Does a voltage-sensitive outer envelope transport mechanism contributes to the chloroplast iron uptake?
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Based on the effects of inorganic salts on chloroplast Fe uptake, the presence of a voltage-dependent step is proposed to play a role in Fe uptake through the outer envelope.
Although iron (Fe) plays a crucial role in chloroplast physiology, only few pieces of information are available on the mechanisms of chloroplast Fe acquisition. Here, the effect of inorganic salts on the Fe uptake of intact chloroplasts was tested, assessing Fe and transition metal uptake using bathophenantroline-based spectrophotometric detection and plasma emission-coupled mass spectrometry, respectively. The microenvironment of Fe was studied by Mössbauer spectroscopy. Transition metal cations (Cd2+, Zn2+, and Mn2+) enhanced, whereas oxoanions (NO3 −, SO4 2−, and BO3 3−) reduced the chloroplast Fe uptake. The effect was insensitive to diuron (DCMU), an inhibitor of chloroplast inner envelope-associated Fe uptake. The inorganic salts affected neither Fe forms in the uptake assay buffer nor those incorporated into the chloroplasts. The significantly lower Zn and Mn uptake compared to that of Fe indicates that different mechanisms/transporters are involved in their acquisition. The enhancing effect of transition metals on chloroplast Fe uptake is likely related to outer envelope-associated processes, since divalent metal cations are known to inhibit Fe2+ transport across the inner envelope. Thus, a voltage-dependent step is proposed to play a role in Fe uptake through the chloroplast outer envelope on the basis of the contrasting effects of transition metal cations and oxoaninons.
KeywordsChloroplast Envelope membrane Iron metabolism Mössbauer spectrosopy Voltage-dependent transport
Light Harvesting Complex II apoprotein
Carbonyl cyanide m-chlorophenyl-hydrazone
Transmembrane electrochemical potential
Rubisco large subunit
This work was supported by the Grants financed by the National Office for Research, Development, and Innovation, Hungary (OTKA-NKFIH PD-112047 and PD-111979), the Spanish Ministry of Economy and Competitivity (Project AGL2013–42175-R, co-financed with FEDER) and the Aragón Government (Group A03) to J.A. Á.S. was also supported by the Bolyai János Research Scholarship of the Hungarian Academy of Sciences (BO/00207/15/4).
- Braun V (2014) Energy-coupled transport across the outer membrane of Gram-negative bacteria. In: Remaut H, Frozens R (eds) Bacterial membranes: Structural and molecular biology. Caister Academic Press, Norfolk, pp 249–282Google Scholar
- Breuers FKH, Bräutigam A, Weber APM (2011) The plastid outer envelope–a highly dynamic interface between plastid and cytoplasm. Front Plant Scie 2:97Google Scholar
- Castagna A, Donnini S, Ranieri A (2009) Adaptation to iron-deficiency requires remodelling of plant metabolism: an insight in chloroplast biochemistry and functionality. In: Ashraf M, Ozturk, H-u-R Athar M (eds) Salinity and water stress. Springer Verlag, Dordrecht, p 205–212Google Scholar
- Gutierrez-Carbonell E, Takahashi D, Lattanzio G, Rodríguez-Celma J, Kehr J, Soll J, Philippar K, Uemura M, Abadía J, López-Millán AF (2014) The distinct functional roles of the inner and outer chloroplast envelope of pea (Pisum sativum) as revealed by proteomic approaches. J Prot Res 13:2941–2953CrossRefGoogle Scholar
- Nikolić M, Römheld V (2007) The dynamics of iron in the leaf apoplast significance for the iron nutrition of plants. In: Sattelmacher B, Horst WJ (eds) The apoplast of higher plants: Compartment of storage, transport and reactions. The significance of the apoplast for the mineral nutrition of higher plants. Springer Verlag, Dordrecht, pp 353–371Google Scholar
- Rellán-Alvarez R, Giner-Martínez-Sierra J, Orduna J, Orera I, Rodríguez-Castrillón JA, García-Alonso JI, Abadía J, Alvarez-Fernández A (2010) Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant Cell Physiol 51:91–102CrossRefPubMedGoogle Scholar
- Rodríguez-Serrano M, Romero-Puertas MC, Pazmiňo DM, Testillano PS, Risueňo MC, del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243CrossRefPubMedPubMedCentralGoogle Scholar