Multi-scale analysis provides insights into the roles of ureide permeases in wheat nitrogen use efficiency.

The ureides allantoin and allantoate serve as nitrogen (N) transport compounds in plants, and more recently, allantoin has been shown to play a role in signaling. In planta, ureide tissue levels are controlled by the activity of enzymes of the purine degradation pathway and by ureide transporters called UPS (ureide permease). Still little is known about the physiological function of UPS proteins in crop plants, and especially in monocotyledon species. Here, we identified 13 TaUPS genes in the wheat (Triticum aestivum L.) genome. Phylogenetic and genome location analyses revealed a close relationship of wheat UPSs to orthologues of grasses and a division into TaUPS1, TaUPS2.1 and TaUPS2.2 groups, each existing of three homeologs, and with a total of four tandem duplications. Expression, localization, and biochemical analyses resolved spatial-temporal expression patterns of TaUPS genes, transporter localization to the plasma membrane, and a role of TaUPS2.1 proteins in cellular import of ureides, and phloem and seed loading. In addition, positive correlations between TaUPS1 and TaUPS2.1 transcripts, and ureide levels were determined. Together the data support TaUPS function in regulating ureide pools in source and sink, and source-to-sink transport. Moreover, comparative studies between wheat cultivars grown at low and high N strengthened a role of TaUPS1 and TaUPS2.1 transporters in efficient N use and in controlling primary metabolism. Co-expression, protein-protein interaction, and haplotype analyses further support TaUPS involvement in N partitioning, N use efficiency, and domestication. Overall, this work provides important knowledge on UPS transporters in grasses and clues for breeding resilient wheat varieties with improved N use efficiency.