First published online March 16, 2005; 10.1105/tpc.104.030452
The Plant Cell 17:1233-1251 (2005)
© 2005 American Society of Plant Biologists
Two P-Type ATPases Are Required for Copper Delivery in Arabidopsis thaliana Chloroplasts
Salah E. Abdel-Ghanya,
Patricia Müller-Mouléb,1,
Krishna K. Niyogib,
Marinus Pilona,2 and
Toshiharu Shikanaic
a Biology Department, Colorado State University, Fort Collins, Colorado 80523
b Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102
c Graduate School of Agriculture, Kyushu University, Fukuoka 812-8581, Japan
2 To whom correspondence should be addressed. E-mail pilon{at}lamar.colostate.edu; fax 970-491-0649.
Copper delivery to the thylakoid lumen protein plastocyanin and the stromal enzyme Cu/Zn superoxide dismutase in chloroplasts is required for photosynthesis and oxidative stress protection. The copper delivery system in chloroplasts was characterized by analyzing the function of copper transporter genes in Arabidopsis thaliana. Two mutant alleles were identified of a previously uncharacterized gene, PAA2 (for P-type ATPase of Arabidopsis), which is required for efficient photosynthetic electron transport. PAA2 encodes a copper-transporting P-type ATPase with sequence similarity to PAA1, which functions in copper transport in chloroplasts. Both proteins localized to the chloroplast, as indicated by fusions to green fluorescent protein. The PAA1 fusions were found in the chloroplast periphery, whereas PAA2 fusions were localized in thylakoid membranes. The phenotypes of paa1 and paa2 mutants indicated that the two transporters have distinct functions: whereas both transporters are required for copper delivery to plastocyanin, copper delivery to the stroma is inhibited only in paa1 but not in paa2. The effects of paa1 and paa2 on superoxide dismutase isoform expression levels suggest that stromal copper levels regulate expression of the nuclear genes IRON SUPEROXIDE DISMUTASE1 and COPPER/ZINC SUPEROXIDE DISMUTASE2. A paa1 paa2 double mutant was seedling-lethal, underscoring the importance of copper to photosynthesis. We propose that PAA1 and PAA2 function sequentially in copper transport over the envelope and thylakoid membrane, respectively.
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