Photosynthetic assimilation of CO ₂ regulates TOR activity

Abstract

The target of rapamycin (TOR) kinase is a master regulator that integrates nutrient signals to promote cell growth in all eukaryotes. It is well established that amino acids and glucose are major regulators of TOR signaling in yeast and metazoan, but whether and how TOR responds to carbon availability in photosynthetic organisms is less understood. In this study, we showed that photosynthetic assimilation of CO2 by the Calvin–Benson–Bassham (CBB) cycle regulates TOR activity in the model single-celled microalga Chlamydomonas reinhardtii. Stimulation of CO2 fixation boosted TOR activity, whereas inhibition of the CBB cycle and photosynthesis down-regulated TOR. We uncovered a tight link between TOR activity and the endogenous level of a set of amino acids including Ala, Glu, Gln, Leu, and Val through the modulation of CO2 fixation and the use of amino acid synthesis inhibitors. Moreover, the finding that the Chlamydomonas starch-deficient mutant sta6 displayed disproportionate TOR activity and high levels of most amino acids, particularly Gln, further connected carbon assimilation and amino acids to TOR signaling. Thus, our results showed that CO2 fixation regulates TOR signaling, likely through the synthesis of key amino acids.

Target of Rapamycin Regulates Photosynthesis and Cell Growth in Auxenochlorella pyrenoidosa

“…Photosynthesis is a plant-specific physiological activity, providing energy and sugars for plants autotrophic growth, which is the biggest difference from animals [ 55 , 56 ]. Previous studies have shown that TOR signaling is closely related to chloroplast development and photosynthesis in plants [ 33 , 57 , 58 ]. Photosynthetic absorption of CO 2 increased TOR activity, which in turn the enhanced TOR activity further promoted photosynthesis in C. reinhardtii [ 58 ].…”

“…Previous studies have shown that TOR signaling is closely related to chloroplast development and photosynthesis in plants [ 33 , 57 , 58 ]. Photosynthetic absorption of CO 2 increased TOR activity, which in turn the enhanced TOR activity further promoted photosynthesis in C. reinhardtii [ 58 ]. Most DEGs involving chloroplast development and photosynthesis, such as thylakoid, porphyrin and chlorophyll biosynthesis, and photosynthesis, were down-regulated under ApTOR inhibition by AZD8055 ( Table 2 ), showing that ApTOR had important effects on chloroplast development and photosynthesis of A. pyrenoidosa .…”

Coordination of Chloroplast Activity with Plant Growth: Clues Point to TOR

“…Finally, chloroplasts have a very strong control over plant growth through TOR regulation, especially in light of the recent demonstration that photosynthetic carbon assimilation has a direct impact on TOR activity in Chlamydomonas reinhardtii [ 98 ].…”

Analyzing the impact of autotrophic and heterotrophic metabolism on the nutrient regulation of TOR

“…A recent study performed in Chlamydomonas demonstrates that the photosynthetic assimilation of CO 2 through the CBB cycle regulates TORC1 activity. Microalgae can transport and efficiently use as the C source for photosynthesis and, remarkably, stimulation of CO 2 fixation with boosts TORC1 activity in Chlamydomonas (Mallén‐Ponce et al ., 2022b). In close agreement, disruption of CO 2 fixation with glycolaldehyde, a specific inhibitor of phosphoribulokinase, was shown to inactivate TORC1 and also to prevent the ‐mediated upregulation of TORC1 (Mallén‐Ponce et al ., 2022b).…”