DGP1 family members mediate large-scale metabolic remodeling by integrating two environmental signals in rice

Low-phosphate (LP) and red-light (RL) remould cellular metabolism in rice (Oryza sativa). Herein, DEEP GREEN PANICLE1 (DGP1) family includes DGP1, DGP1B and DGP1C. LP treatment (10 µM KH2PO4) robustly upregulates DGP1 expression (>20-fold), RL treatment (50 µmol m-2 s-1) induces DGP1 (>80-fold) and DGP1B (>90-fold). The TIGR01589 domain of DGP1s targets cytosolic enzymes to mediate a process of nuclear translocation, including in glycolysis (PK1/4 and GAPC1/2/3), TCA cycle (PDC1, CS, SCSb, FH and MDH) and biosynthesis of non-aromatic amino acids (LeuC2, OCTase and P5CS). Meanwhile, it intervenes photorespiratory pathway by blocking the recruitment of enzyme component P subunit in the glycine decarboxylase complex. Intriguingly, cytosol-to-nucleus relocation of PK1-PK3 and PK3-PK4 complexes facilitates the shikimate pathway toward multiple groups of anti-microbial metabolites. Phenotypically, LP or RL treatment largely modifies cellular metabolome in wild-type plants displaying chemical disease resistance with reduced photosynthesis/photorespiration traits, whereas LP-treated dgp1 mutant or RL-treated dgp1 dgp1b mutant impairs these responses. Overall, rice DGP1s switch primary-secondary metabolism responding ambient changes of light quality and Pi status. The TIGR01589 domain is highly conserved in dicots and monocots with diverse activation-expression modes, suggesting the DGP1 family may extensively mediates environment-triggered metabolic reprogramming in higher plants. Overall design: To better delineate the regulatory role of DGP1 in cellular metabolism, we carried out transcriptome deep sequencing of rice leaves from the DGP1-OE1 overexpressor and WT ZH11 seedlings.