Integration of nutrient, energy, light, and hormone signalling via TOR in plants

Abstract

The multidomain target of rapamycin (TOR) is an atypical serine/threonine protein kinase resembling phosphatidylinositol lipid kinases, but retains high sequence identity and serves a remarkably conserved role as a master signalling integrator in yeasts, plants, and humans. TOR dynamically orchestrates cell metabolism, biogenesis, organ growth, and development transitions in response to nutrient, energy, hormone, and environmental cues. Here we review recent findings on the versatile and complex roles of TOR in transcriptome reprogramming, seedling, root, and shoot growth, and root hair production activated by sugar and energy signalling. We explore how co-ordination of TOR-mediated light and hormone signalling is involved in root and shoot apical meristem activation, proliferation of leaf primordia, cotyledon/leaf greening, and hypocotyl elongation. We also discuss the emerging TOR functions in response to sulfur assimilation and metabolism and consider potential molecular links and positive feedback loops between TOR, sugar, energy, and other essential macronutrients.

Keywords: Energy; glucose; hormone; light; nitrogen; nutrient; phosphorus; signalling; sucrose; sulfur; target of rapamycin.

Fig. 1.

TOR as a central integrator of nutrient, energy, light, and hormone signalling to regulate plant growth. (A) TOR integrates complex signalling pathways in a reciprocal manner. (B) Glucose–TOR target genes are involved in energy and nutrient regulation. The list of genes presented in (B ) was extracted from supplementary table S1 of Xiong et al., 2013. https://media.nature.com/original/nature-assets/nature/journal/v496/n7444/extref/nature12030-s2.xlsx. All microarray data published in Xiong et al., 2013 are available at the Gene Expression Omnibus under accession number GSE40245. TOR, target of rapamycin; LST8, lethal with Sec13 protein 8; RAPTOR, regulatory-associated protein of mTOR; Glc, glucose; Suc, sucrose; Gln, glutamine; SIR, sulfite reductase; SERAT, serine acetyltransferase; OAS, O-acetylserine; ABA, abscisic acid; PYL, pyrabactin resistance 1-like; PP2C, protein phosphatase 2C; SnRK2, SNF1-related protein kinase 2; CRY, cryptochrome photoreceptors; phy, phytochrome; COP1, constitutive photomorphogenesis 1; UGP, UDP-glucose pyrophosphorylase; PGM, phosphoglucomutase; PFK, phosphofructokinase; FBA8, fructose-bisphosphate aldolase 8; GAPC, glyceraldehyde-3-phosphate dehydrogenase C; PGK, phosphoglycerate kinase; IPGAM, 2,3-biphosphoglycerate-independent phosphoglycerate mutase 1; ENO, enolase; PK, pyruvate kinase; ACO, ACC oxidase; IDH, isocitrate dehydrogenase; DLST, dihydrolipoamide succinyltransferase; SCS, succinyl coenzyme A synthetase; SDH, succinate dehydrogenase; FUM, fumarase; mMDH, lactate/malate dehydrogenase; CYTC-2, cytochrome c-2; HCC, homologue of the copper chaperone SCO1; QCR7, cytochrome b-c1 complex subunit 7.

Fig. 2.

The TOR signalling network. TOR promotes translation and BR signalling probably through the signalling relay mediated by S6K1/2 and BIN2 substrates. By directly phosphorylating key transcription factors, E2Fa/b, TOR positively regulates the cell cycle. Phosphorylation of ABA-receptor PYLs by TOR represses ABA signalling. TOR, target of rapamycin; LST8, lethal with Sec13 protein 8; RAPTOR, regulatory-associated protein of mTOR; S6K, S6 kinase; E2F, E2 promoter-binding factor; RPS6, ribosomal protein S6; MRF, MA3-containing translation regulatory factor; eIF3h, eukaryotic initiation factor 3h; BIN, brassinosteroid-insensitive; BZR, brassinosteroid signalling positive regulator; TAP46, type 2A-phosphatase-associated protein 46 kDa; PYL, pyrabactin resistance 1-like; PP2C, protein phosphatase 2C; ABI, ABA-insensitive.