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

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Abstract

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.

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Abbreviations

FRO:

Ferric-chelate reductase/oxidase

MAR1:

Multiple antibiotic resistance 1

NA:

Nicotianamine

NiCo:

Nickel–cobalt transporter

o,o′EDDHA:

Ethylenediamine-N,N′-bis-o-hydroxyphenylacetate

PIC1:

Permease in chloroplast 1

YSL:

Yellow-stripe 1-like

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Acknowledgements

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.

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Correspondence to Ádám Solti.

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

Electronic supplementary material

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425_2018_3037_MOESM1_ESM.pdf

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

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

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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Müller, B., Kovács, K., Pham, HD. et al. Chloroplasts preferentially take up ferric–citrate over iron–nicotianamine complexes in Brassica napus. Planta 249, 751–763 (2019). https://doi.org/10.1007/s00425-018-3037-0

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  • DOI: https://doi.org/10.1007/s00425-018-3037-0

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