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 coordination 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.

ATP Hydrolysis Determines Cold Tolerance by Regulating Available Energy for Glutathione Synthesis in Rice Seedling Plants

“…This suggests that the antagonism between the SnRK1 and TOR may be ambiguous and the kinases may act in a different way under certain physiological circumstances (Rodriguez et al 2019). The target genes of TOR and SnRK1 kinases only partially and not always antagonistically overlay under energy deficiency (Wu et al 2019). Additionally, the TOR was reported to be activated by ATPase (Zoncu et al 2011), which could explain the lower expression level of TOR showed in RIL82 than ZZ39 under cold stress.…”

Reciprocal regulation of photosynthesis and mitochondrial respiration by TOR kinase in Chlamydomonas reinhardtii

“…Thus, the TORC1 complex has been shown to play a crucial role in biogenesis and maturation of chloroplast to promote leaf and cotyledon greening (Li, Gao, Xue, Wang, & Zhao, ; Li, Song, et al, ; Mohammed et al, ; Sun et al, ; Zhang et al, ). Moreover, reports have also indicated that TOR kinase plays an important role in phytohormone signaling including that of auxin, gibberellic acid, brassinosteroids, and cytokinins etc (Li & Sheen, ; Quilichini et al, ; Wang et al, ; Wu et al, ; Xiong et al, ; Zhang et al, ).…”

“…In most land plants, chlorophytes and rhodophytes, no RICTOR ortholog has been found suggesting that only TORC1 is conserved (Shi, Wu, & Sheen, 2018;Tatebe & Shiozaki, 2017;Wu et al, 2019).…”

“…Moreover, mammalian TORC1 can directly sense nutrients such as amino acids via the activation of RAG GTPases that recruit TOR kinase to the lysosomal membrane, whereas Arabidopsis and green algae lack these RAG like GTPases and other amino acid sensors (van Dam, Zwartkruis, Bos, & Snel, 2011;Gonzalez & Hall, 2017; Kim, Goraksha-Hicks, Li, Neufeld, & Guan, 2008;Shi et al, 2018;Xiong & Sheen, 2014). Interestingly, other nutrients such as nitrogen (N), phosphate (Pi), and sulfur (S) that play an important role in plant growth and development also act via the TOR kinase pathway, thus indicating unique plant-associated sensing components that could directly or indirectly activate TOR kinase in many plant species including rice and Arabidopsis (Bakshi, Moin, Datla, & Kirti, 2017;Bakshi, Moin, Madhav, & Kirti, 2019;Couso et al, 2016;Dong et al, 2017;Mubeen, Jüppner, Alpers, Hincha, & Giavalisco, 2018;Shi et al, 2018;Speiser et al, 2018;Wu et al, 2019;Xiong & Sheen, 2015). These studies suggest that plants may have evolved unique components to regulate growth and metabolism and the detailed characterization of the same in plants is still under progress.…”

Cell cycle control by the target of rapamycin signalling pathway in plants

“…Both shoot and root growth are reliant on photosynthates and TOR-dependent activation of cell proliferation (Mohammed et al, 2018;Pfeiffer et al, 2016;Wu et al, 2019;Xiong et al, 2013). In the shoot, to maintain meristem activity, it was suggested that in addition to sugar, auxin biosynthesis is also required that is stimulated by blue and red light receptors and the COP1 signalosome to activate the TOR kinase Fig1A; (Chen et al, 2018;Li et al, 2017).…”