title: Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis.
abstract: 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. 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. 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.affiliation: Department of Chemistry and Biochemistry, and.
authors.forename: Crysten E
authors.initials: CE
authors.lastname: Blaby-Haas
authors.affiliation: Department of Chemistry and Biochemistry, Worcester Polytechnic Institute, Worcester, MA 01609.
authors.forename: Teresita
authors.initials: T
authors.lastname: Padilla-Benavides
authors.affiliation: Department of Chemistry and Biochemistry, and.
authors.forename: Roland
authors.initials: R
authors.lastname: Stübe
authors.affiliation: Department of Chemistry and Biochemistry, Worcester Polytechnic Institute, Worcester, MA 01609.
authors.forename: José M
authors.initials: JM
authors.lastname: Argüello
authors.affiliation: Department of Chemistry and Biochemistry, and Institute of Genomics and Proteomics, University of California, Los Angeles, CA 90095; and sabeeha@chem.ucla.edu.
authors.forename: Sabeeha S
authors.initials: SS
authors.lastname: Merchant
mesh_terms: D017360:Arabidopsis / Q000235:genetics*; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D016825:Chlamydomonas reinhardtii / Q000235:genetics; D025222:Chloroplast Proton-Translocating ATPases / Q000378:metabolism; D002736:Chloroplasts / Q000378:metabolism / Q000502:physiology*; D003001:Cloning, Molecular; D019295:Computational Biology; D003300:Copper / Q000378:metabolism*; D019143:Evolution, Molecular; D006706:Homeostasis / Q000502:physiology*; D015151:Immunoblotting; D056511:Metallochaperones / Q000235:genetics* / Q000378:metabolism; D013482:Superoxide Dismutase / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D056511:Metallochaperones; C000597337:PCH1 protein, Arabidopsis; D003300:Copper; D013482:Superoxide Dismutase; D025222:Chloroplast Proton-Translocating ATPases; C477511:PAA1 protein, Arabidopsis
keywords: Arabidopsis thaliana; Atx1; Cu-transfer; inner envelope; metal transporter