TOR signaling in plants: conservation and innovation

Abstract

Target of rapamycin (TOR) is an evolutionarily conserved protein kinase that plays a central role in both plants and animals, despite their distinct developmental programs and survival strategies. Indeed, TOR integrates nutrient, energy, hormone, growth factor and environmental inputs to control proliferation, growth and metabolism in diverse multicellular organisms. Here, we compare the molecular composition, upstream regulators and downstream signaling relays of TOR complexes in plants and animals. We also explore and discuss the pivotal functions of TOR signaling in basic cellular processes, such as translation, cell division and stem/progenitor cell regulation during plant development.

Keywords: Cell cycle regulation; Meristem; Metabolism reprogramming; Nutrient signaling; Stem cell niche; Target of rapamycin protein kinase.

Fig. 1.

The domain structure of TOR and TOR-containing complexes. The domain structure of TOR, highlighting the mTORC1/2 and AtTORC1 components that bind to each domain.

Fig. 2.

TOR signaling regulates conserved and specialized cellular and developmental processes. The structure of an mTORC1 dimer is shown, highlighting the core components. Conserved (middle), plant-specific (right) and animal/human-specific (left) cellular and developmental processes that are regulated by TORC1 are listed.

Fig. 3.

Upstream regulators of TORC. In mammalian cells, the assembly of a TORC1 dimer is fueled by nutrient/energy-dependent TCA-ETC activities in the mitochondria in a TTT-WAC-RUVBLs complex-dependent manner, which may be conserved in plants. mTORC1 is activated by the small GTPase RHEB at the lysosomal membrane, whereas plant small GTPase ROPs act as AtTORC1 activators downstream of auxin. In both mammals and plants, stresses commonly suppress TORC1 functions through AMPK/SnRK1. The plant stress hormone ABA couples with SnRK2 to regulate AtTORC1 in a reciprocal manner, which balances growth and stress responses. Differences in the localization of TOR-containing complexes in plant and animal cells are also evident; plant AtTORC1-ROP2 is localized to the endosome during auxin activation, whereas nuclear TOR functions have been reported in both plant and mammalian cells. CaMV, Cauliflower mosaic virus; Glc, glucose; Gln, glutamine; PP2C, Protein Phosphatase 2C; PYL, Pyrabactin Resistance 1 Like; RAG, Rag GTPase; RUVBL, RuvB Like AAA ATPase; TCA cycle, tricarboxylic acid cycle; WAC, WW domain containing adaptor with coiled-coil.

Fig. 4.

TOR kinase directly phosphorylates and modulates downstream signaling components. (A,B) Comparison of direct TORC1 substrates and their downstream key signaling components and functions in mammals (A) and plants (B). TFs, transcription factors.

Fig. 5.

TOR plays central roles in plant development. Summary of the developmental processes and events that are regulated by TOR signaling in plants. Schematics of the phenotypes of wild-type (left) and tor (right) plants are also shown for each process/event.

Fig. 6.

TOR regulates stem and progenitor cells in plants and animals. (A-C) Summary of TOR-mediated regulation of stem cells in plant meristems (A), as well as in the mouse intestine (B) and the fly central nervous system (C). TORC promotes the proliferation of stem and progenitor cells in a nutrient/hormone-dependent manner, which is conserved across kingdoms. In mouse intestinal crypts and the fly central nervous system, stem cell functions are regulated non-cell-autonomously. Such regulation depends on TORC1 activities. Ac, acetylation; dTORC1, Drosophila melanogaster TOR complex 1; cADPR, cyclic ADP ribose.