Chloroplast magnesium transporters play essential but differential roles in maintaining magnesium homeostasis

Magnesium (Mg2+) is essential for photosynthesis in the chloroplasts of land plantsand algae. Being the central ion of chlorophyll, cofactor and activator of manyphotosynthetic enzymes including RuBisCO, magnesium-deficient plants may sufferfrom leaf chlorosis symptoms and retarded growth. Therefore, the chloroplast Mg2+concentration is tightly controlled by magnesium transport proteins. Recently, threedifferent transporters from two distinct families have been identified in thechloroplast inner envelope of the model plant Arabidopsis thaliana: MGT10,MGR8, and MGR9. Here, we assess the individual roles of these three proteins inmaintaining chloroplast Mg2+ homeostasis and regulating photosynthesis, and iftheir role is conserved in the model green alga Chlamydomonas reinhardtii.Phylogenetic analysis and heterologous expression revealed that the CorC-likeMGR8 and MGR9 transport Mg2+ by a different mechanism than the CorA-likeMGT10. MGR8 and MGT10 genes are highest expressed in leaves, indicating afunction in chloroplast Mg2+ transport. MGR9 is important for chloroplast functionand plant adaptation in conditions of deficiency or excess of Mg2+. Transmissionelectron microscopy indicated that MGT10 plays a differential role in thylakoidstacking than MGR8 and MGR9. Furthermore, we report that MGR8, MGR9, andMGT10 are involved in building up the pH gradient across the thylakoid membraneand activating photoprotection in conditions of excess light, however themechanism has not been resolved yet. While there are no chloroplast MGR-liketransporters in Chlamydomonas, we show that MRS4 is a homolog of MGT10, that isrequired for photosynthesis and cell growth. Taken together, our findings reveal thatthe studied Mg2+ transporters play essential but differential roles in maintainingchloroplast Mg2+ homeostasis.