The Plant Target of Rapamycin: A Conduc TOR of Nutrition and Metabolism in Photosynthetic Organisms

Abstract

Living organisms possess many mechanisms to sense nutrients and favorable conditions, which allow them to grow and develop. Photosynthetic organisms are very diverse, from green unicellular algae to multicellular flowering plants, but most of them are sessile and thus unable to escape from the biotic and abiotic stresses they experience. The Target of Rapamycin (TOR) signaling pathway is conserved in all eukaryotes and acts as a central regulatory hub between growth and extrinsic factors, such as nutrients or stress. However, relatively little is known about the regulations and roles of this pathway in plants and algae. Although some features of the TOR pathway seem to have been highly conserved throughout evolution, others clearly differ in plants, perhaps reflecting adaptations to different lifestyles and the rewiring of this primordial signaling module to adapt to specific requirements. Indeed, TOR is involved in plant responses to a vast array of signals including nutrients, hormones, light, stresses or pathogens. In this review, we will summarize recent studies that address the regulations of TOR by nutrients in photosynthetic organisms, and the roles of TOR in controlling important metabolic pathways, highlighting similarities and differences with the other eukaryotes.

Keywords: carbon; metabolism; nitrogen; nutrition; photosynthetic organisms; plant; sugars; sulfur; target of rapamycin (TOR).

Figure 1

Regulations and outputs of the TOR signaling pathway in photosynthetic organisms: TOR is a conduc TOR of nutritional and metabolic processes. Legend: The TOR (Target of Rapamycin) protein kinase is a central regulatory hub connecting various environmental and internal signals with the plant and algal metabolic and growth processes. This kinase is the heart of the evolutionary conserved TORC1 complex in which it interacts with LST8 (Lethal with Sec Thirteen protein 8) and RAPTOR (Regulatory-Associated Protein of TOR). The association of R2TP (Pontin/RuvBL1-Reptin/RuvBL2-Spaghetti/Tah1-Pih1), TTT (Tel2-Tti1-Tti2) complex and HSP90 chaperone allow the dimerization and stabilization of the TORC1 complex depending on ATP levels. Light and photosynthesis produce sugars, which, through the ETC (Electron Transport Chain), are known to stimulate TOR activity and to inhibit SnRK1 (Snf1-Related Kinase 1), the antagonist kinase of TOR. SnRK1 is activated by low energy and nutrient conditions and phosphorylates RAPTOR, inhibiting TOR activity. Phosphorus, sulfur, nitrogen and amino acids also stimulate TOR activity. In response to these signals, TOR acts on different targets like S6K (ribosomal protein S6 kinase), YAK1 (Yet another Kinase 1) or TAP46 (PP2A regulatory subunit TAP46) to regulate mRNA translation, nutritional and metabolic processes and in fine plant growth.