A Novel Prokaryote-Type ECF/ABC Transporter Module in Chloroplast Metal Homeostasis

Abstract

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.

The developmental and iron nutritional pattern of PIC1 and NiCo does not support their interdependent and exclusive collaboration in chloroplast iron transport in Brassica napus

“…Recently, it was excluded that Yellow Stripe-like family transporters would have a significant role in the Fe acquisition of chloroplasts that neither utilize Fe-nicotianamine complexes in their Fe uptake nor Yellow Stripe-like 4 showed expression in leaves in Brassica napus (Müller et al 2019). In Arabidopsis, ABC transporters, especially the non-intrinsic ABC protein 14, also have a role in chloroplast Fe homeostasis (Shimoni-Shor et al 2010;Voith von Voithenberg et al 2019) and the presence of Mitoferrin-like 1 protein is predicted in chloroplasts, too. The expression of Mitoferrin-like 1 is up-regulated by the excess of Fe (Tarantino et al 2011).…”

Evolutionary history of ATP‐binding cassette proteins

“…An example are a structurally unique type of importers called the Energy‐Coupling Factor (ECF) transporters [35] that are a sister branch to the clade of type I importer NBDs. Interestingly, this clade also contains NBDs classified as ABCI proteins in plants that are thought to be remnants from the biogenesis of chloroplasts from cyanobacteria [12,36]. Similarly, the NBDs of a clade of exporters unique to prokaryotes and archaea [37] (type IV) seems to be derived from the NBDs of type I importers (Fig.…”

The OsABCI7 Transporter Interacts with OsHCF222 to Stabilize the Thylakoid Membrane in Rice

“…Plants share the specific bacterial-type ABC transporters with prokaryotes, designed as ABCI subgroup. In Arabidopsis (Arabidopsis thaliana), both chloroplast-localized AtABCI10 and AtABCI11 (AtNAP14) proteins participate in the regulation of chloroplast metal homeostasis, and their corresponding T-DNA mutants are totally devoid of chlorophylls with severely deformed leaf structures, aberrant chloroplasts and defective photosynthetic capacity (Shimoni-Shor et al, 2010;Voith von Voithenberg et al, 2019). In rice (Oryza sativa), OsABCI8 is indispensable for chloroplast development by engaging iron transportation and homeostasis (Zeng et al, 2017).…”

“…5I-K). Taken together, we conclude that OsABCI7 plays a crucial role in chloroplast biogenesis, especially under low temperature stress and in the greening process.The homologue of rice OsABCI7, Arabidopsis AtABCI11 (AtNAP14), participates in the regulation of chloroplast metal homeostasis and attaches to the inner envelop membrane of the chloroplast; compared to the wild-type (Col-0), metal elemental contents including iron (Fe), Zinc (Zn), molybdenum (Mo), copper (Cu) are higher, while manganese (Mn) is lower in Atabci11 mutant shoot tissues, whereas Fe and Zn contents in Atabci11 were lower than those of Col-0 in root tissues(Shimoni-Shor et al, 2010;Voith von Voithenberg et al, 2019). Hence, we determined the contents of metal elements, including magnesium (Mg), potassium (K), Fe, Cu and Zn in the shoot and root tissues of WT and cnl1.…”