The immutans variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis

Nuclear gene-induced variegation mutants provide a powerful system to disse ct interactions between the genetic systems of the nucleus-cytoplasm, the c hloroplast, and the mitochondrion. The immutans (im) variegation mutation o f Arabidopsis is nuclear and recessive and results in the production of gre en- and white-sectored leaves. The green sectors contain cells with normal chloroplasts, whereas the white sectors are heteroplastidic and contain cel ls with abnormal, pigment-deficient plastids as well as some normal chlorop lasts. White sector formation can be promoted by enhanced light intensities , but sectoring becomes irreversible early in leaf development. The white s ectors accumulate the carotenoid precursor phytoene. We have positionally c loned IM and found that the gene encodes a 40.5-kD protein with sequence mo tifs characteristic of alternative oxidase, a mitochondrial protein that fu nctions as a terminal oxidase in the respiratory chains of all plants. Howe ver, phylogenetic analyses revealed that the IM protein is only distantly r elated to these other alternative oxidases, suggesting that IM is a novel m ember of this protein class. We sequenced three alleles of im, and all are predicted to be null. Our data suggest a model of variegation in which the IM protein functions early in chloroplast biogenesis as a component of a re dox chain responsible for phytoene desaturation but that a redundant electr on transfer function is capable of compensating for IM activity in some pla stids and cells.