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Chloroplast ATP synthase of spinach contains nine nonidentical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement

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We describe the nucleotide sequence of a 4.0 kilobase pair (kbp) region of the spinach plastid chromosome that encodes three subunits of the ATP synthase CF0 sector proximal to the gene for CF1 subunit alpha. The four genes are located on the same strand and form a transcriptional unit. Our study presents details about the genes and their products, resolves ambiguities in the constitution of the CF0 sector, and establishes precise gene-polypeptide relationships as well as intersubunit homologies in ATP synthases from diverse organisms. The amino acid sequences quences deduced exhibit substantial homology (30%–40%) with published sequences for the F0 subunits a, c (proteolipid) and b from E. coli and mitochondria, which therefore can be presumed to be structurally similar and functionally equivalent. Sequences comparison shows that the counterpart of CF0-I is F0-b. The homologue to the bacterial F0-a is CF0-IV, the product of a newly found gene, designated atpI. The data confirm our previous suggestion that the gene for subunit I, atpF, is split. The gene arrangement is atpI (247 codons)-692 bp spacer-atpH (proteolipid, 81 codons)-395 bp spacer-atpF (exon 1, 145 bp)-764 bp intron class II-atpI (exon 2, 410 bp)-65 bp spacer-atpA (alpha). The detection of atpI implies that the spinach CF0 sector contains four, the entire ATP synthase (CF0-CF1) nine different subunit species. The extra subunit in the membrane sector is the nuclear-encoded component CF0-II which has no known counterpart in E. coli. The six ATP synthase genes that are plastid-encoded are organized in two operons that map 40 kbp away from each other on the organelle chromosome. These transcriptional units, designated atp operons A and B, differ in their functional organisation. The plastid gene arrangement corresponds to the arrangement of genes in the atp (unc) operon of E. coli substantiating the theory that ATP synthase complexes have evolved from a common ancestor.

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Communicated by C.P. Hollenberg

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Hennig, J., Herrmann, R.G. Chloroplast ATP synthase of spinach contains nine nonidentical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement. Mol Gen Genet 203, 117–128 (1986). https://doi.org/10.1007/BF00330392

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