Inhibition of TOR Represses Nutrient Consumption, Which Improves Greening after Extended Periods of Etiolation

Upon illumination, etiolated seedlings experience a transition from heterotrophic to photoautotrophic growth. During this process, the tetrapyrrole biosynthesis pathway provides chlorophyll for photosynthesis. This pathway has to be tightly controlled to prevent the accumulation of photoreactive metabolites and to provide stoichiometric amounts of chlorophyll for its incorporation into photosynthetic protein complexes. Therefore, plants have evolved regulatory mechanisms to synchronize the biosynthesis of chlorophyll and chlorophyll-binding proteins. Two phytochrome-interacting factors (PIF1 and PIF3) and the DELLA proteins, which are controlled by the gibberellin pathway, are key regulators of this process. Here, we show that impairment of TARGET OF RAPAMYCIN (TOR) activity in Arabidopsis (Arabidopsis thaliana), either by mutation of the TOR complex component RAPTOR1B or by treatment with TOR inhibitors, leads to a significantly reduced accumulation of the photoreactive chlorophyll precursor protochlorophyllide in darkness but an increased greening rate of etiolated seedlings after exposure to light. Detailed profiling of metabolic, transcriptomic, and physiological parameters revealed that the TOR-repressed lines not only grow slower, they grow in a nutrient-saving mode, which allows them to resist longer periods of low nutrient availability. Our results also indicated that RAPTOR1B acts upstream of the gibberellin-DELLA pathway and its mutation complements the repressed greening phenotype of pif1 and pif3 after etiolation. Wild type or rb10 plants were grown on half MS media without sucrose under dark for 5 days. The etiolated seedling were exposed to white light for 1 hour or not. Microarray analysis was performed using Affymetrix Gene 1.0 ST Array (Thermo Fisher Scientific) with three biological replicates of WT and rb10 samples. Total RNA was isolated from pools of seedlings and labeling was performed using 1 μg RNA as previously described. Affymetrix Gene 1.0 ST Array hybridizations were performed by Atlas Biolabs.