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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Plant Sci. | doi: 10.3389/fpls.2019.01264

A novel prokaryote-type ECF/ABC transporter module in chloroplast metal homeostasis

Lena Voith von Voithenberg1,  Jiyoung Park2, Roland Stübe1, Christopher Lux3,  Youngsook Lee4 and  Katrin Philippar5*
  • 1Ludwig Maximilian University of Munich, Germany
  • 2University of California, San Diego, United States
  • 3Plant Biology, Center for Human- and Molecular Biology (ZHMB), Saarland University, Germany
  • 4Pohang University of Science and Technology, South Korea
  • 5Saarland University, Germany

During evolution, chloroplasts, which originated by endosymbiosis of a prokaryotic ancestor of today’s cyanobacteria with a eukaryotic host cell, were established as the site for photosynthesis. Therefore, chloroplast organelles are loaded with transition metals including iron, copper, and manganese, which are essential for photosynthetic electron transport due to their redox capacity. Although transport, storage and cofactor-assembly of metal ions in chloroplasts are tightly controlled and crucial throughout plant growth and development, knowledge on the molecular nature of chloroplast metal-transport proteins is still fragmentary. Here we characterized the soluble, ATP-binding ABC-transporter subunits ABCI10 and ABCI11 in Arabidopsis thaliana, which show similarities to components of prokaryotic, multisubunit ABC transporters. Both ABCI10 and ABCI11 proteins appear to be strongly attached to chloroplast-intrinsic membranes, most likely inner envelopes for ABCI10 and possibly plastoglobuli for ABCI11. Loss of ABCI10 and ABCI11 gene products in Arabidopsis leads to extremely dwarfed, albino plants showing impaired chloroplast biogenesis and deregulated metal homeostasis. Further, we identified the membrane-intrinsic protein ABCI12 as potential interaction partner for ABCI10 in the inner envelope. Our results suggest that ABCI12 inserts into the chloroplast inner envelope membrane most likely with five predicted α-helical transmembrane domains and represents the membrane-intrinsic subunit of a prokaryotic-type, energy-coupling factor (ECF) ABC-transporter complex. In bacteria these multisubunit ECF importers are widely distributed for the uptake of nickel and cobalt metal ions as well as for import of vitamins and several other metabolites. Therefore, we propose that ABCI10 (as the ATPase A-subunit) and ABCI12 (as the membrane-intrinsic, energy-coupling T-subunit) are part of a novel, chloroplast envelope-localized, AAT energy-coupling module of a prokaryotic-type ECF transporter, most likely involved in metal ion uptake.

Keywords: ABC transporter, chloroplast, Energy-coupling factor transporter, inner envelope membrane, metal transport, metal homeostasis

Received: 13 Feb 2019; Accepted: 11 Sep 2019.

Copyright: © 2019 Voith von Voithenberg, Park, Stübe, Lux, Lee and Philippar. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Katrin Philippar, Saarland University, Saarbrücken, 66123, Saarland, Germany, katrin.philippar@uni-saarland.de