Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis

Metallochaperones traffic copper (Cu⁺) from its point of entry at the plasma membrane to its destination. In plants, one destination is the chloroplast, which houses plastocyanin, a Cu-dependent electron transfer protein involved in photosynthesis. In this paper, we present a previously unidentified Cu⁺ chaperone that evolved early in the plant lineage by an alternative-splicing event of the pre-mRNA encoding the chloroplast P-type ATPase in Arabidopsis 1 (PAA1). In several land plants, recent duplication events created a separate chaperone-encoding gene coincident with loss of alternative splicing. The plant-specific Cu⁺ chaperone delivers Cu⁺ with specificity for PAA1, which is flipped in the envelope relative to prototypical bacterial ATPases, compatible with a role in Cu⁺ import into the stroma and consistent with the canonical catalytic mechanism of these enzymes. The ubiquity of the chaperone suggests conservation of this Cu⁺-delivery mechanism and provides a unique snapshot into the evolution of a Cu⁺ distribution pathway. Finally, we also provide evidence for an interaction between PAA2, the Cu⁺-ATPase in thylakoids, and the Cu⁺-chaperone for Cu/Zn superoxide dismutase (CCS), uncovering a Cu⁺ network that has evolved to fine-tune Cu⁺ distribution.. Authors: Blaby-Haas, Crysten E. [Univ. of California, Los Angeles, CA (United States). Dept. of Chemistry and Biochemistry; DOE Office of Scientific and Technical Information (OSTI)]; Padilla-Benavides, Teresita [Worcester Polytechnic Inst., MA (United States). Dept. of Chemistry and Biochemistry]; Stübe, Roland [Univ. of California, Los Angeles, CA (United States). Dept. of Chemistry and Biochemistry]; Argüello, José M. [Worcester Polytechnic Inst., MA (United States). Dept. of Chemistry and Biochemistry]; Merchant, Sabeeha S. [Univ. of California, Los Angeles, CA (United States). Dept. of Chemistry and Biochemistry. Inst. of Genomics and Proteomics]. DOE Contract: FC02-02ER63421. Subjects: 60 APPLIED LIFE SCIENCES; Arabidopsis thaliana; Atx1; Cu-transfer; inner envelope; metal transporter