The chloroplast ionome shines light on the dynamics of organellar iron homeostasis

Annually, chloroplasts fix 258 billion tons of CO2 through photosynthesis. Photosynthesis and other biochemical pathways require specific amounts of metal ions in the organelle. Transport proteins in the plastid inner envelope maintain the organellar ion homeostasis. Despite substantial progress over the last decades, many genes encoding plastid ion channels and ion carriers or their regulators remain unknown. To fill this knowledge gap, detailed information on the elemental composition of chloroplasts ie, a plastid ionome, is needed. This will allow us to compare mutants of transporter candidates with wild-type plants. Here, we provide quantitative descriptions of chloroplast ionomes from Arabidopsis thaliana, the metal hyperaccumulator Arabidopsis halleri, Pisum sativum, and Nicotiana benthamiana and analyze similarities and distinctions. Using A. thaliana, we show that plastid ionomes can be genetically manipulated. Chloroplasts of OLIGOPEPTIDE TRANSPORTER3 (OPT3)-deficient mutants contain 14-fold more iron, likely associated with stromal FERRITIN. The removal of FERRITIN in opt3 mutants leads to a substantial decrease in plastid and leaf iron, pointing to an important role of ferritins in shaping the chloroplast ionome. Our study reveals that chloroplast ferritins can be turned into iron sinks. Since crop biofortification to fight hidden hunger has become a global mission, this research provides groundwork to reach this goal.