The GHOST terminal oxidase regulates developmental programming in tomato fruit

ABSTRACT The tomato ghost and Arabidopsis immutans variegation mutants define orthologous genes for a chloroplast quinol oxidase that bears similarity to the mitochondrial alternative oxidase. In this study tomato fruit ripening was used as a model to explore the function of this oxidase. It was found that a lack of GH impacts the biogenesis of chloroplasts and chromoplasts, as well as pericarp tissue morphogenesis, during the ripening process. Most ripening‐related genes are expressed normally during gh fruit development, but late in the process there is a specific repression of mRNA accumulation from carotenoid biosynthetic genes, perhaps due to retrograde (plastid‐to‐nucleus) signalling pathways mediated by lycopene. Metabolic profiling revealed that wild‐type red‐ripe fruit accumulate multiple isomers of phytoene, phytofluene, and ζ ‐carotene, but that the composition of these isomers is different in ripe gh fruit. Profiling also revealed that there is an enhanced ratio of β ‐carotene to lycopene in the ripe gh fruit. This explains the orange colour of these fruit, and is consistent with the proposal that the β ‐cyclization step plays a pivotal role in regulating the partitioning of pathway intermediates. The total carotenoid content of the mutant fruit is significantly higher than normal due to an accumulation of phytoene. Phytoene accumulation, together with an up‐regulation of GH transcripts during ripening, supports the notion that GH plays a central role in carotenogenesis in chromoplasts. However, GH mRNAs are also expressed in tissues and organs other than fruit. This is consistent with the possibility that GH mediates quinol oxidation from a variety of pathways that converge on plastoquinol in plastid membranes.