Target of rapamycin signaling in pea embryos is dependent on glutamine but detached from seed storage protein...

Target of rapamycin (TOR) kinase is the hub of a eukaryotic master signaling network that integrates nutritional and hormonal signals into cellular activities. Most studies on TOR in plants have focused on seedlings, where TOR is most responsive to light and sucrose. Here, we observed differences in nutrient regulation of TOR across plant tissues. Biochemical analyses highlighted the predominance of Gln-TOR signaling in mature Arabidopsis leaves and developing pea seeds, and its integration with hormone signaling and amino acid metabolism. Phosphoproteomic and transcriptomic analysis of developing pea seeds identified established and novel components of TOR signaling, which were enriched for proteins/genes regulating gene expression and autophagy. Unexpectedly, Gln-TOR signaling in pea embryos inhibited or delayed growth and protein accumulation during seed filling. A developmental profile was evident wherein high TOR activity and Gln levels during pea cotyledon cellularization reduced sharply as embryos progressed to seed filling. We observed strong interactions between TOR and abscisic acid (ABA) signaling such that TOR-inhibited embryos were hypersensitive to ABA-induced protein accumulation. We propose that legume seed storage protein biosynthesis displays atypical regulatory properties because it occurs in the face of increasing desiccation stress and is promoted by ABA signaling rather than TOR signaling.