Inner Envelope CHLOROPLAST MANGANESE TRANSPORTER 1 Supports Manganese Homeostasis and Phototrophic Growth in Arabidopsis

Abstract

Manganese (Mn) is an essential catalytic metal in the Mn-cluster that oxidizes water to produce oxygen during photosynthesis. However, the transport protein(s) responsible for Mn²⁺ import into the chloroplast remains unknown. Here, we report the characterization of Arabidopsis CMT1 (Chloroplast Manganese Transporter 1), an evolutionarily conserved protein in the Uncharacterized Protein Family 0016 (UPF0016), that is required for manganese accumulation into the chloroplast. CMT1 is expressed primarily in green tissues, and its encoded product is localized in the inner envelope membrane of the chloroplast. Disruption of CMT1 in the T-DNA insertional mutant cmt1-1 resulted in stunted plant growth, defective thylakoid stacking, and severe reduction of photosystem II complexes and photosynthetic activity. Consistent with reduced oxygen evolution capacity, the mutant chloroplasts contained less manganese than the wild-type ones. In support of its function as a Mn transporter, CMT1 protein supported the growth and enabled Mn²⁺ accumulation in the yeast cells of Mn²⁺-uptake deficient mutant (Δsmf1). Taken together, our results indicate that CMT1 functions as an inner envelope Mn transporter responsible for chloroplast Mn²⁺ uptake.

Keywords: chloroplast inner envelope; manganese transporter; metal transport; oxygen-evolving complex.