, Volume 249, Issue 3, pp 751–763 | Cite as

Chloroplasts preferentially take up ferric–citrate over iron–nicotianamine complexes in Brassica napus

  • Brigitta Müller
  • Krisztina Kovács
  • Hong-Diep Pham
  • Yusuf Kavak
  • Jiři Pechoušek
  • Libor Machala
  • Radek Zbořil
  • Kálmán Szenthe
  • Javier Abadía
  • Ferenc Fodor
  • Zoltán Klencsár
  • Ádám SoltiEmail author
Original Article


Main conclusion

Fe uptake machinery of chloroplasts prefers to utilise Fe(III)–citrate over Fe–nicotianamine complexes.

Iron uptake in chloroplasts is a process of prime importance. Although a few members of their iron transport machinery were identified, the substrate preference of the system is still unknown. Intact chloroplasts of oilseed rape (Brassica napus) were purified and subjected to iron uptake studies using natural and artificial iron complexes. Fe–nicotianamine (NA) complexes were characterised by 5 K, 5 T Mössbauer spectrometry. Expression of components of the chloroplast Fe uptake machinery was also studied. Fe(III)–NA contained a minor paramagnetic Fe(II) component (ca. 9%), a paramagnetic Fe(III) component exhibiting dimeric or oligomeric structure (ca. 20%), and a Fe(III) complex, likely being a monomeric structure, which undergoes slow electronic relaxation at 5 K (ca. 61%). Fe(II)–NA contained more than one similar chemical Fe(II) environment with no sign of Fe(III) components. Chloroplasts preferred Fe(III)–citrate compared to Fe(III)–NA and Fe(II)–NA, but also to Fe(III)–EDTA and Fe(III)–o,o′EDDHA, and the Km value was lower for Fe(III)-citrate than for the Fe–NA complexes. Only the uptake of Fe(III)–citrate was light-dependent. Regarding the components of the chloroplast Fe uptake system, only genes of the reduction-based Fe uptake system showed high expression. Chloroplasts more effectively utilize Fe(III)–citrate, but hardly Fe–NA complexes in Fe uptake.


Bathophenanthroline disulfonate Ferric chelate reductase Gene expression Mössbauer spectroscopy Oilseed rape 



Ferric-chelate reductase/oxidase


Multiple antibiotic resistance 1




Nickel–cobalt transporter




Permease in chloroplast 1


Yellow-stripe 1-like



This work was supported by the grants financed by the National Research, Development and Innovation Office, Hungary (NKFIH PD-112047, PD-111979 and K-124159), VEKOP-2.3.3-15-2016-00008 and the Spanish Ministry of Economy and Competitiveness (MINECO; project AGL2016-75226-R, co-financed with FEDER). Á.S. was also supported by the Bolyai János Research Scholarship of the Hungarian Academy of Sciences (BO/00207/15/4). The authors (JP, LM, and RZ) gratefully acknowledge the financial support provided by the project LO1305 of the Ministry of Education, Youth and Sports of the Czech Republic.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest in relation with the submitted manuscript.

Supplementary material

425_2018_3037_MOESM1_ESM.pdf (28 kb)
Supplementary material 1 Online Resource S1 Extended evaluation of the 57Fe Mössbauer spectra of the Fe(III)–nicotianamine frozen solution (PDF 28 kb)
425_2018_3037_MOESM2_ESM.pdf (34 kb)
Supplementary material 2 Online Resource S2 Table on the 57Fe Mössbauer parameters associated with the spectra of the Fe(III)–nicotianamine frozen solution (PDF 33 kb)
425_2018_3037_MOESM3_ESM.pdf (48 kb)
Supplementary material 3 Online Resource S3 Figure on the expression of BnYsl4 in tissues and organs of different developmental stages expressed in normalised relative quantities (NRQ) (PDF 48 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Brigitta Müller
    • 1
  • Krisztina Kovács
    • 2
  • Hong-Diep Pham
    • 1
  • Yusuf Kavak
    • 1
  • Jiři Pechoušek
    • 3
  • Libor Machala
    • 3
  • Radek Zbořil
    • 3
  • Kálmán Szenthe
    • 4
  • Javier Abadía
    • 5
  • Ferenc Fodor
    • 1
  • Zoltán Klencsár
    • 6
  • Ádám Solti
    • 1
    Email author
  1. 1.Department of Plant Physiology and Molecular Plant Biology, Institute of BiologyELTE Eötvös Loránd UniversityBudapestHungary
  2. 2.Laboratory of Nuclear Chemistry, Institute of ChemistryELTE Eötvös Loránd UniversityBudapestHungary
  3. 3.Departments of Experimental Physics and Physical Chemistry, Faculty of Science, Regional Centre of Advanced Technologies and MaterialsPalacký UniversityOlomoucCzech Republic
  4. 4.RT-Europe Nonprofit Research Ltd.MosonmagyaróvárHungary
  5. 5.Department of Plant Nutrition, Aula Dei Experimental StationSpanish Council for Scientific Research (CSIC)SaragossaSpain
  6. 6.Centre for Energy Research, Hungarian Academy of SciencesBudapestHungary

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