Plant and Soil

, Volume 424, Issue 1–2, pp 435–450 | Cite as

Source of Ca, Cd, Cu, Fe, K, Mg, Mn, Mo and Zn in grains of sunflower (Helianthus annuus) grown in nutrient solution: root uptake or remobilization from vegetative organs?

  • Olaia Liñero
  • Jean-Yves Cornu
  • Alberto de Diego
  • Sylvie Bussière
  • Cécile Coriou
  • Stéphane Thunot
  • Thierry Robert
  • Christophe Nguyen
Regular Article



This study investigated the possible source organs delivering several trace elements to seeds (root uptake versus net remobilization), by studying changes in biomass and element contents in the plant organs.


Sunflowers were grown in a greenhouse using a nutrient solution enriched with Cd. Four samplings were performed from the early flowering to the seeds physiological maturity.


The low grain Ca indicated that phloem was likely the main route for transporting the elements to seeds. Excluding roots, the mass balance of the elements indicated the following contribution of the net remobilization to the total quantities in seeds at maturity: Mg = 50%, Cd = 14%, Cu = 35%, Fe = 29%, Mn = 19%, Zn = 12%. Source organs were mainly the receptacle and the stem. No significant net remobilization was observed for Ca, K and Mo.


The amount of trace elements accumulated in vegetative parts can be redistributed to seeds in an extent that depended on the element. Due to the important contribution of root uptake to the content in seeds at maturity, the availability of elements in soil during the reproductive stages is an important point to consider.


Net remobilization Partitioning Root uptake Sunflower (Helianthus annuusTrace elements 



This work has been financially supported by the French National Research Agency through the SIM-TRACES (ANR-11-CESA-0008) Project.

O. Liñero is grateful to the University of the Basque Country (UPV/EHU) and the University of Bordeaux for her predoctoral fellowship, within the framework of the Cross-Border Euroregional Campus of International Excellence IdEx Bordeaux – Euskampus.

The authors are grateful to L. Augusto for his helpful contribution as internal reviewer of this manuscript.

Supplementary material

11104_2017_3552_MOESM1_ESM.pdf (35 kb)
Online Resource 1 (PDF 34 kb)


  1. Alkio M, Grimm E (2003) Vascular connections between the receptacle and empty achenes in sunflower (Helianthus annuus L.) J Exp Bot 54:345–348CrossRefPubMedGoogle Scholar
  2. Andriunas FA, Zhang HM, Xia X, Patrick JW, Offler CE (2013) Intersection of transfer cells with phloem biology—broad evolutionary trends, function, and induction. Front Plant Sci 4:221CrossRefPubMedPubMedCentralGoogle Scholar
  3. Arduini I, Masoni A, Mariotti M, Pampana S, Ercoli L (2014) Cadmium uptake and translocation in durum wheat varieties differing in grain-cd accumulation. Plant Soil Environ 60:43–49CrossRefGoogle Scholar
  4. Bennett AB, Sweger BL, Spanswick RM (1984) Sink to source translocation in soybean. Plant Physiol 74:434–436CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bittner F (2014) Molybdenum metabolism in plants and crosstalk to iron. Front Plant Sci 5:1–6CrossRefGoogle Scholar
  6. Brown PH, Welch RM, Cary EE (1987) Nickel: a micronutrient essential for higher plants. Plant Physiol 85:801–803CrossRefPubMedPubMedCentralGoogle Scholar
  7. Buckley WT, Buckley KE, Huang JJ (2010) Root cadmium desorption methods and their evaluation with compartmental modeling. New Phytol 188:280–290CrossRefPubMedGoogle Scholar
  8. Burkhead JL, Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 128:799–816CrossRefGoogle Scholar
  9. Chamer AM, Medan D, Mantese AI, Bartoloni NJ (2015) Impact of pollination on sunflower yield: is pollen amount or pollen quality what matters? Field Crop Res 176:61–70CrossRefGoogle Scholar
  10. Curie C, Cassin G, Couch D, Divol F, Higuchi K, Le Jean M, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11CrossRefPubMedGoogle Scholar
  11. Degryse F, Smolders E, Parker DR (2006) Metal complexes increase uptake of Zn and Cu by plants: implications for uptake and deficiency studies in chelator-buffered solutions. Plant Soil 289:171–185CrossRefGoogle Scholar
  12. Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives (2nd ed.). Sinauer Associates, SunderlandGoogle Scholar
  13. Flis P, Ouerdanen L, Grillet L, Curie C, Mari S, Lobinski R (2016) Inventory of metal complexes circulating in plant fluids: a reliable method based on HPLC coupled with dual elemental and high-resolution molecular mass spectrometric detection. New Phytol 211:1129–1141CrossRefPubMedGoogle Scholar
  14. Frick H, Pizzolato TD (1987) Adaptive value of the xylem discontinuity in partitioning of photoassimilate to the grain. Bull Torrey Bot Club 114:252–259CrossRefGoogle Scholar
  15. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613CrossRefPubMedGoogle Scholar
  16. Hall AJ, Connor DJ, Whitfield DM (1989) Contribution of pre-anthesis assimilates to grain-filling in irrigated and water-stressed sunflower crops I. estimates using labelled carbon. Field Crop Res 20:95–112CrossRefGoogle Scholar
  17. 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 52:1473–1481CrossRefPubMedGoogle Scholar
  18. Harris NS, Taylor GJ (2013) Cadmium uptake and partitioning in durum wheat during grain filling. BMC Plant Biol 13:103CrossRefPubMedPubMedCentralGoogle Scholar
  19. Harris WR, Sammons RD, Grabiak RC (2012) A speciation model of essential trace metal ions in phloem. J Inorg Biochem 116:140–150CrossRefPubMedGoogle Scholar
  20. Hart JJ, Welch RM, Norvell WA, Kochian LV (2006) Characterization of cadmium uptake, translocation and storage in near-isogenic lines of durum wheat that differ in grain cadmium concentration. New Phytol 172:261–271CrossRefPubMedGoogle Scholar
  21. Himelblau E, Amasino RM (2001) Nutrients mobilized from leaves of arabidopsis thaliana during leaf senescence. J Plant Physiol 158:1317–1323CrossRefGoogle Scholar
  22. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. circular 347 (3rd ed.). California Agricultural Experiment Station. The College of Agriculture, University of California, BerkeleyGoogle Scholar
  23. Hocking PJ, Steer BT (1983) Uptake and partitioning of selected mineral elements in sunflower (Helianthus annuus L.) during growth. Field Crop Res 6:93–107CrossRefGoogle Scholar
  24. Karley AJ, White PJ (2009) Moving cationic minerals to edible tissues: potassium, magnesium, calcium. Curr Opin Plant Biol 23:291–298CrossRefGoogle Scholar
  25. 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 5:51CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kochian LV (1991) Mechanisms of micronutrient uptake and translocation in plants. In: Mortvedt JJ, Cox FR, Shuman LM, Welch RM (eds) Micronutrients in agriculture. Soil Science Society of America, Inc., Madison, p 229–296Google Scholar
  27. Koen E, Besson-Bard A, Duc C, Astier J, Gravot A, Richaud P, Lamotte O, Boucherez J, Gaymard F, Wendehenne D (2013) Arabidopsis thaliana nicotianamine synthase 4 is required for proper response to iron deficiency and to cadmium exposure. Plant Sci 209:1–11CrossRefPubMedGoogle Scholar
  28. Kumar A, Singh UM, Manohar M, Gaur VS (2015) Calcium transport from source to sink: understanding the mechanism(s) of acquisition, translocation, and accumulation for crop biofortification. Acta Physiol Plant 37:1722CrossRefGoogle Scholar
  29. Küpper H, Kochian LV (2010) Transcriptional regulation of metal transport genes and mineral nutrition during acclimatization to cadmium and zinc in the Cd/Zn hyperaccumulator, Thlaspi caerulescens (ganges population). New Phytol 185:14–129CrossRefGoogle Scholar
  30. 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 361:177–187CrossRefGoogle Scholar
  31. Kutrowska A, Szelag M (2014) Low-molecular weight organic acids and peptides involved in the long-distance transport of trace metals. Acta Physiol Plant 36:1957–1968CrossRefGoogle Scholar
  32. Lindström LI, Pellegrini CN, Hernández LF (2007) Histological development of the sunflower fruit pericarp as affected by pre- and early post-anthesis canopy shading. Field Crop Res 103:229–238CrossRefGoogle Scholar
  33. Macnicol RD, Beckett PHT (1985) Critical tissue concentrations of potentially toxic elements. Plant Soil 8:107–129CrossRefGoogle Scholar
  34. Maillard A, Diquélou S, Billard V, Laîné 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 6:317CrossRefPubMedPubMedCentralGoogle Scholar
  35. Marschner H, Marschner P (2012) Marschner’s mineral nutrition of higher plants, 3rd edition. Academic Press, San DiegoGoogle Scholar
  36. Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562CrossRefPubMedPubMedCentralGoogle Scholar
  37. Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2003) Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol 54:431–454CrossRefPubMedGoogle Scholar
  38. Olsen LI, Palmgren MG (2014) Many rivers to cross: the journey of zinc from soil to seed. Front Plant Sci 5:30PubMedPubMedCentralGoogle Scholar
  39. Page V, Feller U (2015) Heavy metals in crop plants: transport and redistribution processes on the whole plant level. Agronomy 5:447–463CrossRefGoogle Scholar
  40. Pate JS, Peoples MB, van Bel AJ, Kuo J, Atkins CA (1985) Diurnal water balance of the cowpea fruit. Plant Physiol 77:148–156CrossRefPubMedPubMedCentralGoogle Scholar
  41. Patrick JW, Offler CE (2001) Compartmentation of transport and transfer events in developing seeds. J Exp Bot 52:551–564CrossRefPubMedGoogle Scholar
  42. Patrick JW, Zhang WH, Tyerman SD, Offler CE, Walker NA (2001) Role of membrane transport in phloem translocation of assimilates and water. Aust J Plant Physiol 13:695–707Google Scholar
  43. Pearson J, Rengel Z (1994) Distribution and remobilization of Zn and Mn during grain development in wheat. J Exp Bot 45:1829–1835CrossRefGoogle Scholar
  44. Pearson JN, Rengel Z, Jenner CF, Graham RD (1995) Transport of zinc and manganese to developing wheat grains. Physiol Plantarum 95:449–455CrossRefGoogle Scholar
  45. Rauser WE (1987) Compartmental efflux analysis and removal of extracellular cadmium from roots. Plant Physiol 85:62–65CrossRefPubMedPubMedCentralGoogle Scholar
  46. Rawson H, Constable G (1980) Carbon production of sunflower cultivars in field and controlled environments. I photosynthesis and transpiration of leaves, stems and heads. Aust J Plant Physiol 7:555–573CrossRefGoogle Scholar
  47. Riesen O, Feller U (2005) Redistribution of nickel, cobalt, manganese, zinc, and cadmium via the phloem in young and maturing wheat. J Plant Nutr 28:421–430CrossRefGoogle Scholar
  48. Schmidt SB, Jensen PE, Husted S (2016) Manganese deficiency in plants: the impact on photosystem II. Trends Plant Sci 21:622–632CrossRefPubMedGoogle Scholar
  49. Shi R, Weber G, Köster J, Reza-Hajirezaei M, Zou C, Zhang F, Von Wirén N (2012) Senescence-induced iron mobilization in source leaves of barley (Hordeum vulgare) plants. New Phytol 195:372–383CrossRefPubMedGoogle Scholar
  50. Socha AL, Guerinot ML (2014) Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Front Plant Sci 5:106CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sperotto RA (2013) Zn/Fe remobilization from vegetative tissues to rice seeds: should I stay or should I go? Ask Zn/Fe supply! Plant Nutr 4:464Google Scholar
  52. Steer BT, Hocking PJ, Low A (1988) Dry matter, minerals and carbohydrates in the capitulum of sunflower (Helianthus annuus): effects of competition between seeds, and defoliation. Field Crop Res 18:71–85CrossRefGoogle Scholar
  53. Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15:1263–1280PubMedPubMedCentralGoogle Scholar
  54. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. In: Springer series in wood science, 2nd ed. Springer-Verlag Berlin Heidelberg, BerlinGoogle Scholar
  55. Wang Y, Wu WH (2013) Potassium transport and signaling in higher plants. Annu Rev Plant Biol 64:451–476CrossRefPubMedGoogle Scholar
  56. Waters B, Grusak MA (2008) Whole-plant mineral partitioning throughout the life cycle in Arabidopsis thaliana ecotypes Columbia, Landsberg erecta, Cape Verde Islands, and the mutant line ysl1ysl3. New Phytol 177:389–405PubMedGoogle Scholar
  57. Waters BM, Sankaran RP (2011) Moving micronutrients from the soil to the seeds: genes and physiological processes from a biofortification perspective. Plant Sci 180:562–574CrossRefPubMedGoogle Scholar
  58. Wegner LH (2014) Root pressure and beyond: energetically uphill water transport into xylem vessels? J Exp Bot 65:381–393CrossRefPubMedGoogle Scholar
  59. 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 63:2729–2737CrossRefPubMedPubMedCentralGoogle Scholar
  60. Yamaji N, Ma JF (2014) The node, a hub for mineral nutrient distribution in graminaceous plants. Trends Plant Sci 19:556–563CrossRefPubMedGoogle Scholar
  61. Zhang W, Zhou Y, Dibley KE, Tyerman SD, Furbank RT, Patrick JW (2007) Nutrient loading of developing seeds. Funct Plant Biol 34:314–331CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.ISPA, INRA, Bordeaux Science AgroVillenave d’OrnonFrance
  2. 2.Department of Analytical Chemistry, Faculty of Science and TechnologyUniversity of the Basque Country (UPV/EHU)BilbaoSpain

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