TOR kinase, a GPS in the complex nutrient and hormonal signaling networks to guide plant growth and development

Abstract

To survive and sustain growth, sessile plants have developed sophisticated internal signalling networks that respond to various external and internal cues. Despite the central roles of nutrient and hormone signaling in plant growth and development, how hormone-driven processes coordinate with metabolic status remains largely enigmatic. Target of rapamycin (TOR) kinase is an evolutionarily conserved master regulator that integrates energy, nutrients, growth factors, hormones and stress signals to promote growth in all eukaryotes. Inspired by recent comprehensive systems, chemical, genetic and genomic studies on plant TOR, this review discusses a potential role of TOR as the global positioning system to both temporally and spatially direct plant growth and developmental programs by integrating dynamic information in the complex nutrient and hormonal signaling networks. We further evaluate and depict the possible functional and mechanistic models for how a single protein kinase TOR is able to recognize, integrate and even distinguish a plethora of positive and negative input signals to execute appropriate and distinct downstream biological processes via multiple partners and effectors.

Direct and indirect responses of the Arabidopsis transcriptome to an induced increase in trehalose 6-phosphate

“…In mammals, yeast and plants, TOR acts as a counterpart to AMPK/SNF1/SnRK1 to positively regulate ribosome biogenesis (Sabatini, 2017; Ryabova et al, 2018; Wu et al, 2019; Meng et al, 2022; Scarpin et al, 2022). There is emerging evidence for multi-layered interactions between TOR and SnRK1 in plants (Nukarinen et al,2016, Wang et al, 2018; Belda-Palazon et al, 2020).…”

“…There are also interactions between Tre6P and ABA signaling (Avonce et al, 2004; Ramon et al 2007; Debast et al, 2011; Tian et al, 2019; Belda-Palazón et al, 2020, 2022), and reduced-function mutant alleles of tps1 are hypersensitive to ABA (Gómez et al, 2010). It is known that TOR phosphorylates and inhibits all eight members of the PYR/PYL ABA receptor family (Meng et al, 2022). Strikingly, elevated Tre6P led to decreased transcript abundance for seven of the eight family members, with four responding in a manner consistent with them being repressed by Tre6P-dependent signaling, three of the four also being repressed by constitutive overexpression of TPS (Zhang et al, 2009) and all four being induced by transient overexpression of SnRKα1 indicating that Tre6P is acting via inhibition of SnRK1(Supplemental Figure S15D).…”

“…Another open question concerns the relationship between Tre6P signaling and TARGET OF RAPAMYCIN (TOR), which operates in an antagonistic manner to SnRK1 to promote metabolism and growth (Lastdräger et al, 2014; Baena-González and Hanson, 2017; Wu et al, 2019, Meng et al, 2022). The TOR and SnRK1 complexes are expressed in the vasculature (Moreau et al, 2012, Williams et al, 2014), overlapping with AtTPS1 expression (Fichtner et al, 2020), underlining the possibility of regulatory interactions between TOR, SnRK1 and Tre6P.…”

“…The metabolic profiles of Arabidopsis lst8 ( lethal with sec thirteen 8 ) mutants that lack a regulatory subunit of the TOR complex exhibit similarities to those of plants with constitutively elevated Tre6P (Moreau et al, 2012). Furthermore, TOR signaling interacts closely with other signaling pathways that control metabolism and growth including brassinosteroid (BR) and ABA signaling (Zhang et al, 2016; Wang et al, 2018a; Wu et al, 2019, Meng et al, 2022) and there is long-standing evidence for an interaction between the latter and Tre6P signaling (Avonce et al, 2004; Gomez et al, 2010; Debast et al, 2011; Tian et al, 2019; Belda-Palazón et al, 2020, 2022). Further open questions include whether there are interactions between Tre6P and other sugar-signaling pathways like the transcription factor (TF) BASIC LEUCINE ZIPPER 11 (bZIP11; Hanson et al, 2008; Ma et al, 2011) that is translationally regulated by sucrose (Weise et al, 2004; Rahmani et al, 2009) and acts downstream of SnRK1 in the transcriptional orchestration of starvation responses.…”

Identification of a pluripotency-inducing small compound, PLU, that induces callus formation via Heat Shock Protein 90-mediated activation of auxin signaling

“…In this regard, the sugar-type preference of PLU for the pluripotency induction may be noteworthy. It is known that the glucose/sucrose ratio affects growth and development and that sugar signaling is complexly intertwined with cytokinin signaling ( Wang et al., 2021 ; Meng et al., 2022 ). Exploring a mechanism underlying the sugar-type preference of PLU may lead to understanding why PLU can effectively induce pluripotency without the external application of cytokinin.…”