Phosphite-Mediated Suppression of Anthocyanin Accumulation Regulated by Mitochondrial ATP Synthesis and Sugars in Arabidopsis

Despite the essential role of phosphate (Pi) in plant growth and development, how plants sense and signal the change of Pi supply to adjust its uptake and utilization is not yet well understood. Pi itself has been proposed to be a signaling molecule that regulates Pi starvation responses (PSRs) because phosphite (Phi), a non-metabolized Pi analog, suppresses several PSRs. In this study, we identified a phosphite-insensitive1 (phi1) mutant which retained anthocyanin, a visible PSR, in Phi-containing but Pi-deficient medium. phi1 mutants were impaired in the gene encoding an FAd subunit of mitochondrial F1Fo-ATP synthase and showed a reduced mitochondrial ATP level in roots, growth hypersensitivity to oligomycin and an increased mitochondrial membrane potential, suggesting that this gene has a crucial role in mitochondrial ATP synthesis. phi1 mutants accumulated a high level of sugars in shoots, which may account for the increased accumulation of anthocyanin and starch in Phi-containing conditions. Gene expression analysis showed that a subset of genes involved in carbohydrate metabolism in phi1 was misregulated in response to Phi. The majority of genes were repressed by Pi starvation and, unlike wild-type plants, their repression in phi1 was not affected by the addition of Phi. Our findings show that defective mitochondrial ATP synthesis results in sugar accumulation, leading to alteration of Phi-mediated suppression of PSRs. This study reinforces the role of sugars, and also reveals a cross-talk among ATP, sugars and Pi/Phi molecules in mediating PSRs.