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. 2020 Jan 16;182(4):1613–1623. doi: 10.1104/pp.19.01214

Target of Rapamycin Signaling in Plant Stress Responses1,[OPEN]

Liwen Fu a,✉, Pengcheng Wang b,2, Yan Xiong a,2,3
PMCID: PMC7140942  PMID: 31949028

Recent significant advances allow a more complete understanding of the many functions for TOR signaling in plant responses to different nutrient deficiencies and abiotic stresses.

Abstract

Target of Rapamycin (TOR) is an atypical Ser/Thr protein kinase that is evolutionally conserved among yeasts, plants, and mammals. In plants, TOR signaling functions as a central hub to integrate different kinds of nutrient, energy, hormone, and environmental signals. TOR thereby orchestrates every stage of plant life, from embryogenesis, meristem activation, root, and leaf growth to flowering, senescence, and life span determination. Besides its essential role in the control of plant growth and development, recent research has also shed light on its multifaceted roles in plant environmental stress responses. Here, we review recent findings on the involvement of TOR signaling in plant adaptation to nutrient deficiency and various abiotic stresses. We also discuss the mechanisms underlying how plants cope with such unfavorable conditions via TOR–abscisic acid crosstalk and TOR-mediated autophagy, both of which play crucial roles in plant stress responses. Until now, little was known about the upstream regulators and downstream effectors of TOR in plant stress responses. We propose that the Snf1-related protein kinase–TOR axis plays a role in sensing various stress signals, and predict the key downstream effectors based on recent high-throughput proteomic analyses.

Plants are challenged throughout their life cycles by various types of environmental stresses, such as nutrient deficiencies, extreme temperatures, drought, and high salinity. To deal with such unfavorable growth conditions, plants have evolved elaborate and efficient stress perception and signal transduction systems. Furthermore, plant stress responses are always accompanied by extensive transcriptional, translational, and metabolic changes to redirect energy and nutrient resources for stress adaptation. Increasing evidence has revealed an essential role of target of rapamycin (TOR), a master regulator of energy maintenance and metabolic homeostasis in all eukaryotic organisms, in plant stress responses and stress adaptation.

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TOR was first identified in budding yeast through genetic mutant screens for resistance to rapamycin, a chemical molecule produced by the bacterium Streptomyces hygroscopicus (Heitman et al., 1991). Subsequent studies identified TOR genes in almost all eukaryotes, including animals and plants (Kunz et al., 1993; Menand et al., 2002; Sabatini et al., 1994). TOR is an atypical Ser/Thr protein kinase, resembling phosphatidylinositol lipid kinases, that is both structurally and functionally conserved among all eukaryotes (Xiong and Sheen, 2014). TOR exerts its function in complex forms. In mammals and yeasts, TOR forms at least two structurally and functionally distinct protein complexes (TORCs) with both shared (LST8) and distinct (Raptor in TORC1; Rictor and mSIN1 in TORC2) TOR-interacting partners. In plants, the precise compositions of the TOR kinase complexes have not been characterized. TOR, Raptor, and LST8 (but neither Rictor nor mSIN1) gene orthologs could be identified in all available plant genomes, indicating that only classical TORC1 exists in plants. One copy of TOR, two copies of Raptor (RaptorA and RaptorB), and two copies of LST8 (LST8-1 and LST8-2) exist in the Arabidopsis (Arabidopsis thaliana) genome, although LST8-2 might be a pseudogene due to its undetectable transcript level (Anderson et al., 2005; Deprost et al., 2005; Moreau et al., 2012). Gain-of-function and loss-of-function analyses have revealed that Arabidopsis TOR, Raptor, and LST8 are all essential for regulating multiple aspects of plant growth, development, and stress adaptation (Anderson et al., 2005; Deprost et al., 2005; Ren et al., 2011; Moreau et al., 2012; Xiong et al., 2013). It is worth noting that, based on these functional analyses, TOR appears to regulate a much broader spectrum of biological functions than Raptor or LST8. For example, the null tor mutant is embryo-lethal, while the raptora/b double mutant exhibits normal embryonic development but is arrested during seedling development, and the lst8-1 mutant only exhibits modest dwarf growth and early senescence phenotypes. Interestingly, although most eukaryotes have only one copy of the TOR gene, two TOR genes have been identified in three polyploids (Glycine max, Populus trichocarpa, and Brassica rapa) and four TOR genes have been identified in allotetraploid cotton (Gossypium hirsutum; Song et al., 2019). Sessile plants might possess unique TOR complexes with plant-specific components that serve as a functional equivalent of TORC2 or may even have plant-specialized functions for adaptation to constant environmental challenges.

In plants, TOR functions as a central hub that integrates signals, including nutrient, hormone, light, energy, and other environmental cues to orchestrate growth and development. TOR modulates a myriad of cellular activities, including cell division, cell expansion, transcription, mRNA translation, ribosome biogenesis, metabolism, nutrient assimilation and transport, and signaling via multiple partners and effectors in complex signaling networks, which have been extensively discussed in several excellent recent reviews (Shi et al., 2018; Jamsheer K et al., 2019; Ryabova et al., 2019; Wu et al., 2019). Besides its essential role in the control of plant growth and development, recent research also suggests an indispensable role for TOR in plant environmental stress responses. Plants with TOR dysfunctions behave as if they are stressed, even in the absence of a stressor. Transcriptome and metabolomics analyses in lst8-1 and the conditionally inducible tor-es, amiR-tor mutant revealed a broad regulation of plant stress- and autophagy-related genes, and diverse plant metabolic pathways modulating myo-inositol, raffinose, and galactinol, which usually accumulate under stress conditions such as high light, nutrient starvation, cold, drought, and high salt (Moreau et al., 2012; Caldana et al., 2013; Xiong et al., 2013). Downregulated TOR signaling by chemical inhibitor AZD-8055 also activates genes involved in stress hormone (e.g. ethylene, jasmonic acid, and abscisic acid [ABA]) signaling pathways (Dong et al., 2015). Intriguingly, modulating TOR expression can cause either stress-sensitive or stress-tolerant phenotypes depending on the type of stress encountered, further supporting the multifaceted roles of TOR in plant responses to abiotic stress (Deprost et al., 2007; Bakshi et al., 2017; Wang et al., 2017; Dong et al., 2019). Here, we focus on recent advances that enable a more thorough understanding of TOR’s many functions in plant responses to different nutrient deficiencies and various abiotic stresses, and discuss potential upstream regulators and downstream effectors of TOR.

TOR SIGNALING IN NUTRIENT SENSING AND DEFICIENCY

Plants obtain different kinds of nutrients from above-ground photosynthesis and below-ground soil nutrient assimilation. The ability to sense, assimilate, transport, and utilize various nutrients between sink and source organs is vital for plant survival and growth. TOR is a core component in plant nutrient sensing and communication networks.

In plants, Glc derived from photosynthesis in leaf sources provides carbon-based energy and building blocks (Sheen, 2014; Li and Sheen, 2016). Depletion of Glc completely blocks the kinase activity of TOR, and increases the expression of sets of autophagy- and protein degradation-related genes, indicating that recycling processes are activated to overcome the nutrient-deficient conditions (Xiong and Sheen, 2012; Xiong et al., 2013). Glc can quickly reactivate TOR activity via the glycolysis–mitochondria–electron transport chain energy relay, as chemical inhibitors targeting the first step of glycolysis and different steps of the electron transport chain completely prevent TOR activation by Glc. Thus, sugar-mediated TOR can sense the cellular metabolic and bioenergetic status to manipulate energy signaling in plants. Glc-activated TOR then phosphorylates and activates transcription factor E2Fa/E2Fb to promote root growth and true leaf formation by enhancing cell division activity in the root meristem and shoot apex, respectively (Xiong and Sheen, 2012; Xiong et al., 2013; Li et al., 2017). Interestingly, in the shoot apex, Glc alone is not enough to activate cell proliferation; the Rho-like small GTPase ROP2 was shown to bind to and activate TOR in a synergistic action along with Glc and auxin signaling (Xiong and Sheen, 2012; Xiong et al., 2013; Li et al., 2017). TOR also mediates crosstalk between sugar signaling and brassinosteroid signaling. Glc-activated TOR can inhibit autophagy to stabilize BZR1, which is a positive regulator in brassinosteroid signaling, to promote cell growth in hypocotyls (Zhang et al., 2016).

Sulfur is another important nutrient for plants. Sulfur assimilation begins with SO42− that is absorbed by sulfate transporters in the roots and transformed into adenosine 5′-phosphosulfate (APS), SO32−, and S2−, which are catalyzed by ATP sulfurylase, APS reductase (APR), and sulfite reductase (SIR), respectively (Jobe et al., 2019). S2− then reacts with o-acetyl-Ser to produce Cys, which serves as the donor for either protein synthesis or sulfur-containing compounds including glutathione (GSH) and various glucosinolates. Recently, the relationship between TOR and sulfur signaling has become evident. In the sir1-1 mutant, which could not produce S2−, TOR activity is abolished, and Glc content is significantly lower than that in wild-type Arabidopsis (Dong et al., 2017). Interestingly, exogenous supply of Glc or grafting the wild-type shoot onto the sir1-1 root rescues TOR activity, cell division in root apical meristem, and the growth arrest phenotype in the sir1-1 mutant (Dong et al., 2017), suggesting that sulfur availability does not affect TOR signaling independently, but acts through Glc energy signaling. Moreover, reducing GSH synthesis by inhibiting Glu-Cys ligase activity partially restores the dwarf phenotype and increases TOR activity in the sir1-1mutant, suggesting that reallocation of sulfur flux from GSH biosynthesis to protein translation can promote plant growth via the regulation of TOR (Speiser et al., 2018). In addition, Malinovsky et al. (2017) reported that a distinct plant defense-related glucosinolate, 3-hydroxypropylglucosinolate, can function like a TOR inhibitor to block Glc-TOR–promoted root meristem activation and root elongation. Thus, the direction of sulfur flux and its derived metabolites appear to serve key roles in balancing plant growth and stress responses via TOR regulation in response to environmental cues.

Organic nitrogen-containing molecules (amino acids) are key upstream signals for mammalian TOR activation. A very recent study showed that the accumulation of branched-chain amino acids could also upregulate TOR activity in Arabidopsis, causing reorganization of the actin cytoskeleton and actin-associated endomembranes (Cao et al., 2019). Although amino acid sensors for Leu, Arg, and Gln have been discovered in mammalian systems in the past decades (Saxton and Sabatini, 2017), no orthologs have been identified in plant genomes. Plants obtain organic nitrogen through nitrogen assimilation. Plants take in nitrate/ammonium from the soil and convert these compounds to Gln, and then into other amino acids via the Gln synthetase/Gln-2-oxoglutarate aminotransferase cycle (Krapp, 2015). It has been reported that Arabidopsis seedlings overexpressing TOR are hypersensitive to high nitrate inhibition of root growth (Deprost et al., 2007). Recent studies showed that TOR is inhibited in nitrogen-deprived seedlings, and that resupply of either nitrate, ammonium, or amino acids quickly reactivates TOR (Liu et al., 2018). However, nitrogen starvation is often associated with higher level of sugars. It remains to be examined whether inhibition of TOR by nitrogen starvation, like sulfur deprivation, is related to metabolic and energy generation processes, or if plants have evolved unique nitrogen-sensing systems for TOR activation.

A direct link between other essential inorganic nutrients and TOR is also being established. Couso et al. (2020) reported that in Chlamydomonas reinhardtii, phosphorus deprivation negatively affected LST8 protein stability, resulting in a downregulation of TORC1 activity. Interestingly, in addition to the direct influence of carbon, nitrogen, sulfur, and phosphorus availability on TOR kinase activity, genome-wide transcriptional profiling has revealed that Glc-TOR signaling activates transcription of genes involved in sulfur assimilation and transport including APS1, APS3, APK1, APK2, APR1, APR2, APR3, SIR, SULTR1.2, SULTR2.2, SULTR3.5, and SULTR4.2, as well as genes involved in nitrogen assimilation and transport, including NIA1, NIA2, NIR1, NRT1.1, NRT1.2, NRT1.5, NRT2.2, and NRT 3.1 (Xiong et al., 2013). Therefore, there is a reciprocal positive feedback regulation loop among Glc, sulfur, and nitrogen signaling, and TOR may function as a central hub that orchestrates nutrient acquisition, shuttling, and communication between above-ground and below-ground tissues (Fig. 1).

Figure 1.

Figure 1.

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TOR signaling networks mediate nutrient interorgan dialogues to drive plant growth. Plant obtain carbon, nitrogen, sulfur, phosphate, and other micronutrients from above-ground photosynthesis and below-ground soil nutrient assimilation. There is a reciprocal positive feedback regulation loop among Glc, sulfur, and nitrogen signaling, and TOR functions as a central hub that orchestrates nutrient acquisition, shuttling, and communication between interorgan coordination. ETC, electron transport chain; NIA, nitrate reductase; NIR, nitrite reductase; NRT, nitrate transporter; SULTR, sulfate transporter; SWEET, Suc transporter; TPS, trehalose-6-phosphate synthase.

TOR SIGNALING IN ABIOTIC STRESSES

Advancing research has shown that TOR plays multifaceted roles in the plant response to various kinds of abiotic stress, and may function as either a positive or a negative regulator depending on the type and duration of stress encountered.

Temperature is a major factor in plant metabolism and growth. Wang et al. (2017) showed that Arabidopsis TOR activity is quickly abolished by cold treatment at time points as early as 10 min, but recovers after 2 h of treatment. Furthermore, cold treatment compromises enhanced anthocyanin accumulation in the inducible tor-es mutant under normal temperature, indicating that TOR is likely to be a negative regulator in cold acclimation. Because inhibition of translation is essential for cold tolerance, inactive TOR might decrease translation in plants to prepare them for unfavorable cold conditions (Wang et al., 2017). However, another independent study suggested that TOR seems to positively regulate the plant cold response (Dong et al., 2019). Depletion of AtTHADA (which codes for AtTHADA, the plant protein ortholog of the cold response regulator HsTHADA in humans) lowers energy status, decreases TOR activity, and causes growth arrest in Arabidopsis (Dong et al., 2019). Meanwhile, the Atthada mutant and TOR-RNAi (35-7) lines are hypersensitive to cold conditions (Dong et al., 2019). The differences between these studies might be caused by different silencing efficiencies in different TOR-RNAi lines or by different growth conditions, further indicating the complexity and dynamic nature of the TOR-regulated cold response.

In addition to cold stress, TOR is involved in high temperature tolerance. Exogenous application of Glc, overexpression of TOR, and overexpression of E2Fa all result in higher heat shock gene expression and seedling survival rates after recovery from heat stress treatment. Downregulation of TOR, downregulation of E2Fa, and treatment with the TOR inhibitor AZD-8055 or Torin1 lead to decreased seedling survival (Sharma et al., 2019). HIKESHI-LIKE PROTEIN1 (AtHLP1) is an ortholog of HsHikeshi, which imports HSP70 into the nucleus to promote thermo-tolerance in humans (Kose et al., 2012; Koizumi et al., 2014; Sharma et al., 2019). Glc-TOR-activated E2Fa directly binds to the promoter of AtHLP1 to activate AtHLP1. AtHLP1 binds directly to the promoters of many heat shock genes, which in turn leads to histone acetylation and H3K4me3 accumulation to activate and maintain thermo-memory, eventually enhancing thermo-tolerance (Sharma et al., 2019). Interestingly, proHLP1::GUS exhibits strong GUS induction in the proliferation zone of the shoot apex after 24 h of heat stress recovery in the presence of Glc. These results suggest that cell proliferation in the shoot apex must be coordinated with internal and external cues to maintain growth and survival, and is mediated by Glc-TOR energy signaling.

TOR positively regulates the plant response to drought and osmotic stresses. In Arabidopsis, TOR overexpression lines have a longer primary root than control lines exposed to a high concentration of potassium chloride (Deprost et al., 2007). Ectopic expression of Arabidopsis TOR gene in rice (Oryza indica) enhances water-use efficiency, growth, and yield under water-limiting conditions (Bakshi et al., 2017). These transgenic rice lines also show seed germination insensitivity to ABA treatment (Bakshi et al., 2017, 2019). These observations suggest that constitutive TOR expression might alleviate the effect of drought or osmotic stress on plant growth.

In contrast, TOR negatively regulates the plant response to oxidative stress and DNA/RNA damage. Maf1 is a conserved repressor of RNA polymerase III, which is responsible for synthesizing small RNAs, 5S ribosomal RNA, and tRNAs. Maf1’s activity is mediated by phosphorylation/dephosphorylation, and dephosphorylation of Maf1 promotes its repressor activity. Both oxidative stress or DNA/RNA damage and TOR silencing stimulate Maf1 dephosphorylation (Ahn et al., 2019). It is very likely that these stresses inhibit TOR activity to enhance the dephosphorylation of Maf1 and activate its repressor function. In this way, plants may slow down protein synthesis and cell growth or division to overcome these environmental stresses.

CROSSTALK BETWEEN TOR SIGNALING AND ABA SIGNALING

The phytohormone ABA plays a key role in integrating a wide range of stress signals and controlling downstream stress responses. Upon stress, ABA accumulates rapidly and binds to its intracellular PYR/PYL/RCAR receptors. The ABA-receptor complex binds to and inhibits the clade A PP2C protein phosphatases. PP2C inhibition releases the activity of Snf1-related protein kinase 2s (SnRK2s), which phosphorylate downstream targets to mediate protective responses such as stomatal closure and the expression of ABA-responsive genes (Chen et al., 2020).

TOR signaling has been found to regulate ABA biosynthesis and distribution. ABA content is decreased in raptorb seedlings, lst8-1 seedlings, and seedlings treated with the TOR inhibitor AZD-8055 (Kravchenko et al., 2015). Some genes that encode critical enzymes in ABA biosynthesis, such as NECD3 and AOO3, show decreased expression in the raptorb mutant (Kravchenko et al., 2015). However, the ABA content of raptorb mutant seeds is elevated (Salem et al., 2017), suggesting that TOR may also be involved in the distribution of ABA.

TOR signaling and ABA signaling converge on two Protein Phosphatase 2A (PP2A)-associated proteins, TAP46 and TIP41 (Ahn et al., 2011; Hu et al., 2014; Punzo et al., 2018a, 2018b). TAP46 is directly phosphorylated by TOR kinase, and functions as a positive effector in TOR signaling (Ahn et al., 2011). Meanwhile, TAP46 negatively regulates the phosphatase activity of PP2A, prevents it from dephosphorylating ABI5 (thereby stabilizes ABI5), and finally enhances ABA sensitivity in plants (Hu et al., 2014). TIP41 interacts with the catalytic subunit of PP2A and negatively regulates ABA sensitivity (Punzo et al., 2018a, 2018b). TIP41 is also involved in TOR signaling. The tip41 mutants display growth retardation, similar to the phenotype caused by TOR silencing, and are hypersensitive to the TOR inhibitor AZD-8055 (Punzo et al., 2018a, 2018b). Recent large-scale genetic screens for insensitivity to the TOR inhibitor AZD-8055 identified two important mediators of ABA signaling, YAK1 and ABI4, as the key downstream regulators of TOR signaling to control root growth, meristem activation, and seed germination (Li et al., 2015; Kim et al., 2016; Barrada et al., 2019).

Upon sensing environmental stresses, plants usually transiently sacrifice growth and activate protective stress responses. Recently, a reciprocal negative crosstalk between TOR and ABA signaling has been shown to regulate such a trade-off between plant growth and stress adaptation (Fig. 2; Wang et al., 2018). In unstressed Arabidopsis, TOR phosphorylates ABA receptors at a highly conserved Ser, corresponding to Ser-119 in PYL1, to compromise ABA signaling by abolishing PYL binding activity to ABA, thereby inhibiting PP2C phosphatase. Expression of phosphor-mimicking PYL1S119D in multiple ABA receptor mutants does not complement the ABA-insensitive phenotype (Wang et al., 2018). The raptorb and lst8-1 mutants display hypersensitivity to exogenous ABA application (Salem et al., 2017; Wang et al., 2018). On the other hand, ABA also antagonizes TOR signaling. ABA-activated SnRK2s directly interact and phosphorylate RaptorB. This phosphorylation triggers the disassociation of RaptorB from the TOR complex, and thereby inhibits TOR’s kinase activity (Wang et al., 2018). Therefore, under nutrient-rich conditions, active TOR inhibits ABA signaling to direct resources to growth, whereas under stress conditions, ABA signaling is activated, and ABA-activated SnRK2 inhibits TOR activity to sacrifice growth for survival during stress. Importantly, the Ser residue corresponding to Ser-119 in PYL1 is highly conserved across all 121 PYLs from 12 different plant species, suggesting that this phosphor-regulatory feedback loop is a conserved mechanism that land plants utilize to optimize the balance of growth and stress responses. Strikingly, several PYLs (PYL5 to PYL12) in Arabidopsis can bind to and inhibit PP2Cs even in the absence of ABA (Hao et al., 2011; Fujii and Zhu, 2012), while the phosphor-mimicking mutation of the TOR phosphorylation site within PYL10 abolishes this ABA-independent interaction with PP2Cs (Wang et al., 2018). Therefore, TOR might also inhibit the activation of the ABA-independent PYLs under nonstress conditions to promote growth and development.

Figure 2.

Figure 2.

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A Tai-Chi model of the phospho-reciprocal regulation of the TOR kinase and ABA signaling to balance plant growth and stress response. Under growth-promoting conditions, active TOR phosphorylates ABA receptors PYR/PYLs to inhibit ABA signaling, and directs resources toward growth; under stress conditions, ABA-activated SnRK2s phosphorylate Raptor to decrease TOR activity, and sacrifice growth for survival during stress.

TOR NEGATIVELY REGULATES AUTOPHAGY

Autophagy is a process in which harmful or unwanted cellular components are delivered into lytic vacuoles to be recycled (Zhuang et al., 2018; Signorelli et al., 2019). Autophagy promotes plant resistance to nutrient deficiency, salt stress, drought stress, oxidative stress, and endoplasmic reticulum stress (Pu et al., 2017a). TOR is one of the key negative regulators of autophagy. Downregulation of TOR expression or kinase activity leads to constitutive activation of autophagy (Liu and Bassham, 2010). However, TOR antagonizes some, but not all, of the abiotic stress-triggered autophagy process (Liu and Bassham, 2010; Pu et al., 2017a, 2017b; Soto-Burgos and Bassham, 2017). Nutrient deficiency, salt stress, and drought stress all induce autophagy through TOR kinase, as overexpression of TOR under these condition significantly reduces the autophagy caused by these stresses (Pu et al., 2017a, 2017b; Soto-Burgos and Bassham, 2017). However, oxidative stress and ER stress trigger autophagy in a TOR-independent manner (Pu et al., 2017a, 2017b; Soto-Burgos and Bassham, 2017).

The autophagy-related1 (ATG1)/ATG13/ATG17 kinase complex plays an essential role in the onset of autophagy, and is the direct TORC1 substrate in mammals and yeast. In Arabidopsis, there are three ATG1 and two ATG13 homologs; their roles in the regulation of autophagy in response to nutrient starvation have been uncovered (Suttangkakul et al., 2011). Son et al. (2018) found that ATG13 contains a motif that could be phosphorylated by TOR kinase, and that deletion of this TOR-recognized motif in ATG13 enhances autophagy in Arabidopsis protoplasts. Recent high-throughput phosphoproteomics analysis using Arabidopsis suspension cell culture also revealed that ATG1s and ATG13s are direct TOR substrates. These studies reinforce that TOR-regulated phosphorylation of the ATG1/ATG13/ATG17 complex is essential for inhibiting autophagy in plants.

The upstream signals of TOR signaling also regulate autophagy. As a growth hormone, auxin stimulates TOR activity through a physical interaction between TOR and auxin-activated ROP2 to promote the activation of shoot apex cell proliferation (Schepetilnikov et al., 2013; Li et al., 2017). Interestingly, auxin also acts upstream of TOR in the regulation of autophagy. As mentioned above, nutrient deficiency, salt stress, and drought stress induce autophagy via TOR signaling, but the addition of auxin prevents the autophagy phenomenon induced by these stress conditions (Pu et al., 2017a). Meanwhile, auxin has no effect on oxidative or ER stress-induced autophagy, indicating that auxin specifically affects TOR-dependent autophagy (Pu et al., 2017a).

UPSTREAM REGULATORS OF PLANT TOR-STRESS SIGNALING

In contrast with the significant progress made in discovering the various molecular functions of TOR signaling in plant stress responses, the upstream regulators of TOR remain poorly understood. Plants possess a family of unique Rho-like small GTPases with 11 members that function as central hubs in signaling networks (Nagawa et al., 2010). As mentioned above, ROP2/3/6 has been shown to bind to and activate TOR stimulated by auxin signaling (Schepetilnikov et al., 2013; Li et al., 2017). Whether other ROPs are involved in stress sensing and regulation in TOR signaling remains a worthwhile question to be studied.

SnRKs are a group of kinases that play vital roles in a wide range of plant stress responses. Plants contain three SnRK families: SnRK1s, SnRK2s, and SnRK3s (Halford and Hey, 2009). Increasing evidence suggests that part of the SnRK-regulated stress response is achieved by the SnRKs-TOR module.

SnRK1 complex functions as a conserved energy sensor, which is activated under low energy conditions and is repressed under energy-rich conditions. In yeast and animal cells, nutrient starvations stimulate SNF1/AMPK, which repress TOR activity by phosphorylating Raptor proteins to suppresses cell growth and biosynthetic processes (Gwinn et al., 2008). In Arabidopsis, KIN10/11 protein kinases provide catalytic activities in the SnRK1 complex, and act antagonistically to TOR in the regulation of convergent primary sugar-responsive genes (Baena-González et al., 2007; Xiong et al., 2013; Li and Sheen, 2016), indicating that KIN10/11 functions upstream of TOR to regulate energy starvation processes. Furthermore, it was reported that KIN10 interacts with and phosphorylates Raptor in the TOR complex, providing a biochemical basis for the SnRK1-TOR regulation module (Nukarinen et al., 2016). Notably, KIN10 also functions upstream of TOR to activate autophagy (Pu et al., 2017b; Soto-Burgos and Bassham, 2017).

The SnRK2s are a group of plant-specific Ser/Thr kinases with 10 members (Kulik et al., 2011). SnRK2.2, SnRK2.3, and SnRK2.6 are key regulators in ABA signaling, where all 10 members are essential for osmotic stress responses (Zhu, 2016). As discussed above, ABA-dependent SnRK2.6 phosphorylates RaptorB and dissociates it from the TOR complex (Fig. 2). In this way, SnRK2s shut down TOR-promoted growth and enhance stress adaptation responses (Wang et al., 2018). Osmotic stresses also repress TOR activity (Wang et al., 2018), and PYR1/PYLs/RCARs could interact with SnRK2s to inhibit activation of SnRK2s upon osmotic stress condition (Zhao et al., 2018). Whether TOR phosphorylation of PYLs regulates osmotic stress-induced SnRK2 activation or vice versa is not known yet.

SnRK3 is also known as Calcineurin B-like protein-interacting protein kinase (CIPK; Manik et al., 2015). Arabidopsis has 26 CIPKs in total (Kolukisaoglu et al., 2004). The majority of stresses trigger rapid, transient Ca2+ signatures; and consequently, as a Ca2+ sensor, the Calcineurin B-like protein-CIPK module participates broadly in various kinds of stress responses, especially in ion homeostasis (Liu et al., 2000; Zhu, 2016; Sardar et al., 2017). Interestingly, the expression of SnRK3.24 (CIPK5) is downregulated after long-term TOR inhibition (Dong et al., 2015), and the cipk5 mutant exhibits decreased TOR activity (Meteignier et al., 2017), suggesting that SnRK3s might, like KIN10 and SnRK2s, phosphorylate Raptor to regulate TOR activity and signaling.

DOWNSTREAM EFFECTORS OF PLANT TOR-STRESS SIGNALING

TOR is a core merging point in the plant stress signaling network. However, until now, only a very limited number of TOR substrates or TOR-regulated proteins have been identified. Very recently, van Leene et al. (2019) performed quantitative phosphoproteomics and interactome analysis using Arabidopsis cell cultures with or without AZD8055 treatment. A total of 83 TOR-regulated phosphoproteins and 215 proteins interacting with the TOR complex (TOR, LST8-1, RaptorA, or RaptorB) were identified (van Leene et al., 2019). Some of these proteins may be direct TOR substrates. We performed a literature search to examine the biological functions of these proteins, and found that 19% of TOR-regulated phosphoproteins and 20% of TOR complex interacting proteins participate in various stress responses (Table 1). These TOR signaling-related targets include VirE2-Interacting Protein1 involved in osmotic and sulfate deprivation response, General Control Nonderepressible5 affecting histone acetylation under cold and salt stress, ATG1/13 for autophagy induction, and La-related protein1 involved in the heat stress-triggered mRNA degradation process (Pitzschke et al., 2009; Merret et al., 2013; Qi et al., 2017; Son et al., 2018; Zheng et al., 2019). These putative TOR substrates provide valuable directions for future studies of TOR-regulated stress responses.

Table 1. TOR-regulated stress-related proteins.

Protein AGI No.a Related Plant Stress Responses Methods
VIP1 At1g43700 Wound, cold, heavy metal, salt, osmotic, oxidative, and mechanical stress; sulfur deficiency (Pitzsche et al., 2009; Wu et al., 2010; Tsugama et al., 2012, 2018) Phosphoproteomics
OZF1 At2g19810 Sugar and nitrogen deficiency; oxidative, drought, salt, and osmotic stress (Contento et al., 2004; Peng et al., 2007; Huang et al., 2011; Lee et al., 2012; Ding et al., 2013) Phosphoproteomics
ATG1c At2g37840 Autophagy-related stress (Qi et al., 2017) Phosphoproteomics
BAM1 At3g23920 Drought, osmotic, salt, and heat stress (Simpson et al., 2003; Monroe et al., 2014; Prasch et al., 2015; Liu et al., 2019b) Phosphoproteomics
At3g26730 At3g26730 ABA-related stress (Bang et al., 2008) Phosphoproteomics
ATG13 At3g49590 Autophagy-related stress (Son et al., 2018) Phosphoproteomics
ATG1b At3g53930 Autophagy-related stress (Qi et al., 2017) Phosphoproteomics
GCN5 At3g54610 Cold and salt stress (Pavangadkar et al., 2010; Zheng et al., 2019) Phosphoproteomics
EIF4G At3g60240 Heat stress (Wu et al., 2013) Phosphoproteomics
ATG1a At3g61960 Autophagy-related stress (Qi et al., 2017) Phosphoproteomics
ATHD1 At4g38130 Salt, drought, and heat stress (Ueda et al., 2018) Phosphoproteomics
LARP1a At5g21160 Heat stress (Merret et al., 2013) Phosphoproteomics
SGS3 At5g23570 Heat stress (Liu et al., 2019a) Phosphoproteomics
YAK1 At5g35980 ABA-related and drought stress (Kim et al., 2016) Phosphoproteomics
PLDRP1 At5g39570 Drought and salt stress (Ufer et al., 2017) Phosphoproteomics
PAH2 At5g42870 Phosphorus depletion (Nakamura et al., 2009) Phosphoproteomics
AKS2 At1g05805 ABA-related stress (Takahashi et al., 2013) Interactome
PFD4 At1g08780 ABA-related and cold stress (Kurup et al., 2000; Perea-Resa et al., 2017) Interactome
KINβγ At1g09020 Sugar deficiency (Emanuelle et al., 2015) Interactome
FHY2 At1g09570 UV and cold stress (Rusaczonek et al., 2015) Interactome
HOP1 At1g12270 Heat stress (Fernández-Bautista et al., 2018) Interactome
HSP70B At1g16030 Heat stress (Sung et al., 2001) Interactome
CAT1 At1g20630 Drought stress (Hsieh et al., 2002; Xing et al., 2008) Interactome
CPK11 At1g35670 ABA-related stress (Zhu et al., 2007) Interactome
TUA2 At1g50010 Wounding, osmotic, and cold stress (Testerink et al., 2004) Interactome
FYPP1 At1g50370 ABA-related stress (Dai et al., 2013) Interactome
MKK4 At1g51660 Wounding and osmotic stress (Li et al., 2018) Interactome
CPN60B At1g55490 Cold stress (Goulas et al., 2006) Interactome
PP2A-1 At1g59830 ABA-related stress (Punzo et al., 2018b) Interactome
HOP2 At1g62740 Heat stress (Fernández-Bautista et al., 2018) Interactome
PP2A At1g69960 ABA-related and salt stress (Hu et al., 2017) Interactome
PP5 At2g42810 Heat stress (Park et al., 2011) Interactome
KIN10 At3g01090 Autophagy-related and ABA-related stress; low-energy, carbon, and phosphorus deficiency (Hamasaki et al., 2019) Interactome
S6K1 At3g08730 Cold, salt, and osmotic stress (Mahfouz et al., 2006) Interactome
HSP70 At3g09440 Cold and heat stress (Sharma et al., 2007) Interactome
2CPA At3g11630 Cold and oxidative stress (Goulas et al., 2006; Pulido et al., 2010; Juszczak et al., 2016) Interactome
HSC70-4 At3g12580 Heat, salt, osmotic, and oxidative stress (Montero-Barrientos et al., 2010) Interactome
KIN11 At3g29160 Sugar deficiency (Baena-González et al., 2007; Sheen, 2014) Interactome
ATJ3 At3g44110 Salt and osmotic stress (Salas-Muñoz et al., 2016) Interactome
ATG13 At3g49590 Autophagy-related stress (Son et al., 2018) Interactome
ATG1b At3g53930 Autophagy-related stress (Qi et al., 2017) Interactome
FER3 At3g56090 Oxidative stress (Ravet et al., 2009) Interactome
MPK4 At4g01370 Salt and heat stress (Andrási et al., 2019) Interactome
GRXS17 At4g04950 Cold, heat, and drought stress (Wu et al., 2017) Interactome
TUA6 At4g14960 Salt stress (Dinneny et al., 2008) Interactome
ATPDX1 At5g01410 Chilling, drought, salt, osmotic, and ozone stress (Denslow et al., 2007) Interactome
HSP70-1 At5g02500 Cold, heat, salt, osmotic, and heavy metal stress (Lee and Schöffl, 1996; Zhang et al., 2003; Leng et al., 2017) Interactome
UBP12 At5g06600 UV stress (Al Khateeb et al., 2019) Interactome
TSN1 At5g07350 Heat and salt stress (Gutierrez-Beltran et al., 2015) Interactome
GDH2 At5g07440 Salt stress (Jiang et al., 2007) Interactome
ASN3 At5g10240 Nitrogen deficiency (Bi et al., 2007) Interactome
GDH1 At5g18170 Low oxygen stress (Sarry et al., 2006) Interactome
ATJ2 At5g22060 Heat and cold stress (Li et al., 2005) Interactome
PFD5 At5g23290 Salt stress (Rodríguez-Milla and Salinas, 2009) Interactome
YAK1 At5g35980 ABA-related and drought stress (Kim et al., 2016) Interactome
PFD3 At5g49510 Salt stress (Rodríguez-Milla and Salinas, 2009) Interactome
TAP46_2A At5g53000 Cold stress (Harris et al., 1999) Interactome
ATG101 At5g66930 Autophagy-related stress (Li et al., 2014) Interactome
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a

AGI, Arabidopsis Gene-Initiative Identifier

graphic file with name PP_201901214R1_fx2.jpg

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CONCLUSION

During the last decade, our knowledge of plant TOR signaling has increased significantly. It is now clear that TOR acts as a master regulator to sense and transduce nutrient, energetic, hormonal, metabolic, and environmental stress inputs into physiological, molecular, and developmental responses for growth and stress adaptation. Despite the great wealth of information that has become available, several questions still remain to be answered, and many others are emerging (see Outstanding Questions). In addition to its well-known roles in regulation of protein translation, it will be fruitful to dissect how TOR signaling represses a vast spectrum of primary target gene pathways in stress and immune responses. As a protein kinase, the phosphorylation of Thr-449 in the TOR-substrate protein ribosomal S6 kinase1 is used as a conserved indicator of endogenous TOR activity. Developing tissue-specific and fluorescence-visualized TOR kinase activity markers will help to quantitatively measure TOR activity and specific signaling output in different organs, e.g. sink and source tissues, thereby facilitating a more accurate interpretation of the different or even opposite phenotypes when TOR signaling is perturbed under various environmental conditions.

Footnotes

1

This work was supported by the Recruitment Program of Global Experts, People’s Republic of China, the National Natural Science Foundation of China (grant no. 31870269 to Y.X. and grant no. 31771358 to P.W.), Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDB27040106 to P.W.), and the Basic Forestry and Proteomics Research Centre, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University.

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