The Plant Target of Rapamycin: A Conduc TOR of Nutrition and Metabolism in Photosynthetic Organisms
Abstract
:1. Introduction
2. The TOR Complex in Plants and Algae
3. SnRK1 and TOR in Plants: An Intricate Reciprocal Interaction
4. The Sweet Side of TOR: Sugars as Regulatory Factors and Outputs
5. Nitrogen Regulations of TORC1
6. TOR Sulfur, Phosphate and Potassium
7. Conclusions and Future Prospects
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Dutrochet, H. L’Agent Immédiat du Mouvement Vital Chez les Végétaux et Chez les Animaux; Nabu Press: Paris, France, 1826. [Google Scholar]
- Ingram, G.; Waites, R. Keeping it together: co-ordinating plant growth. Curr. Opin. Plant Biol. 2006, 9, 12–20. [Google Scholar] [CrossRef]
- Wolters, H.; Jürgens, G. Survival of the flexible: Hormonal growth control and adaptation in plant development. Nat. Rev. Genet. 2009, 10, 305–317. [Google Scholar] [CrossRef]
- Dobrenel, T.; Caldana, C.; Hanson, J.; Robaglia, C.; Vincentz, M.; Veit, B.; Meyer, C. TOR Signaling and Nutrient Sensing. Annu. Rev. Plant Biol. 2016, 67, 261–285. [Google Scholar] [CrossRef] [PubMed]
- Albert, V.; Hall, M.N. mTOR signaling in cellular and organismal energetics. Curr. Opin. Cell Biol. 2015, 33, 55–66. [Google Scholar] [CrossRef] [PubMed]
- Dibble, C.C.; Manning, B.D. Signal integration by mTORC1 coordinates nutrient input with biosynthetic output. Nat. Cell Biol. 2013, 15, 555–564. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rousseau, A.; Bertolotti, A. An evolutionarily conserved pathway controls proteasome homeostasis. Nature 2016, 536, 184–189. [Google Scholar] [CrossRef] [PubMed]
- Liu, G.Y.; Sabatini, D.M. mTOR at the nexus of nutrition, growth, ageing and disease. Nat. Rev. Mol. Cell Biol. 2020, 21, 183–203. [Google Scholar] [CrossRef]
- Efeyan, A.; Comb, W.C.; Sabatini, D.M. Nutrient-sensing mechanisms and pathways. Nature 2015, 517, 302–310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Saxton, R.A.; Sabatini, D.M. mTOR Signaling in Growth, Metabolism, and Disease. Cell 2017, 169, 361–371. [Google Scholar] [CrossRef] [PubMed]
- Pérez-Pérez, M.E.; Couso, I.; Crespo, J.L. The TOR Signaling Network in the Model Unicellular Green Alga Chlamydomonas reinhardtii. Biomolecules 2017, 7, 54. [Google Scholar] [CrossRef] [Green Version]
- Pancha, I.; Chokshi, K.; Tanaka, K.; Imamura, S. Microalgal Target of Rapamycin (TOR): A Central Regulatory Hub for Growth, Stress Response and Biomass Production. Plant Cell Physiol. 2020, 61, 675–684. [Google Scholar] [CrossRef] [PubMed]
- Shi, L.; Wu, Y.; Sheen, J. TOR signaling in plants: conservation and innovation. Development 2018, 145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rodriguez, M.; Parola, R.; Andreola, S.; Pereyra, C.; Martínez-Noël, G. TOR and SnRK1 signaling pathways in plant response to abiotic stresses: Do they always act according to the “yin-yang” model? Plant Sci. 2019, 288, 110220. [Google Scholar] [CrossRef]
- Wu, Y.; Shi, L.; Li, L.; Fu, L.; Liu, Y.; Xiong, Y.; Sheen, J. Integration of nutrient, energy, light, and hormone signalling via TOR in plants. J. Exp. Bot. 2019, 70, 2227–2238. [Google Scholar] [CrossRef] [PubMed]
- Brunkard, J.O. Exaptive Evolution of Target of Rapamycin Signaling in Multicellular Eukaryotes. Dev. Cell 2020, 54, 142–155. [Google Scholar] [CrossRef]
- Ryabova, L.A.; Robaglia, C.; Meyer, C. The Target of Rapamycin kinase in photosynthetic organisms: roles and regulations. J. Exp. Bot. 2019, 70, 2211–2338. [Google Scholar] [CrossRef]
- Templeton, G.W.; Moorhead, G.B. The phosphoinositide-3-OH-kinase-related kinases of Arabidopsis thaliana. EMBO Rep. 2005, 6, 723–728. [Google Scholar] [CrossRef] [Green Version]
- Sugimoto, K. Branching the Tel2 pathway for exact fit on phosphatidylinositol 3-kinase-related kinases. Curr. Genet. 2018, 64, 965–970. [Google Scholar] [CrossRef]
- Kim, S.G.; Hoffman, G.R.; Poulogiannis, G.; Buel, G.R.; Jang, Y.J.; Lee, K.W.; Kim, B.Y.; Erikson, R.L.; Cantley, L.C.; Choo, A.Y.; et al. Metabolic stress controls mTORC1 lysosomal localization and dimerization by regulating the TTT-RUVBL1/2 complex. Mol. Cell 2013, 49, 172–185. [Google Scholar] [CrossRef] [Green Version]
- Van Leene, J.; Han, C.; Gadeyne, A.; Eeckhout, D.; Matthijs, C.; Cannoot, B.; De Winne, N.; Persiau, G.; Van De Slijke, E.; Van de Cotte, B.; et al. Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase. Nat. Plants 2019, 5, 316–327. [Google Scholar] [CrossRef]
- Brunkard, J.O.; Xu, M.; Scarpin, M.R.; Chatterjee, S.; Shemyakina, E.A.; Goodman, H.M.; Zambryski, P. TOR dynamically regulates plant cell-cell transport. Proc. Natl. Acad. Sci. USA 2020, 117, 5049–5058. [Google Scholar] [CrossRef] [PubMed]
- Garcia, N.; Messing, J. TTT and PIKK Complex Genes Reverted to Single Copy Following Polyploidization and Retain Function Despite Massive Retrotransposition in Maize. Front. Plant Sci. 2017, 8, 1723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tatebe, H.; Shiozaki, K. Evolutionary Conservation of the Components in the TOR Signaling Pathways. Biomolecules 2017, 7, 77. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Menand, B.; Desnos, T.; Nussaume, L.; Berger, F.; Bouchez, D.; Meyer, C.; Robaglia, C. Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc. Natl. Acad. Sci. USA 2002, 99, 6422–6427. [Google Scholar] [CrossRef] [Green Version]
- Deprost, D.; Truong, H.; Robaglia, C.; Meyer, C. An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development. Biochem. Biophys. Res. Commun. 2005, 326, 844–850. [Google Scholar] [CrossRef]
- Moreau, M.; Azzopardi, M.; Clément, G.; Dobrenel, T.; Marchive, C.; Renne, C.; Martin-Magniette, M.L.; Taconnat, L.; Renou, J.P.; Robaglia, C.; et al. Mutations in the Arabidopsis homolog of LST8/GβL, a partner of the target of Rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 2012, 24, 463–481. [Google Scholar] [CrossRef] [Green Version]
- Anderson, G.; Veit, B.; Hanson, M. The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth. BMC Biol. 2005, 3, 12. [Google Scholar] [CrossRef] [Green Version]
- Salem, M.A.; Li, Y.; Wiszniewski, A.; Giavalisco, P. Regulatory-associated protein of TOR (RAPTOR) alters the hormonal and metabolic composition of Arabidopsis seeds, controlling seed morphology, viability and germination potential. Plant J. 2017, 92, 525–545. [Google Scholar] [CrossRef] [Green Version]
- Salem, M.A.; Li, Y.; Bajdzienko, K.; Fisahn, J.; Watanabe, M.; Hoefgen, R.; Schöttler, M.A.; Giavalisco, P. RAPTOR Controls Developmental Growth Transitions by Altering the Hormonal and Metabolic Balance. Plant Physiol. 2018, 177, 565–593. [Google Scholar] [CrossRef] [Green Version]
- Aylett, C.H.; Sauer, E.; Imseng, S.; Boehringer, D.; Hall, M.N.; Ban, N.; Maier, T. Architecture of human mTOR complex 1. Science 2016, 351, 48–52. [Google Scholar] [CrossRef]
- Forzani, C.; Duarte, G.T.; Van Leene, J.; Clément, G.; Huguet, S.; Paysant-Le-Roux, C.; Mercier, R.; De Jaeger, G.; Leprince, A.S.; Meyer, C. Mutations of the AtYAK1 Kinase Suppress TOR Deficiency in Arabidopsis. Cell Rep. 2019, 27, 3696–3708.e3695. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mahfouz, M.M.; Kim, S.; Delauney, A.J.; Verma, D.P. Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 2006, 18, 477–490. [Google Scholar] [CrossRef] [Green Version]
- Prouteau, M.; Desfosses, A.; Sieben, C.; Bourgoint, C.; Lydia Mozaffari, N.; Demurtas, D.; Mitra, A.K.; Guichard, P.; Manley, S.; Loewith, R. TORC1 organized in inhibited domains (TOROIDs) regulate TORC1 activity. Nature 2017, 550, 265–269. [Google Scholar] [CrossRef] [Green Version]
- Montané, M.H.; Menand, B. ATP-competitive mTOR kinase inhibitors delay plant growth by triggering early differentiation of meristematic cells but no developmental patterning change. J. Exp. Bot. 2013, 64, 4361–4374. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiong, Y.; Sheen, J. Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. J. Biol. Chem. 2012, 287, 2836–2842. [Google Scholar] [CrossRef] [Green Version]
- Deng, K.; Yu, L.; Zheng, X.; Zhang, K.; Wang, W.; Dong, P.; Zhang, J.; Ren, M. Target of Rapamycin Is a Key Player for Auxin Signaling Transduction in Arabidopsis. Front. Plant Sci. 2016, 7, 291. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dong, P.; Xiong, F.; Que, Y.; Wang, K.; Yu, L.; Li, Z.; Ren, M. Expression profiling and functional analysis reveals that TOR is a key player in regulating photosynthesis and phytohormone signaling pathways in Arabidopsis. Front. Plant Sci. 2015, 6, 677. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Crespo, J.; Díaz-Troya, S.; Florencio, F. Inhibition of target of rapamycin signaling by rapamycin in the unicellular green alga Chlamydomonas reinhardtii. Plant Physiol. 2005, 139, 1736–1749. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roustan, V.; Weckwerth, W. Quantitative Phosphoproteomic and System-Level Analysis of TOR Inhibition Unravel Distinct Organellar Acclimation in. Front. Plant Sci. 2018, 9, 1590. [Google Scholar] [CrossRef] [Green Version]
- Werth, E.G.; McConnell, E.W.; Couso Lianez, I.; Perrine, Z.; Crespo, J.L.; Umen, J.G.; Hicks, L.M. Investigating the effect of target of rapamycin kinase inhibition on the Chlamydomonas reinhardtii phosphoproteome: from known homologs to new targets. New Phytol. 2019, 221, 247–260. [Google Scholar] [CrossRef] [Green Version]
- Dobrenel, T.; Mancera-Martínez, E.; Forzani, C.; Azzopardi, M.; Davanture, M.; Moreau, M.; Schepetilnikov, M.; Chicher, J.; Langella, O.; Zivy, M.; et al. The Arabidopsis TOR Kinase Specifically Regulates the Expression of Nuclear Genes Coding for Plastidic Ribosomal Proteins and the Phosphorylation of the Cytosolic Ribosomal Protein S6. Front. Plant Sci. 2016, 7, 1611. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Enganti, R.; Cho, S.K.; Toperzer, J.D.; Urquidi-Camacho, R.A.; Cakir, O.S.; Ray, A.P.; Abraham, P.E.; Hettich, R.L.; von Arnim, A.G. Phosphorylation of Ribosomal Protein RPS6 Integrates Light Signals and Circadian Clock Signals. Front. Plant Sci. 2017, 8, 2210. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nukarinen, E.; Nägele, T.; Pedrotti, L.; Wurzinger, B.; Mair, A.; Landgraf, R.; Börnke, F.; Hanson, J.; Teige, M.; Baena-Gonzalez, E.; et al. Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation. Sci. Rep. 2016, 6, 31697. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barrada, A.; Djendli, M.; Desnos, T.; Mercier, R.; Robaglia, C.; Montané, M.H.; Menand, B. A TOR-YAK1 signaling axis controls cell cycle, meristem activity and plant growth in. Development 2019, 146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ryabova, L.A.; Robaglia, C.; Meyer, C. Target of Rapamycin kinase: central regulatory hub for plant growth and metabolism. J. Exp. Bot. 2019, 70, 2211–2216. [Google Scholar] [CrossRef]
- Bassham, D.C.; Crespo, J.L. Autophagy in plants and algae. Front. Plant Sci. 2014, 5, 679. [Google Scholar] [CrossRef] [Green Version]
- Dong, Y.; Teleman, A.A.; Jedmowski, C.; Wirtz, M.; Hell, R. The Arabidopsis THADA homologue modulates TOR activity and cold acclimation. Plant Biol. 2019, 21, 77–83. [Google Scholar] [CrossRef]
- Soto-Burgos, J.; Bassham, D.C. SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana. PLoS ONE 2017, 12, e0182591. [Google Scholar] [CrossRef] [Green Version]
- Baena-González, E.; Hanson, J. Shaping plant development through the SnRK1-TOR metabolic regulators. Curr. Opin. Plant Biol. 2017, 35, 152–157. [Google Scholar] [CrossRef]
- Ling, N.X.Y.; Kaczmarek, A.; Hoque, A.; Davie, E.; Ngoei, K.R.W.; Morrison, K.R.; Smiles, W.J.; Forte, G.M.; Wang, T.; Lie, S.; et al. mTORC1 directly inhibits AMPK to promote cell proliferation under nutrient stress. Nat. Metab. 2020, 2, 41–49. [Google Scholar] [CrossRef]
- Belda-Palazón, B.; Adamo, M.; Valerio, C.; Confraria, A.; Ferreira, L.; Margalha, L.; Rodrigues, A.; Meyer, C.; Rodriguez, P.L.; Baena-González, E. A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nat. Plant 2020. [Google Scholar] [CrossRef] [PubMed]
- Díaz-Granados, V.H.; López-López, J.M.; Flores-Sánchez, J.; Olguin-Alor, R.; Bedoya-López, A.; Dinkova, T.D.; Salazar-Díaz, K.; Vázquez-Santana, S.; Vázquez-Ramos, J.M.; Lara-Núñez, A. Glucose modulates proliferation in root apical meristems via TOR in maize during germination. Plant Physiol. Biochem. 2020, 155, 126–135. [Google Scholar] [CrossRef] [PubMed]
- Smeekens, S.; Ma, J.; Hanson, J.; Rolland, F. Sugar signals and molecular networks controlling plant growth. Curr. Opin. Plant Biol. 2010, 13, 274–279. [Google Scholar] [CrossRef]
- Figueroa, C.M.; Lunn, J.E. A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose. Plant Physiol. 2016, 172, 7–27. [Google Scholar] [CrossRef] [Green Version]
- Sakr, S.; Wang, M.; Dédaldéchamp, F.; Perez-Garcia, M.D.; Ogé, L.; Hamama, L.; Atanassova, R. The Sugar-Signaling Hub: Overview of Regulators and Interaction with the Hormonal and Metabolic Network. Int. J. Mol. Sci. 2018, 19, 2506. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roberts, D.J.; Tan-Sah, V.P.; Ding, E.Y.; Smith, J.M.; Miyamoto, S. Hexokinase-II positively regulates glucose starvation-induced autophagy through TORC1 inhibition. Mol. Cell 2014, 53, 521–533. [Google Scholar] [CrossRef] [Green Version]
- Moore, B.; Zhou, L.; Rolland, F.; Hall, Q.; Cheng, W.H.; Liu, Y.X.; Hwang, I.; Jones, T.; Sheen, J. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 2003, 300, 332–336. [Google Scholar] [CrossRef] [Green Version]
- Baena-González, E.; Lunn, J.E. SnRK1 and trehalose 6-phosphate—Two ancient pathways converge to regulate plant metabolism and growth. Curr. Opin. Plant Biol. 2020, 55, 52–59. [Google Scholar] [CrossRef]
- Xiong, Y.; McCormack, M.; Li, L.; Hall, Q.; Xiang, C.; Sheen, J. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 2013, 496, 181–186. [Google Scholar] [CrossRef] [Green Version]
- Pfeiffer, A.; Janocha, D.; Dong, Y.; Medzihradszky, A.; Schöne, S.; Daum, G.; Suzaki, T.; Forner, J.; Langenecker, T.; Rempel, E.; et al. Integration of light and metabolic signals for stem cell activation at the shoot apical meristem. Elife 2016, 5, e17023. [Google Scholar] [CrossRef]
- Ahmad, Z.; Magyar, Z.; Bögre, L.; Papdi, C. Cell cycle control by the target of rapamycin signalling pathway in plants. J. Exp. Bot. 2019, 70, 2275–2284. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caldana, C.; Martins, M.C.M.; Mubeen, U.; Urrea-Castellanos, R. The magic ‘hammer’ of TOR: the multiple faces of a single pathway in the metabolic regulation of plant growth and development. J. Exp. Bot. 2019, 70, 2217–2225. [Google Scholar] [CrossRef]
- Mohammed, B.; Bilooei, S.F.; Dóczi, R.; Grove, E.; Railo, S.; Palme, K.; Ditengou, F.A.; Bögre, L.; López-Juez, E. Converging Light, Energy and Hormonal Signaling Control Meristem Activity, Leaf Initiation, and Growth. Plant Physiol. 2018, 176, 1365–1381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, K.; Seo, P.J. Arabidopsis TOR signaling is essential for sugar-regulated callus formation. J. Integr. Plant Biol. 2017, 59, 742–746. [Google Scholar] [CrossRef] [Green Version]
- Horváth, B.M.; Magyar, Z.; Zhang, Y.; Hamburger, A.W.; Bakó, L.; Visser, R.G.; Bachem, C.W.; Bögre, L. EBP1 regulates organ size through cell growth and proliferation in plants. EMBO J. 2006, 25, 4909–4920. [Google Scholar] [CrossRef]
- Deprost, D.; Yao, L.; Sormani, R.; Moreau, M.; Leterreux, G.; Nicolaï, M.; Bedu, M.; Robaglia, C.; Meyer, C. The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep. 2007, 8, 864–870. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lokdarshi, A.; Papdi, C.; Pettkó-Szandtner, A.; Dorokhov, S.; Scheres, B.; Magyar, Z.; von Arnim, A.G.; Bögre, L.; Horváth, B.M. ErbB-3 BINDING PROTEIN 1 Regulates Translation and Counteracts RETINOBLASTOMA RELATED to Maintain the Root Meristem. Plant Physiol. 2020, 182, 919–932. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, N.; Meng, Y.; Li, X.; Zhou, Y.; Ma, L.; Fu, L.; Schwarzländer, M.; Liu, H.; Xiong, Y. Metabolite-mediated TOR signaling regulates the circadian clock in. Proc. Natl. Acad. Sci. USA 2019, 116, 25395–25397. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Riegler, S.; Servi, L.; Fuchs, A.; Godoy Herz, M.A.; Kubaczka, M.G.; Venhuizen, P.; Schweighofer, A.; Simpson, C.; Brown, J.W.S.; Christian Meyer, C.; et al. Light remote control of alternative splicing in roots through TOR kinase. BioRxiv 2018. [Google Scholar] [CrossRef]
- Ren, M.; Venglat, P.; Qiu, S.; Feng, L.; Cao, Y.; Wang, E.; Xiang, D.; Wang, J.; Alexander, D.; Chalivendra, S.; et al. Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis. Plant Cell 2012, 24, 4850–4874. [Google Scholar] [CrossRef] [Green Version]
- Caldana, C.; Li, Y.; Leisse, A.; Zhang, Y.; Bartholomaeus, L.; Fernie, A.R.; Willmitzer, L.; Giavalisco, P. Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. Plant J. 2013, 73, 897–909. [Google Scholar] [CrossRef] [PubMed]
- Imamura, S.; Kawase, Y.; Kobayashi, I.; Sone, T.; Era, A.; Miyagishima, S.Y.; Shimojima, M.; Ohta, H.; Tanaka, K. Target of rapamycin (TOR) plays a critical role in triacylglycerol accumulation in microalgae. Plant Mol. Biol. 2015, 89, 309–318. [Google Scholar] [CrossRef]
- Broach, J.R. Nutritional control of growth and development in yeast. Genetics 2012, 192, 73–105. [Google Scholar] [CrossRef] [Green Version]
- Weisman, R. Target of Rapamycin (TOR) Regulates Growth in Response to Nutritional Signals. Microbiol. Spectr. 2016, 4. [Google Scholar] [CrossRef]
- Wolfson, R.L.; Sabatini, D.M. The Dawn of the Age of Amino Acid Sensors for the mTORC1 Pathway. Cell Metab. 2017, 26, 301–309. [Google Scholar] [CrossRef] [Green Version]
- González, A.; Hall, M.N. Nutrient sensing and TOR signaling in yeast and mammals. EMBO J. 2017, 36, 397–408. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Malamy, J.E. Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 2005, 28, 67–77. [Google Scholar] [CrossRef]
- Krapp, A.; David, L.C.; Chardin, C.; Girin, T.; Marmagne, A.; Leprince, A.S.; Chaillou, S.; Ferrario-Méry, S.; Meyer, C.; Daniel-Vedele, F. Nitrate transport and signalling in Arabidopsis. J. Exp. Bot. 2014, 65, 789–798. [Google Scholar] [CrossRef]
- O’Brien, J.A.; Vega, A.; Bouguyon, E.; Krouk, G.; Gojon, A.; Coruzzi, G.; Gutiérrez, R.A. Nitrate Transport, Sensing, and Responses in Plants. Mol. Plant 2016, 9, 837–856. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vidal, E.A.; Alvarez, J.M.; Araus, V.; Riveras, E.; Brooks, M.D.; Krouk, G.; Ruffel, S.; Lejay, L.; Crawford, N.M.; Coruzzi, G.M.; et al. Nitrate in 2020: Thirty Years from Transport to Signaling Networks. Plant Cell 2020, 32, 2094–2119. [Google Scholar] [CrossRef]
- Beck, T.; Hall, M.N. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 1999, 402, 689–692. [Google Scholar] [CrossRef] [PubMed]
- Ahn, C.S.; Ahn, H.K.; Pai, H.S. Overexpression of the PP2A regulatory subunit Tap46 leads to enhanced plant growth through stimulation of the TOR signalling pathway. J. Exp. Bot. 2015, 66, 827–840. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mubeen, U.; Jüppner, J.; Alper, J.; Hincha, D.K.; Giavalisco, P. Target of Rapamycin Inhibition in Chlamydomonas reinhardtii Triggers de Novo Amino Acid Synthesis by Enhancing Nitrogen Assimilation. Plant Cell 2018, 30, 2240–2254. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roustan, V.; Bakhtiari, S.; Roustan, P.J.; Weckwerth, W. Quantitative in vivo phosphoproteomics reveals reversible signaling processes during nitrogen starvation and recovery in the biofuel model organism. Biotechnol. Biofuels 2017, 10, 280. [Google Scholar] [CrossRef] [Green Version]
- Sun, X.; Chen, H.; Wang, P.; Chen, F.; Yuan, L.; Mi, G. Low nitrogen induces root elongation via auxin-induced acid growth and auxin-regulated target of rapamycin (TOR) pathway in maize. J. Plant Physiol. 2020, 254, 153281. [Google Scholar] [CrossRef]
- Lam, H.M.; Coschigano, K.T.; Oliveira, I.C.; Melo-Oliveira, R.; Coruzzi, G.M. The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47, 569–593. [Google Scholar] [CrossRef]
- Galili, G.; Amir, R.; Fernie, A.R. The Regulation of Essential Amino Acid Synthesis and Accumulation in Plants. Annu. Rev. Plant Biol. 2016, 67, 153–178. [Google Scholar] [CrossRef]
- Dinkeloo, K.; Boyd, S.; Pilot, G. Update on amino acid transporter functions and on possible amino acid sensing mechanisms in plants. Semin. Cell Dev. Biol. 2018, 74, 105–113. [Google Scholar] [CrossRef]
- Lee, D.Y.; Fiehn, O. Metabolomic response of Chlamydomonas reinhardtii to the inhibition of target of rapamycin (TOR) by rapamycin. J. Microbiol. Biotechnol. 2013, 23, 923–931. [Google Scholar] [CrossRef] [Green Version]
- Sormani, R.; Yao, L.; Menand, B.; Ennar, N.; Lecampion, C.; Meyer, C.; Robaglia, C. Saccharomyces cerevisiae FKBP12 binds Arabidopsis thaliana TOR and its expression in plants leads to rapamycin susceptibility. BMC Plant Biol. 2007, 7, 26. [Google Scholar] [CrossRef] [Green Version]
- Díaz-Troya, S.; Pérez-Pérez, M.E.; Pérez-Martín, M.; Moes, S.; Jeno, P.; Florencio, F.J.; Crespo, J.L. Inhibition of protein synthesis by TOR inactivation revealed a conserved regulatory mechanism of the BiP chaperone in Chlamydomonas. Plant Physiol. 2011, 157, 730–741. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Y.; Bassham, D. TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS ONE 2010, 5, e11883. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gent, L.; Forde, B.G. How do plants sense their nitrogen status? J. Exp. Bot. 2017, 68, 2531–2539. [Google Scholar] [CrossRef] [Green Version]
- O’Leary, B.M.; Oh, G.G.K.; Lee, C.P.; Millar, A.H. Metabolite Regulatory Interactions Control Plant Respiratory Metabolism via Target of Rapamycin (TOR) Kinase Activation. Plant Cell 2020, 32, 666–682. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leiber, R.; John, F.; Verhertbruggen, Y.; Diet, A.; Knox, J.; Ringli, C. The TOR pathway modulates the structure of cell walls in Arabidopsis. Plant Cell 2010, 22, 1898–1908. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schaufelberger, M.; Galbier, F.; Herger, A.; de Brito Francisco, R.; Roffler, S.; Clement, G.; Diet, A.; Hörtensteiner, S.; Wicker, T.; Ringli, C. Mutations in the Arabidopsis ROL17/isopropylmalate synthase 1 locus alter amino acid content, modify the TOR network, and suppress the root hair cell development mutant lrx1. J. Exp. Bot. 2019, 70, 2313–2323. [Google Scholar] [CrossRef] [PubMed]
- Cao, P.; Kim, S.J.; Xing, A.; Schenck, C.A.; Liu, L.; Jiang, N.; Wang, J.; Last, R.L.; Brandizzi, F. Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis. Elife 2019, 8, e50747. [Google Scholar] [CrossRef]
- Mahmoud, S.; Planes, M.D.; Cabedo, M.; Trujillo, C.; Rienzo, A.; Caballero-Molada, M.; Sharma, S.C.; Montesinos, C.; Mulet, J.M.; Serrano, R. TOR complex 1 regulates the yeast plasma membrane proton pump and pH and potassium homeostasis. FEBS Lett. 2017, 591, 1993–2002. [Google Scholar] [CrossRef]
- Saliba, E.; Evangelinos, M.; Gournas, C.; Corrillon, F.; Georis, I.; André, B. The yeast H+-ATPase Pma1 promotes Rag/Gtr-dependent TORC1 activation in response to H+-coupled nutrient uptake. Elife 2018, 7, e31981. [Google Scholar] [CrossRef]
- Deng, K.; Wang, W.; Feng, L.; Yin, H.; Xiong, F.; Ren, M. Target of rapamycin regulates potassium uptake in Arabidopsis and potato. Plant Physiol. Biochem. 2020, 155, 357–366. [Google Scholar] [CrossRef]
- Couso, I.; Pérez-Pérez, M.E.; Ford, M.M.; Martínez-Force, E.; Hicks, L.M.; Umen, J.G.; Crespo, J.L. Phosphorus Availability Regulates TORC1 Signaling via LST8 in Chlamydomonas. Plant Cell 2020, 32, 69–80. [Google Scholar] [CrossRef] [Green Version]
- Couso, I.; Evans, B.S.; Li, J.; Liu, Y.; Ma, F.; Diamond, S.; Allen, D.K.; Umen, J.G. Synergism between Inositol Polyphosphates and TOR Kinase Signaling in Nutrient Sensing, Growth Control, and Lipid Metabolism in Chlamydomonas. Plant Cell 2016, 28, 2026–2042. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takahashi, H.; Kopriva, S.; Giordano, M.; Saito, K.; Hell, R. Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 2011, 62, 157–184. [Google Scholar] [CrossRef] [PubMed]
- Dong, Y.; Silbermann, M.; Speiser, A.; Forieri, I.; Linster, E.; Poschet, G.; Allboje Samami, A.; Wanatabe, M.; Sticht, C.; Teleman, A.A.; et al. Sulfur availability regulates plant growth via glucose-TOR signaling. Nat. Commun. 2017, 8, 1174. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Malinovsky, F.G.; Thomsen, M.F.; Nintemann, S.J.; Jagd, L.M.; Bourgine, B.; Burow, M.; Kliebenstein, D.J. An evolutionarily young defense metabolite influences the root growth of plants via the ancient TOR signaling pathway. Elife 2017, 6, e29353. [Google Scholar] [CrossRef]
- Giehl, R.F.; von Wirén, N. Root nutrient foraging. Plant Physiol. 2014, 166, 509–517. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ikmi, A.; Steenbergen, P.J.; Anzo, M.; McMullen, M.R.; Stokkermans, A.; Ellington, L.R.; Gibson, M.C. Feeding-dependent tentacle development in the sea anemone Nematostella vectensis. Nat. Commun. 2020, 11, 4399. [Google Scholar] [CrossRef]
- Mutvei, A.P.; Nagiec, M.J.; Hamann, J.C.; Kim, S.G.; Vincent, C.T.; Blenis, J. Rap1-GTPases control mTORC1 activity by coordinating lysosome organization with amino acid availability. Nat Commun. 2020, 11, 1416. [Google Scholar] [CrossRef]
- Jüppner, J.; Mubeen, U.; Leisse, A.; Caldana, C.; Wiszniewski, A.; Steinhauser, D.; Giavalisco, P. The target of rapamycin kinase affects biomass accumulation and cell cycle progression by altering carbon/nitrogen balance in synchronized Chlamydomonas reinhardtii cells. Plant J. 2018, 93, 355–376. [Google Scholar] [CrossRef] [Green Version]
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Ingargiola, C.; Turqueto Duarte, G.; Robaglia, C.; Leprince, A.-S.; Meyer, C. The Plant Target of Rapamycin: A Conduc TOR of Nutrition and Metabolism in Photosynthetic Organisms. Genes 2020, 11, 1285. https://doi.org/10.3390/genes11111285
Ingargiola C, Turqueto Duarte G, Robaglia C, Leprince A-S, Meyer C. The Plant Target of Rapamycin: A Conduc TOR of Nutrition and Metabolism in Photosynthetic Organisms. Genes. 2020; 11(11):1285. https://doi.org/10.3390/genes11111285
Chicago/Turabian StyleIngargiola, Camille, Gustavo Turqueto Duarte, Christophe Robaglia, Anne-Sophie Leprince, and Christian Meyer. 2020. "The Plant Target of Rapamycin: A Conduc TOR of Nutrition and Metabolism in Photosynthetic Organisms" Genes 11, no. 11: 1285. https://doi.org/10.3390/genes11111285