supply.


Cd remobilization significantly contributes to the accumulation of Cd in durum wheat grains. Cd remobilization is not tightly linked with N remobilization and behaves like a senescent-independent process in durum wheat.


Low-dose cadmium Cereal Post-anthesis uptake Remobilization Senescence Stable isotope labeling 



This work has been financially supported by ARVALIS-Institut du végétal through the “CADUR” project, by the French National Institute of Agronomic Research (INRA), by the French National Research Agency through the “CADON” project (ANR-15-CE21-0001) and by the CNRS-INSU EC2CO program (Ecodyn) through the “CADMIGRAIN” project. The authors thank Valérie Nicaise for internal review, Sylvie Milin (INRA) for technical help in determining the grain concentrations in N and C, PhD Juan Carlos Raposo from SGIker of UPV/EHU for technical and human support in ICP-MS and ICP-AES measurements and the China Scholarship Council (CSC) for the doctoral scholarship of Bo-Fang Yan.

Supplementary material

11104_2018_3560_MOESM1_ESM.doc (734 kb)
ESM 1 (DOC 734 kb)


  1. Aciksoz SB, Yazici A, Ozturk L, Cakmak I (2011) Biofortification of wheat with iron through soil and foliar application of nitrogen and iron fertilizers. Plant Soil 349:215–225. CrossRefGoogle Scholar
  2. Archambault DJ, Marentes E, Buckley W, Clarke J, Taylor GJ (2001) A rapid, seedling-based bioassay for identifying low cadmium-accumulating individuals of durum wheat (Triticum turgidum L.). Euphytica 117:175–182.
  3. Ben Slimane R, Bancal P, Bancal M-O (2013) Down-regulation by stems and sheaths of grain filling with mobilized nitrogen in wheat. Field Crop Res 140:59–68. CrossRefGoogle Scholar
  4. Buckley WT, Buckley KE, Huang JJ (2010) Root cadmium desorption methods and their evaluation with compartmental modeling. New Phytol 188:280–290. CrossRefPubMedGoogle Scholar
  5. Cakmak I, Kutman UB (2017) Agronomic biofortification of cereals with zinc: a review. Eur J Soil Sci.
  6. Chan DY, Hale BA (2004) Differential accumulation of Cd in durum wheat cultivars: uptake and retranslocation as sources of variation. J Exp Bot 55:2571–2579. CrossRefPubMedGoogle Scholar
  7. Clarke JM, Clarke FR, Pozniak CJ (2010) Forty-six years of genetic improvement in Canadian durum wheat cultivars. Can J Plant Sci 90:791–801. CrossRefGoogle Scholar
  8. EC (2006) Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuff. Off J Eur Union 364:5–24Google Scholar
  9. EFSA (2012) Cadmium dietary exposure in the European population. EFSA J 10:2551. CrossRefGoogle Scholar
  10. Emanuelli T, Milbradt BG, Kolinski Callegaro M, Augusti PR (2014) Wheat bran and cadmium in human health. In: Watson RR, Preedy VR, Zibadi S (eds) Wheat and rice in disease prevention and health. Academic, San Diego. ​
  11. Erenoglu EB, Kutman UB, Ceylan Y, Yildiz B, Cakmak I (2011) Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of zinc (65Zn) in wheat. New Phytol 189:438–448. CrossRefPubMedGoogle Scholar
  12. Gao X, Brown KR, Racz GJ, Grant CA (2010) Concentration of cadmium in durum wheat as affected by time, source and placement of nitrogen fertilization under reduced and conventional-tillage management. Plant Soil 337:341–354. CrossRefGoogle Scholar
  13. Gustafsson JP (2011) Visual MINTEQ ver. 3.0. Department of Land and Water Resources Engineering, Royal Institute of Technology: Stockholm, Sweden. Internet:
  14. 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. CrossRefPubMedGoogle Scholar
  15. Harris NS, Taylor GJ (2013) Cadmium uptake and partitioning in durum wheat during grain filling. BMC Plant Biol 13:103. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Henry R, Kettlewell P (1996) Cereal grain quality. Springer, Netherlands.
  17. Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53:927–937. CrossRefPubMedGoogle Scholar
  18. Juraniec M, Hermans C, Salis P, Geelen D, Verbruggen N (2017) Impact of post-flowering nitrate availability on nitrogen remobilization in hydroponically grown durum wheat. J Plant Nutr Soil Sci 180:273–278.
  19. Khan MA, Castro-Guerrero N, Mendoza-Cozatl DG (2014) Moving toward a precise nutrition: preferential loading of seeds with essential nutrients over non-essential toxic elements. Front Plant Sci 5:51. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kutman UB, Yildiz B, Cakmak I (2011) Effect of nitrogen on uptake, remobilization and partitioning of zinc and iron throughout the development of durum wheat. Plant Soil 342:149–164. CrossRefGoogle Scholar
  21. Kutman UB, Kutman BY, Ceylan Y, Ova EA, Cakmak I (2012) Contributions of root uptake and remobilization to grain zinc accumulation in wheat depending on post-anthesis zinc availability and nitrogen nutrition. Plant Soil 361:177–187. CrossRefGoogle Scholar
  22. Liñero O, Cornu J-Y, Candaudap F, Pokrovsky OS, Bussière S, Coriou C, Humann-Guilleminot T, Robert T, Thunot S, de Diego A, Nguyen C (2016) Short-term partitioning of Cd recently taken up between sunflowers organs (Helianthus annuus) at flowering and grain filling stages: effect of plant transpiration and allometry. Plant Soil 408:163–181. CrossRefGoogle Scholar
  23. Maillard A, Diquelou S, Billard V, Laine P, Garnica M, Prudent M, Garcia-Mina JM, Yvin JC, Ourry A (2015) Leaf mineral nutrient remobilization during leaf senescence and modulation by nutrient deficiency. Front Plant Sci 6:317. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Marschner H (2011) Marschner's mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  25. Masclaux C, Quilleré I, Gallais A, Hirel B (2001) The challenge of remobilisation in plant nitrogen economy. A survey of physio-agronomic and molecular approaches. Ann Appl Biol 138:69–81. CrossRefGoogle Scholar
  26. McLaughlin MJ, Smolders E, Merckx R, Maes A (1997) Plant uptake of Cd and Zn in chelator-buffered nutrient solution depends on ligand type. In: Ando T, Fujita K, Mae T, Matsumoto H, Mori S, Sekiya J (eds) Plant nutrition for sustainable food production and environment. Developments in Plant and Soil Sciences, vol 78. Springer, Dordrecht.
  27. Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259. CrossRefPubMedPubMedCentralGoogle Scholar
  28. O’Brien TP, Sammut ME, Lee JW, Smart MG (1985) The vascular system of the wheat spikelet. Aust J Plant Physiol 12:487–511.
  29. Perilli P, Mitchell LG, Grant CA, Pisante M (2010) Cadmium concentration in durum wheat grain (Triticum turgidum) as influenced by nitrogen rate, seeding date and soil type. J Sci Food Agric 90:813–822. PubMedGoogle Scholar
  30. Perrier F, Yan B, Candaudap F, Pokrovsky OS, Gourdain E, Meleard B, Bussière S, Coriou C, Robert T, Nguyen C, Cornu JY (2016) Variability in grain cadmium concentration among durum wheat cultivars: impact of aboveground biomass partitioning. Plant Soil 404:307–320.
  31. Pottier M, Masclaux-Daubresse C, Yoshimoto K, Thomine S (2014) Autophagy as a possible mechanism for micronutrient remobilization from leaves to seeds. Front Plant Sci 5.
  32. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  33. Rodda MS, Li G, Reid RJ (2011) The timing of grain Cd accumulation in rice plants: the relative importance of remobilisation within the plant and root Cd uptake post-flowering. Plant Soil 347:105–114. CrossRefGoogle Scholar
  34. Rodríguez-Cea A, Fernández De La Campa MDR, García Alonso JI, Sanz-Medel A (2006) The use of enriched 111Cd as tracer to study de novo cadmium accumulation and quantitative speciation in Anguilla anguilla tissues. J Anal At Spectrom 21:270–278. CrossRefGoogle Scholar
  35. Sperotto RA, Ricachenevsky FK, Duarte GL, Boff T, Lopes KL, Sperb ER, Grusak MA, Fett JP (2009) Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230:985–1002. CrossRefPubMedGoogle Scholar
  36. Tavarez M, Macri A, Sankaran RP (2015) Cadmium and zinc partitioning and accumulation during grain filling in two near isogenic lines of durum wheat. Plant Physiol Biochem 97:461–469. CrossRefPubMedGoogle Scholar
  37. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  38. US Department of Agriculture, Agricultural Research Service, Nutrient Data Laboratory (2015) USDA national nutrient database for standard reference, Release 28. Full Report (All Nutrients): 20076, Wheat, durum. Internet:
  39. Welch RM, Norvell WA (1999) Mechanisms of cadmium uptake, translocation and deposition in plants. In: McLaughlin MJ, Singh BR (eds) Cadmium in soils and plants. Developments in Plant and Soil Sciences, vol 85. Springer, Dordrecht.
  40. Wu CY, Lu LL, Yang XE, Feng Y, Wei YY, Hao HL, Stoffella PJ, He ZL (2010) Uptake, translocation, and remobilization of zinc absorbed at different growth stages by rice genotypes of different Zn densities. J Agric Food Chem 58:6767–6773. CrossRefPubMedGoogle Scholar
  41. Yamaguchi N, Ishikawa S, Abe T, Baba K, Arao T, Terada Y (2012) Role of the node in controlling traffic of cadmium, zinc, and manganese in rice. J Exp Bot 63:2729–2737. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Yamaji N, Ma JF (2014) The node, a hub for mineral nutrient distribution in graminaceous plants. Trends Plant Sci 19:556–563. CrossRefPubMedGoogle Scholar
  43. Yamaji N, Xia J, Mitani-Ueno N, Yokosho K, Ma JF (2013) Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol 162:927–939.
  44. Zimmerl S, Lafferty J, Buerstmayr H (2014) Assessing diversity in Triticum durum cultivars and breeding lines for high versus low cadmium content in seeds using the CAPS marker usw47. Plant Breed 133:712–717. CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.ISPA, Bordeaux Sciences Agro, INRAVillenave d’OrnonFrance
  2. 2.Université Toulouse, CNRS, GET, UMR 5563ToulouseFrance

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