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Authors: Iftah Marash, Rupali Gupta, Gautam Anand, Meirav Leibman-Markus, Naomi Lindner, Alon Israeli, Dov Nir, Adi Avni and Maya Bar.
Plant, Cell & Environment (2024)
Abstract: "Plants constantly perceive and process environmental signals and balance between the energetic demands of growth and defense. Growth arrest upon pathogen attack was previously suggested to result from a redirection of the plants' metabolic resources towards the activation of plant defense. The energy sensor Target of Rapamycin (TOR) kinase is a conserved master coordinator of growth and development in all eukaryotes. Although TOR is positioned at the interface between development and defense, little is known about the mechanisms by which TOR may potentially regulate the relationship between these two modalities. The plant hormones cytokinin (CK) and gibberellin (GA) execute various aspects of plant development and defense. The ratio between CK and GA was reported to determine the outcome of developmental programmes. Here, investigating the interplay between TOR-mediated development and TOR-mediated defense in tomato, we found that TOR silencing resulted in rescue of several different aberrant developmental phenotypes, demonstrating that TOR is required for the execution of developmental cues. In parallel, TOR inhibition enhanced immunity in genotypes with a low CK/GA ratio but not in genotypes with a high CK/GA ratio. TOR-inhibition mediated disease resistance was found to depend on developmental status, and was abolished in strongly morphogenetic leaves, while being strongest in mature, differentiated leaves. CK repressed TOR activity, suggesting that CK-mediated immunity may rely on TOR downregulation. At the same time, TOR activity was promoted by GA, and TOR silencing reduced GA sensitivity, indicating that GA signalling requires normal TOR activity. Our results demonstrate that TOR likely acts in concert with CK and GA signalling, executing signalling cues in both defense and development. Thus, differential regulation of TOR or TOR-mediated processes could regulate the required outcome of development-defense prioritisation."
Authors: Jianhui Ma, Yuke Geng, Hong Liu, Mengqi Zhang, Shujuan Liu, Chenyang Hao, Jian Hou, Youfu Zhang, Daijing Zhang, Weijun Zhang, Xueyong Zhang and Tian Li.
Journal of Integrative Plant Biology (2023)
Abstract: "Drought is a major environmental stress limiting global wheat (Triticum aestivum) production. Exploring drought tolerance genes is important for improving drought adaptation in this crop. Here, we cloned and characterized TaTIP41, a novel drought tolerance gene in wheat. TaTIP41 is a putative conserved component of target of rapamycin (TOR) signaling, and the TaTIP41 homoeologs were expressed in response to drought stress and abscisic acid (ABA). The overexpression of TaTIP41 enhanced drought tolerance and the ABA response, including ABA-induced stomatal closure, while its downregulation using RNA interference (RNAi) had the opposite effect. Furthermore, TaTIP41 physically interacted with TaTAP46, another conserved component of TOR signaling. Like TaTIP41, TaTAP46 positively regulated drought tolerance. Furthermore, TaTIP41 and TaTAP46 interacted with type-2A protein phosphatase (PP2A) catalytic subunits, such as TaPP2A-2, and inhibited their enzymatic activities. Silencing TaPP2A-2 improved drought tolerance in wheat. Together, our findings provide new insights into the roles of TaTIP41 and TaTAP46 in the drought tolerance and ABA response in wheat, and their potential application in improving wheat environmental adaptability."
Authors: Michael Stitz, David Kuster, Maximilian Reinert, Mikhail Schepetilnikov, Béatrice Berthet, Jazmin Reyes-Hernández, Denis Janocha, Anthony Artins, Marc Boix, Rossana Henriques, Anne Pfeiffer, Jan Lohmann, Emmanuel Gaquerel and Alexis Maizel.
The EMBO Journal (2023)
Synopsis: Shoot-derived sugar promotes lateral root formation, but the mechanism through which it influences cell differentiation in this context is not well understood. Here, we learn that TOR kinase mediates lateral root formation by inducing the translation of lateral root-promoting transcription factor transcripts in a sugar-dependent manner. Lateral root formation is an important consumer of shoot-derived carbon. Pericycle activation requires shoot-derived carbohydrates and TOR. TOR promotes the translation of transcription factors ARF19, ARF7, and LBD16. TOR suppresses non-canonical primary root branching by inhibiting WOX11 expression.
Abstract: "Plant organogenesis requires matching the available metabolic resources to developmental programs. In Arabidopsis, the root system is determined by primary root-derived lateral roots (LRs), and adventitious roots (ARs) formed from non-root organs. Lateral root formation entails the auxin-dependent activation of transcription factors ARF7, ARF19, and LBD16. Adventitious root formation relies on LBD16 activation by auxin and WOX11. The allocation of shoot-derived sugar to the roots influences branching, but how its availability is sensed for LRs formation remains unknown. We combine metabolic profiling with cell-specific interference to show that LRs switch to glycolysis and consume carbohydrates. The target-of-rapamycin (TOR) kinase is activated in the lateral root domain. Interfering with TOR kinase blocks LR initiation while promoting AR formation. The target-of-rapamycin inhibition marginally affects the auxin-induced transcriptional response of the pericycle but attenuates the translation of ARF19, ARF7, and LBD16. TOR inhibition induces WOX11 transcription in these cells, yet no root branching occurs as TOR controls LBD16 translation. TOR is a central gatekeeper for root branching that integrates local auxin-dependent pathways with systemic metabolic signals, modulating the translation of auxin-induced genes."
Authors: Fangjie Xiong, Jianwei Tian, Zhenzhen Wei, Kexuan Deng, Yan Li and Yanjie Zhang.
Journal of Experimental Botany (2023)
Abstract: "Tomato fruit ripening is a unique process of nutritional and energy metabolism. Target of rapamycin (TOR), a conserved serine/threonine protein kinase in eukaryotes, controls cell growth and metabolism by integrating nutrient, energy, and hormone signals. However, it remains unclear whether TOR participates in the modulation of fruit ripening. Here, we showed that the manipulation of SlTOR by chemical or genetic methods greatly alters the process of tomato fruit maturation. Expression pattern analysis revealed that the transcripts of SlTOR declined as fruit ripening progressed. Moreover, suppression of SlTOR by TOR inhibitor AZD8055 or knockdown of its transcripts by inducible RNA interference accelerated fruit ripening and led to overall effects on fruit maturity, including color and metabolism changes, fruit softening, and expression of ripening-related genes. Genome-wide transcription indicated that silencing SlTOR reprogrammed transcription profiling associated with ripening, such as cell wall and phytohormone pathways, in particular, elevated the expression of ethylene biosynthetic genes (SlACS2, SlACS4, and SlACO1) and further promoted ethylene production. In contrast, the ethylene action inhibitor 1-MCP efficiently blocked fruit maturation even under SlTOR inhibition. These results suggest that accelerated fruit ripening caused by SlTOR inhibition depends on ethylene and that SlTOR might function as a regulator in ethylene metabolism."
Authors: Christian Montes, Ping Wang, Ching-Yi Liao, Trevor M. Nolan, Gaoyuan Song, Natalie M. Clark, J. Mitch Elmore, Hongqing Guo, Diane C. Bassham, Yanhai Yin and Justin W. Walley.
New Phytologist (2022)
Abstract: "Brassinosteroids (BRs) and Target of Rapamycin Complex (TORC) are two major actors coordinating plant growth and stress responses. Brassinosteroids function through a signaling pathway to extensively regulate gene expression and TORC is known to regulate translation and autophagy. Recent studies have revealed connections between these two pathways, but a system-wide view of their interplay is still missing. We quantified the level of 23 975 transcripts, 11 183 proteins, and 27 887 phosphorylation sites in wild-type Arabidopsis thaliana and in mutants with altered levels of either BRASSINOSTEROID INSENSITIVE 2 (BIN2) or REGULATORY ASSOCIATED PROTEIN OF TOR 1B (RAPTOR1B), two key players in BR and TORC signaling, respectively. We found that perturbation of BIN2 or RAPTOR1B levels affects a common set of gene-products involved in growth and stress responses. Furthermore, we used the multi-omic data to reconstruct an integrated signaling network. We screened 41 candidate genes identified from the reconstructed network and found that loss of function mutants of many of these proteins led to an altered BR response and/or modulated autophagy activity."
Authors: Borja Belda-Palazón, Mónica Costa, Tom Beeckman, Filip Rolland and Elena Baena-González.
PNAS (2022)
Abstract: "The phytohormone abscisic acid (ABA) promotes plant tolerance to major stresses such as drought, partly by modulating growth through poorly understood mechanisms. Here, we show that ABA-triggered repression of cell proliferation in the Arabidopsis thaliana root meristem relies on the swift subcellular relocalization of SNF1-RELATED KINASE 1 (SnRK1). Under favorable conditions, the SnRK1 catalytic subunit, SnRK1α1, is enriched in the nuclei of root cells, and this is accompanied by normal cell proliferation and meristem size. Depletion of two key drivers of ABA signaling, SnRK2.2 and SnRK2.3, causes constitutive cytoplasmic localization of SnRK1α1 and reduced meristem size, suggesting that, under nonstress conditions, SnRK2s promote growth by retaining SnRK1α1 in the nucleus. In response to ABA, SnRK1α1 translocates to the cytoplasm, and this is accompanied by inhibition of target of rapamycin (TOR), decreased cell proliferation, and reduced meristem size. Blocking nuclear export with leptomycin B abrogates ABA-driven SnRK1α1 relocalization to the cytoplasm and ABA-elicited inhibition of TOR. Furthermore, fusing SnRK1α1 to an SV40 nuclear localization signal leads to defective ABA-dependent TOR repression. Altogether, we demonstrate that SnRK2-dependent changes in SnRK1α1 subcellular localization are crucial for inhibiting TOR and root growth in response to ABA. Rapid relocalization of central regulators such as SnRK1 may represent a general strategy of eukaryotic organisms to respond to environmental changes."
Authors: Limei Song, Guoyun Xu, Tingting Li, Huina Zhou, Qinlu Lin, Jia Chen, Long Wang, Dousheng Wu, Xiaoxu Li, Lifeng Wang, Sirui Zhu and Feng Yu.
Molecular Plant (2022)
Abstract: "Target of rapamycin (TOR) kinase is an evolutionarily conserved major regulator of nutrient metabolism and organismal growth in eukaryotes. In plants, nutrients are remobilized and reallocated between shoots and roots under low nutrient conditions, and nitrogen and nitrogen-related nutrients (e.g., amino acids) are key upstream signals leading to TOR activation in shoots under low nutrient conditions. However, how these forms of nitrogen can be sensed to activate TOR in plants is still poorly understood. Here, we found that the plant receptor kinase FERONIA (FER) interacts with the TOR pathway to regulate nutrient (nitrogen and amino acid) signaling under low nutrient conditions, and exerts similar metabolic effects in response to nitrogen-deficiency in Arabidopsis. FER and its partner RIPK kinase interact with the TOR/RAPTOR complex to positively modulate TOR signaling activity. In this process, the receptor complex FER/RIPK can phosphorylate the TOR complex component RAPTOR1B. The RALF1 peptide, a ligand of the FER/RIPK receptor complex, increases TOR activation in the young leaf by enhancing FER-TOR interactions, leading to promotion of true leaf growth in Arabidopsis under low nutrient conditions. These data indicate plant prioritization of nutritional stress over RALF1-mediated inhibition of cell growth under low nutrient conditions. In addition, specific amino acids (e.g., Gln, Asp, and Gly) promote true leaf growth under nitrogen-deficient conditions via the FER-TOR axis. Our study reveals a mechanism by which the RALF1-FER pathway activates TOR in the plant adaptive response to low nutrients."
Authors: Michael Stitz, David Kuster, Maximilian Reinert, Mikhail Schepetilnikov, Béatrice Berthet, Denis Janocha, Anthony Artins, Marc Boix, Rossana Henriques, Anne Pfeiffer, Jan Lohmann, Emmanuel Gaquerel and Alexis Maizel.
bioRxiv (2022)
Abstract: "Plants post-embryonic organogenesis requires matching the available metabolic resources to the developmental programs. The root system is determined by the formation of lateral roots (LR), which in Arabidopsis thaliana entails the auxin-induced activation of founder cells located in the pericycle. While the allocation of sugars to roots influences root branching, how sugar availability is sensed for auxin-triggered formation of LRs remains unknown. Here, we combine metabolic profiling with cell-specific genetic interference to show that LR formation is an important sink for carbohydrate accompanied by a switch to glycolysis. We show that the target-of-rapamycin (TOR) kinase is locally activated in the pericycle and the founder cells and that both chemical and genetic inhibition of TOR kinase lead to a block of LR initiation. TOR marginally affects the auxin-induced transcriptional response of the pericycle but modulates the translation of ARF19, ARF7 and LBD16, three key targets of auxin signalling. These data place TOR as a gatekeeper for post-embryonic LR formation that integrates local auxin-dependent pathways with systemic metabolic signals, modulating the translation of auxin induced gene expression."
Authors: Astrid Wingler and Rossana Henriques.
Physiologia Plantarum (2022)
Abstract: "Plant growth and development depend on the availability of carbohydrates synthesized in photosynthesis (source activity) and utilization of these carbohydrates for growth (sink activity). External conditions, such as temperature, nutrient availability and stress, can affect source as well as sink activity. Optimal utilization of resources is under circadian clock control. This molecular timekeeper ensures that growth responses are adjusted to different photoperiod and temperature settings by modulating starch accumulation and degradation accordingly. For example, during the night, starch degradation is required to provide sugars for growth. Under favourable growth conditions, high sugar availability stimulates growth and development, resulting in an overall accelerated life cycle of annual plants. Key signalling components include trehalose-6-phosphate (Tre6P), which reflects sucrose availability and stimulates growth and branching when the conditions are favourable. Under sink limitation, Tre6P does, however, inhibit night-time starch degradation. Tre6P interacts with Sucrose-non-fermenting1-Related Kinase1 (SnRK1), a protein kinase that inhibits growth under starvation and stress conditions and delays development (including flowering and senescence). Tre6P inhibits SnRK1 activity, but SnRK1 increases the Tre6P to sucrose ratio under favourable conditions. Alongside Tre6P, Target of Rapamycin (TOR) stimulates processes such as protein synthesis and growth when sugar availability is high. In annual plants, an accelerated life cycle results in early leaf and plant senescence, thus shortening the lifespan. While the availability of carbohydrates in the form of sucrose and other sugars also plays an important role in seasonal life cycle events (phenology) of perennial plants, the sugar signalling pathways in perennials are less well understood."
Authors: Ching-Yi Liao, Yunting Pu, Trevor M. Nolan, Christian Montes, Hongqing Guo, Justin Walley, Yanhai Yin and Diane C. Bassham.
bioRxiv (2022)
Abstract: "Macroautophagy/autophagy is a conserved recycling process that maintains cellular homeostasis during environmental stress. Autophagy is negatively regulated by TARGET OF RAPAMYCIN (TOR), a nutrient-regulated protein kinase that in plants is activated by several phytohormones, leading to increased growth. However, the detailed molecular mechanisms by which TOR integrates autophagy and hormone-signaling are poorly understood. Here, we show that TOR modulates brassinosteroid (BR)-regulated plant growth and stress-response pathways. Active TOR was required for full BR-induced growth in Arabidopsis thaliana. Autophagy was constitutively up-regulated upon blocking BR biosynthesis or signaling, and down-regulated by increasing the activity of the BR pathway. BRASSINOSTEROID-INSENSITIVE 2 (BIN2) kinase, a GSK3-like kinase functioning as a negative regulator in BR signaling, directly phosphorylated Regulatory-Associated Protein of TOR 1B (RAPTOR1B), a substrate-recruiting subunit in the TOR complex, at a conserved serine residue within a typical BIN2 phosphorylation motif. Mutation of RAPTOR1B serine 916 to alanine, to block phosphorylation by BIN2, repressed autophagy and increased phosphorylation of the TOR substrate autophagy-related protein 13a (ATG13a). By contrast, this mutation had only a limited effect on growth. We present a model in which RAPTOR1B is phosphorylated and inhibited by BIN2 when BRs are absent, activating the autophagy pathway. When BRs signal and inhibit BIN2, RAPTOR1B is thus less inhibited by BIN2 phosphorylation. This leads to increased TOR activity and ATG13a phosphorylation, and decreased autophagy activity. Our studies define a new mechanism by which coordination between BR and TOR signaling pathways helps to maintain the balance between plant growth and stress responses."
Authors: Anuj Choudhary, Antul Kumar, Nirmaljit Kaur and Harmanjot Kaur.
Physiologia Plantarum (2022)
Abstract: "Sugars, the chemically bound form of energy, are formed by the absorption of photosynthetically active radiation and fixation in plants. During evolution, plants availed the sugar molecules as a resource, balancing molecule and signaling molecule. The multifaceted role of sugar molecules in response to environmental stimuli makes it the central coordinator required for growth, survival and continuity. During the course of evolution, the molecular networks have become complex to adapt or acclimate to the changing environment. Sugar molecules are sensed both intra and extra-cellularly by their specific sensors. The signal is transmitted by a signaling loop that involves various downstream signaling molecules, transcriptional factors and, most pertinent, the sensors TOR and SnRK1. In this review, the focus has been retained on the significance of the sugar sensors during signaling and induced modules to regulate plant growth, development, biotic and abiotic stress. It is interesting to visualize the sugar molecule as a signaling unit and not only a nutrient. Complete information on the downstream components of sugar signaling will open the gates for improving the qualitative and quantitative elements of crop plants."
Authors: Chao Han, Wenbo Hua, Jinge Li, Yan Qiao, Lianmei Yao, Wei Hao, Ruizhi Li, Min Fan, Geert De Jaeger, Wenqiang Yang and Ming-Yi Bai.
The Plant Cell (2022)
Abstract: "Starch is the main energy storage carbohydrate in plants and serves as an essential carbon storage molecule for plant metabolism and growth under changing environmental conditions. The TARGET of RAPAMYCIN (TOR) kinase is an evolutionarily conserved master regulator that integrates energy, nutrient, hormone, and stress signaling to regulate growth in all eukaryotes. Here, we demonstrate that TOR promotes guard cell starch degradation and induces stomatal opening in Arabidopsis thaliana. Starvation, caused by plants growing under short photoperiod or low light photon irradiance, as well as inactivation of TOR, impaired guard cell starch degradation and stomatal opening. Sugar and TOR induce the accumulation of β-AMYLASE1 (BAM1), which is responsible for starch degradation in guard cells. The plant steroid hormone brassinosteroid (BR) and transcription factor BZR1 play crucial roles in sugar-promoted expression of BAM1. Furthermore, sugar supply induced BAM1 accumulation, but TOR inactivation led to BAM1 degradation, and the effects of TOR inactivation on BAM1 degradation were abolished by the inhibition of autophagy and proteasome pathways or by phospho-mimicking mutation of BAM1 at serine-31. Such regulation of BAM1 activity by sugar–TOR signaling allows carbon availability to regulate guard cell starch metabolism and stomatal movement, ensuring optimal photosynthesis efficiency of plants."
Authors: Pingping Wang, Tongtong Wang, Jingyi Han, Ming Li, Yanxiu Zhao, Tong Su and Changle Ma.
Frontiers in Plant Science (2021)
Abstract: "Autophagy is a ubiquitous process used widely across plant cells to degrade cellular material and is an important regulator of plant growth and various environmental stress responses in plants. The initiation and dynamics of autophagy in plant cells are precisely controlled according to the developmental stage of the plant and changes in the environment, which are transduced into intracellular signaling pathways. These signaling pathways often regulate autophagy by mediating TOR (Target of Rapamycin) kinase activity, an important regulator of autophagy initiation; however, some also act via TOR-independent pathways. Under nutrient starvation, TOR activity is suppressed through glucose or ROS (reactive oxygen species) signaling, thereby promoting the initiation of autophagy. Under stresses, autophagy can be regulated by the regulatory networks connecting stresses, ROS and plant hormones, and in turn, autophagy regulates ROS levels and hormone signaling. This review focuses on the latest research progress in the mechanism of different external signals regulating autophagy."
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Authors: Kun-Lun Li, Hui Xue, Ren-Jie Tang and Sheng Luan.
PNAS (2023)
Significance: Low nutrient status in soils is often limiting to plant growth, making the use of fertilizers a necessity in crop production. However, heavy use of fertilizers is costly and pollutes environment. Understanding how plants respond and adapt to changing nutrient status is critical for breeding effort to increase nutrient use efficiency and cut fertilizers. This paper describes a mechanism that allows plants to adjust growth based on external potassium (K) status. High-K activates the target of rapamycin complex (TORC) pathway that in turn inactivates the low-K-responsive calcineurin B-like proteins (CBL)–CBL-interacting kinases (CIPK) network, whereas K-deficiency turns on the CBL–CIPK network that inhibits the TORC pathway, underlying transitions between adaptation and growth promotion in plants depending on K availability.
Abstract: "Potassium (K) is an essential macronutrient for plant growth, and its availability in the soil varies widely, requiring plants to respond and adapt to the changing K nutrient status. We show here that plant growth rate is closely correlated with K status in the medium, and this K-dependent growth is mediated by the highly conserved nutrient sensor, target of rapamycin (TOR). Further study connected the TOR complex (TORC) pathway with a low-K response signaling network consisting of calcineurin B-like proteins (CBL) and CBL-interacting kinases (CIPK). Under high K conditions, TORC is rapidly activated and shut down the CBL–CIPK low-K response pathway through regulatory-associated protein of TOR (RAPTOR)–CIPK interaction. In contrast, low-K status activates CBL–CIPK modules that in turn inhibit TORC by phosphorylating RAPTOR, leading to dissociation and thus inactivation of the TORC. The reciprocal regulation of the TORC and CBL–CIPK modules orchestrates plant response and adaptation to K nutrient status in the environment."
Authors: Iftah Marash, Rupali Gupta, Gautam Anand, Meirav Leibman-Markus, Naomi Lindner, Alon Israeli, Dov Nir, Adi Avni and Maya Bar.
bioRxiv (2023)
Abstract: "Plants constantly perceive and process environmental signals and balance between the energetic demands of growth and defense. Growth arrest upon pathogen attack was previously suggested to result from a redirection of the plants' metabolic resources towards the activation of plant defense. The energy sensor Target of Rapamycin (TOR) kinase is a conserved master coordinator of growth and development in all eukaryotes. Although TOR is positioned at the interface between development and defense, little is known about the mechanisms in which TOR may potentially regulate the relationship between these two modalities. The plant hormones cytokinin (CK) and gibberellin (GA) execute various aspects of plant development and defense. The ratio between CK and GA was reported to determine the outcome of developmental programs. Here, investigating the interplay between TOR-mediated development and TOR-mediated defense in tomato, we found that TOR silencing resulted in rescue of several different aberrant developmental phenotypes, demonstrating that TOR is required for the execution of developmental cues. In parallel, TOR inhibition enhanced immunity in genotypes with a low CK/GA ratio but not in genotypes with a high CK/GA ratio. TOR-inhibition mediated disease resistance was found to depend on developmental status, and was abolished in strongly morphogenetic leaves, while being strongest in mature, differentiated leaves. CK repressed TOR activity, suggesting that CK-mediated immunity may rely on TOR downregulation. At the same time, TOR activity was promoted by GA , and TOR silencing reduced GA sensitivity, indicating that GA signaling requires normal TOR activity. Our results demonstrate that TOR likely acts in concert with CK and GA signaling, executing signaling cues in both defense and development. Thus, differential regulation of TOR or TOR-mediated processes could regulate the required outcome of development-defense prioritization."
Authors: Shuyao Kong, Mingyuan Zhu, Maria Regina Scarpin, David Pan, Longfei Jia, Ryan E Martinez, Simon Alamos, Vijaya Lakshmi Vadde, Hernan G. Garcia, Shu-Bing Qian, Jacob O. Brunkard and Adrienne H. K. Roeder.
bioRxiv (2023)
Abstract: "Robustness is the invariant development of phenotype despite environmental changes and genetic perturbations. In the Arabidopsis flower bud, four sepals initiate at robust positions and times and grow to equal size to enclose and protect the inner floral organs. We previously characterized the mutant development related myb-like1 (drmy1), where 3-5 sepals initiate at irregular positions and variable times and grow to different sizes, compromising their protective function. The molecular mechanism underlying this loss of robustness was unclear. Here, we show that drmy1 has reduced TARGET OF RAPAMYCIN (TOR) activity, ribosomal content, and translation. Translation reduction decreases the protein level of ARABIDOPSIS RESPONSE REGULATOR7 (ARR7), a rapidly synthesized and degraded cytokinin signaling inhibitor. The resultant upregulation of cytokinin signaling disrupts the robust positioning of auxin signaling, causing variable sepal initiation. Our work shows that the homeostasis of translation, a ubiquitous cellular process, is crucial for the robust spatiotemporal patterning of organogenesis."
Authors: Rossana Henriques, Maria Juliana Calderan-Rodrigues, José Luis Crespo, Elena Baena-González and Camila Caldana.
Journal of Experimental Botany (2022)
Abstract: "Twenty years have passed since the identification of the target of rapamycin (TOR) protein kinase in Arabidopsis. Research has expanded from functional characterization of the TOR complex (TORC1) and development of specific chemical inhibitors, to mapping the diverse biological relationships upstream and downstream of TORC1. New insights have been obtained on the mechanisms linking environmental perception to TORC1-mediated growth responses under optimal and stress conditions. Furthermore, molecular connections have been established between TORC1 and several phytohormone and nutrient signalling pathways (e.g. brassinosteroids, ethylene, and nitrogen), which together reinforce this pathway as a major hub controlling growth responses from unicellular algae to flowering plants."
Authors: Ching-Yi Liao, Yunting Pu, Trevor M. Nolan, Christian Montes, Hongqing Guo, Justin W. Walley, Yanhai Yin and Diane C. Bassham.
Autophagy (2022)
Abstract: "Macroautophagy/autophagy is a conserved recycling process that maintains cellular homeostasis during environmental stress. Autophagy is negatively regulated by TOR (target of rapamycin), a nutrient-regulated protein kinase that in plants is activated by several phytohormones, leading to increased growth. However, the detailed molecular mechanisms by which TOR integrates autophagy and hormone signaling are poorly understood. Here, we show that TOR modulates brassinosteroid (BR)-regulated plant growth and stress-response pathways. Active TOR was required for full BR-mediated growth in Arabidopsis thaliana. Autophagy was constitutively up-regulated upon blocking BR biosynthesis or signaling, and down-regulated by increasing the activity of the BR pathway. BIN2 (brassinosteroid-insensitive 2) kinase, a GSK3-like kinase functioning as a negative regulator in BR signaling, directly phosphorylated RAPTOR1B (regulatory-associated protein of TOR 1B), a substrate-recruiting subunit in the TOR complex, at a conserved serine residue within a typical BIN2 phosphorylation motif. Mutation of RAPTOR1B serine 916 to alanine, to block phosphorylation by BIN2, repressed autophagy and increased phosphorylation of the TOR substrate ATG13a (autophagy-related protein 13a). By contrast, this mutation had only a limited effect on growth. We present a model in which RAPTOR1B is phosphorylated and inhibited by BIN2 when BRs are absent, activating the autophagy pathway. When BRs signal and inhibit BIN2, RAPTOR1B is thus less inhibited by BIN2 phosphorylation. This leads to increased TOR activity and ATG13a phosphorylation, and decreased autophagy activity. Our studies define a new mechanism by which coordination between BR and TOR signaling pathways helps to maintain the balance between plant growth and stress responses."
Authors: Yanyan Meng, Nan Zhang, Jiatian Li, Xuehong Shen, Jen Sheen and Yan Xiong.
Journal of Experimental Botany (2022)
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."
Authors: Gustavo Ravelo-Ortega, Jesús Salvador López-Bucio and José López-Bucio.
In book: "Mitigation of Plant Abiotic Stress by Microorganisms" (2022)
Abstract: "Microorganisms are integral components of plants for adaptation and surveillance to an ever-changing biosphere. Bacterial cell-to-cell signaling is achieved through biosynthesis, release, and perception of small molecules, which include the N-acyl-l-homoserine lactones (AHLs) and cyclodipeptides. Roots can recognize their prokaryotic partners to modulate waving and skewing and promote branching and absorptive potential. Such reciprocal signaling is achieved by two classes of amino lipids from the plant side, namely, alkamides and N-acyl ethanolamines (NAEs) that behave as structural mimics of AHLs. Abscisic acid (ABA), a canonical phytohormone orchestrating stress adaptation, has been found recently to act not only in rhizobacteria-mediated adaptation to abiotic stress, but also in the decodification of quorum-sensing signaling through cross talk with target of rapamycin (TOR) kinase. Understanding the specific mechanisms of the root adaptive and behavioral traits influenced by prokaryotes should help manage agriculture more appropriately in the long term."
Authors: Iftah Marash, Rupali Gupta, Meirav Leibman-Markus, Adi Avni and Maya Bar.
bioRxiv (2022)
Abstract: "Target of Rapamycin (TOR) kinase is a conserved energy sensor that regulates plant growth and development in response to nutritional and environmental inputs. TOR downregulation enhances plant immunity. Cytokinin (CK) also mediates both development and defense processes. Although TOR is positioned at the interface between development and defense, little is known about the mechanisms in which TOR may potentially regulate the switch between these two modalities. Here, we investigated this switch, by examining of the relationship between TOR and CK-driven cues. We show that TOR-silencing or inhibition enhanced immunity in WT or CK-deficient backgrounds, while it reduced immunity in a high-CK background. TOR-silencing resulted in "normalization" of developmental phenotypes associated with high or low CK levels, as well as of other classical developmental mutants, demonstrating that TOR is required for the execution of developmental cues. We found that CK represses TOR activity, suggesting the existence of a cross talk mechanism between the two pathways. Our results demonstrate that TOR likely acts downstream to CK signaling and hormonal signaling in general, executing signaling cues resulting from both high and low CK, in both defense and development. Thus, differential regulation of TOR or TOR-mediated processes could underlie a development-defense switch."
Authors: Trang Hieu Nguyen, Alain Goossens and Elia Lacchini.
Current Opinion in Plant Biology (2022)
Highlights: • Jasmonate boosts defense and metabolic processes to increase plant resilience. • Jasmonate is linked to light-regulated processes, HY5 activity, and photomorphogenesis. • Jasmonate connects with the central energy sensor TOR and the SnRK complex. • Like adrenaline in animals, jasmonate boosts plant performances but overexposure can be harmful.
Abstract: "Over the years, jasmonates (JAs) have become recognized as one of the main plant hormones that regulate stress responses by activating defense programs and the production of specialized metabolites. High JA levels have been associated with reduced plant growth, supposedly as a result of the reallocation of carbon sources from primary growth to the biosynthesis of defense compounds. Recent advances suggest however that tight regulatory networks integrate several sensing pathways to steer plant metabolism, and thereby drive the trade-off between growth and defense. In this review, we discuss how JA influences primary metabolism and how it is connected to light-regulated processes, nutrient sensing and energy metabolism. Finally, we speculate that JA, in a conceptual parallelism with adrenaline for humans, overall boosts cellular processes to keep up with an increased metabolic demand during harsh times.
Authors: Manvi Sharma, Mohan Sharma, Muhammed Jamsheer K, and Ashverya Laxmi.
Plant, Cell & Environment (2022)
Abstract: "The role of jasmonates (JAs) in primary root growth and development and in plant response to external stimuli is already known. However, its role in lateral root (LR) development remains to be explored. Our work identified methyl jasmonate (MeJA) as a key phytohormone in determining the branching angle of Arabidopsis LRs. MeJA inclines the LRs to a more vertical orientation, which was dependent on the canonical JAR1-COI1-MYC2,3,4 signalling. Our work also highlights the dual roles of light in governing LR angle. Light signalling enhances JA biosynthesis, leading to erect root architecture; whereas, glucose (Glc) induces wider branching angles. Combining physiological and molecular assays, we revealed that Glc antagonizes the MeJA response via TARGET OF RAPAMYCIN (TOR) signalling. Moreover, physiological assays using auxin mutants, MYC2-mediated transcriptional activation of LAZY2, LAZY4 and auxin biosynthetic gene CYP79B2,and asymmetric distribution of DR5::GFP and PIN2::GFP pinpointed the role of an intact auxin mechanism required by MeJA for vertical growth of LRs. We also demonstrated that light perception and signalling are indispensable for inducing vertical angles by MeJA. Thus, our investigation highlights antagonism between light and Glc signalling and how they interact with JA-auxin signals to optimize the branching angle of LRs."
Authors: Borja Belda-Palazón, Mónica Costa, Tom Beeckman, Filip Rolland and Elena Baena-González.
bioRxiv (2021)
Abstract: "The phytohormone abscisic acid (ABA) promotes plant tolerance to major stresses like drought, partly by modulating plant growth and development. However, the underlying mechanisms are poorly understood. Here, we show that cell proliferation in the Arabidopsis thaliana root meristem is controlled by the interplay between three kinases, SNF1-RELATED KINASE 2 (SnRK2), the main driver of ABA signaling, the SnRK1 energy sensor, and the growth-promoting TARGET OF RAPAMYCIN (TOR) kinase. Under favorable conditions, the SnRK1α1 catalytic subunit is enriched in the nuclei of root meristematic cells and this is accompanied by normal cell proliferation and meristem size. Depletion of SnRK2s in a snrk2.2 snrk2.3 double mutant causes constitutive cytoplasmic localization of SnRK1α1 and a reduction in meristem size, suggesting that, under non-stress conditions, SnRK2s enable growth by retaining SnRK1α1 in the nucleus. In response to elevated ABA levels, SnRK1α1 translocates to the cytoplasm and this is accompanied by inhibition of TOR, decreased cell proliferation and meristem size. Blocking nuclear export with leptomycin B abrogates ABA-driven SnRK1α1 relocalization to the cytoplasm and the inhibition of TOR. Fusion of SnRK1α1 to an SV40 nuclear localization signal leads to defective TOR repression in response to ABA, demonstrating that SnRK1α1 nuclear exit is a premise for this repression. Finally, the SnRK2-dependent changes in SnRK1α1 subcellular localization are specific to the proliferation zone of the meristem, underscoring the relevance of this mechanism for growth regulation."
Authors: Xiulan Xie, Ying Wang, Raju Datla and Maozhi Ren.
International Journal of Molecular Sciences (2021)
Abstract: "The programs associated with embryonic roots (ERs), primary roots (PRs), lateral roots (LRs), and adventitious roots (ARs) play crucial roles in the growth and development of roots in plants. The root functions are involved in diverse processes such as water and nutrient absorption and their utilization, the storage of photosynthetic products, and stress tolerance. Hormones and signaling pathways play regulatory roles during root development. Among these, auxin is the most important hormone regulating root development. The target of rapamycin (TOR) signaling pathway has also been shown to play a key role in root developmental programs. In this article, the milestones and influential progress of studying crosstalk between auxin and TOR during the development of ERs, PRs, LRs and ARs, as well as their functional implications in root morphogenesis, development, and architecture, are systematically summarized and discussed."
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