The IMMUTANS Variegation Locus of Arabidopsis Defines a Mitochondrial Alternative Oxidase Homolog That Functions during Early Chloroplast Biogenesis

Abstract

Nuclear gene-induced variegation mutants provide a powerful system to dissect interactions between the genetic systems of the nucleus-cytoplasm, the chloroplast, and the mitochondrion. The immutans (im) variegation mutation of Arabidopsis is nuclear and recessive and results in the production of green- and white-sectored leaves. The green sectors contain cells with normal chloroplasts, whereas the white sectors are heteroplastidic and contain cells with abnormal, pigment-deficient plastids as well as some normal chloroplasts. White sector formation can be promoted by enhanced light intensities, but sectoring becomes irreversible early in leaf development. The white sectors accumulate the carotenoid precursor phytoene. We have positionally cloned IM and found that the gene encodes a 40.5-kD protein with sequence motifs characteristic of alternative oxidase, a mitochondrial protein that functions as a terminal oxidase in the respiratory chains of all plants. However, phylogenetic analyses revealed that the IM protein is only distantly related to these other alternative oxidases, suggesting that IM is a novel member 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 redox chain responsible for phytoene desaturation but that a redundant electron transfer function is capable of compensating for IM activity in some plastids and cells.

The Arabidopsis Spontaneous Cell Death1 gene, encoding a ζ-carotene desaturase essential for carotenoid biosynthesis, is involved in chloroplast development, photoprotection and retrograde signalling

“…These developmental defects are partly attributed to the loss of or reduced carotenoid-mediated antioxidant activity, impaired chlorophyll biosynthesis and reduced PS II capacity [4,[26][27][28]. Moreover, the ABAdeficient phenotype is often associated with precocious seed germination (viviparous), reduced seed dormancy and compromised stress response [10].…”

Activation of the Stt7/STN7 Kinase through Dynamic Interactions with the Cytochrome b6f Complex

“…In the case of overreduction of the acceptor side of PSI, excess electrons can reduce molecular oxygen through the Mehler reaction to superoxide, which is then converted to hydrogen peroxide by a plastid superoxide dismutase and ultimately to water by a peroxidase (Asada, 2000). Over-reduction of the PQ pool can be alleviated by PTOX, the plastid terminal oxidase responsible for oxidizing PQH 2 to form hydrogen peroxide, which is subsequently converted to water (Carol et al, 1999;Cournac et al, 2000;Wu et al, 1999).…”

Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis

“…Another Arabidopsis mutant, immutans, accumulates phytoene in variegated white tissues. The IMMUTANS gene encodes plastid terminal oxidase, the disruption of which prevents oxidation during chlorophyll biosynthesis and results in the accumulation of phytoene [16,17]. However, mutations in the gene encoding the phytoene desaturase itself (designated PDS3) [14] have not been reported.…”

“…First-strand cDNA synthesis was performed in a 20-µL-reaction volume consisting of 3 µg of total RNA, oligodT [12][13][14][15][16][17][18] and SuperScript TM reverse transcriptase (GIBCO BRL). The reaction was allowed to proceed at 42 ºC for 50 min before being terminated by treatment at 70 ºC for 15 min.…”