A plastid carbohydrate carrier mediates ribose recycling from nucleotide catabolism and glucose export from starch degradation

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In plants, nucleotide degradation releases ribose in the cytosol. An unidentified transporter then brings the ribose into the plastids for phosphorylation. This process of ribose recycling is particularly prominent in root nodules of soybean (Glycine max) and common bean (Phaseolus vulgaris) during symbiotic nitrogen fixation. In this biological context, we identified a plastid ribose transporter, which is an ortholog of the putative plastid glucose transporter (pGlcT) of Arabidopsis thaliana. We show that Arabidopsis mutants of At-pGlcT, but not of the related At-pGlcT2, accumulate ribose and fructose constitutively, whereas glucose accumulates only at night. Uridine feeding experiments leading to cytosolic ribose release indicated that At-pGlcT transports ribose from the cytosol into the plastids. Uptake assays with complemented Escherichia coli sugar transport mutants directly demonstrated that At-pGlcT transports ribose, glucose, and fructose. Ribose and fructose accumulation were also observed in CRISPR-induced bean nodule mutants of Pv-pGlcT. Additionally, our data show that ribose recycling is important for producing allantoin, a nitrogen fixation product used for nitrogen export from nodules to shoots. We conclude that pGlcT is a plastid facilitator for the import of ribose from nucleotide catabolism, for the export of glucose from nocturnal starch breakdown, and for cytosol-plastid fructose exchange in vivo.

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