1932

Abstract

All living organisms rely on nutrients to sustain cell metabolism and energy production, which in turn need to be adjusted based on available resources. The evolutionarily conserved target of rapamycin (TOR) protein kinase is a central regulatory hub that connects environmental information about the quantity and quality of nutrients to developmental and metabolic processes in order to maintain cellular homeostasis. TOR is activated by both nitrogen and carbon metabolites and promotes energy-consuming processes such as cell division, mRNA translation, and anabolism in times of abundance while repressing nutrient remobilization through autophagy. In animals and yeasts, TOR acts antagonistically to the starvation-induced AMP-activated kinase (AMPK)/sucrose nonfermenting 1 (Snf1) kinase, called Snf1-related kinase 1 (SnRK1) in plants. This review summarizes the immense knowledge on the relationship between TOR signaling and nutrients in nonphotosynthetic organisms and presents recent findings in plants that illuminate the crucial role of this pathway in conveying nutrient-derived signals and regulating many aspects of metabolism and growth.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-043014-114648
2016-04-29
2024-04-12
Loading full text...

Full text loading...

/deliver/fulltext/arplant/67/1/annurev-arplant-043014-114648.html?itemId=/content/journals/10.1146/annurev-arplant-043014-114648&mimeType=html&fmt=ahah

Literature Cited

  1. Adami A, García-Alvarez B, Arias-Palomo E, Barford D, Llorca O. 1.  2007. Structure of TOR and its complex with KOG1. Mol. Cell 27:509–16 [Google Scholar]
  2. Ahn CS, Ahn HK, Pai HS. 2.  2015. Overexpression of the PP2A regulatory subunit Tap46 leads to enhanced plant growth through stimulation of the TOR signalling pathway. J. Exp. Bot. 66:827–40 [Google Scholar]
  3. Ahn CS, Han JA, Lee HS, Lee S, Pai HS. 3.  2011. The PP2A regulatory subunit Tap46, a component of the TOR signaling pathway, modulates growth and metabolism in plants. Plant Cell 23:185–209 [Google Scholar]
  4. Albert V, Hall MN. 4.  2015. mTOR signaling in cellular and organismal energetics. Curr. Opin. Cell Biol. 33:55–66 [Google Scholar]
  5. Anderson GH, Alvarez ND, Gilman C, Jeffares DC, Trainor VC. 5.  et al. 2004. Diversification of genes encoding mei2-like RNA binding proteins in plants. Plant Mol. Biol. 54:653–70 [Google Scholar]
  6. Anderson GH, Hanson M. 6.  2005. The Arabidopsis Mei2 homologue AML1 binds AtRaptor1B, the plant homologue of a major regulator of eukaryotic cell growth. BMC Plant Biol. 5:2 [Google Scholar]
  7. Anderson GH, Veit B, Hanson M. 7.  2005. The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth. BMC Biol. 3:12 [Google Scholar]
  8. Avila-Ospina L, Moison M, Yoshimoto K, Masclaux-Daubresse C. 8.  2014. Autophagy, plant senescence, and nutrient recycling. J. Exp. Bot. 65:3799–811 [Google Scholar]
  9. Backer JM. 9.  2008. The regulation and function of class III PI3Ks: novel roles for Vps34. Biochem. J. 410:1–17 [Google Scholar]
  10. Baena-González E, Sheen J. 10.  2008. Convergent energy and stress signaling. Trends Plant Sci. 13:474–82 [Google Scholar]
  11. Baretić D, Williams RL. 11.  2014. The structural basis for mTOR function. Semin. Cell Dev. Biol. 36:91–101 [Google Scholar]
  12. Bassham DC, Crespo JL. 12.  2014. Autophagy in plants and algae. Front. Plant Sci. 5:679 [Google Scholar]
  13. Beck T, Hall MN. 13.  1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689–92 [Google Scholar]
  14. Bentzinger CF, Romanino K, Cloëtta D, Lin S, Mascarenhas JB. 14.  et al. 2008. Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab. 8:411–24 [Google Scholar]
  15. Boex-Fontvieille E, Daventure M, Jossier M, Zivy M, Hodges M, Tcherkez G. 15.  2013. Photosynthetic control of Arabidopsis leaf cytoplasmic translation initiation by protein phosphorylation. PLOS ONE 8:e70692 [Google Scholar]
  16. Bögre L, Henriques R, Magyar Z. 16.  2013. TOR tour to auxin. EMBO J. 32:1069–71 [Google Scholar]
  17. Breitkreutz A, Choi H, Sharom JR, Boucher L, Neduva V. 17.  et al. 2010. A global protein kinase and phosphatase interaction network in yeast. Science 328:1043–46 [Google Scholar]
  18. Broach JR. 18.  2012. Nutritional control of growth and development in yeast. Genetics 192:73–105 [Google Scholar]
  19. Browning KS, Bailey-Serres J. 19.  2015. Mechanism of cytoplasmic mRNA translation. Arabidopsis Book 13:e0176 [Google Scholar]
  20. Caldana C, Li Y, Leisse A, Zhang Y, Bartholomaeus L. 20.  et al. 2012. Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. Plant J. 73:897–909 [Google Scholar]
  21. Castrillo JI, Zeef LA, Hoyle DC, Zhang N, Hayes A. 21.  et al. 2007. Growth control of the eukaryote cell: a systems biology study in yeast. J. Biol. 6:4 [Google Scholar]
  22. Chantranupong L, Wolfson RL, Sabatini DM. 22.  2015. Nutrient-sensing mechanisms across evolution. Cell 161:67–83 [Google Scholar]
  23. Chapman KD, Dyer JM, Mullen RT. 23.  2012. Biogenesis and functions of lipid droplets in plants. J. Lipid Res. 53:215–26 [Google Scholar]
  24. Chapman KD, Ohlrogge JB. 24.  2012. Compartmentation of triacylglycerol accumulation in plants. J. Biol. Chem. 287:2288–94 [Google Scholar]
  25. Charon C, Bruggeman Q, Thareau V, Henry Y. 25.  2012. Gene duplication within the green lineage: the case of TEL genes. J. Exp. Bot. 63:5061–77 [Google Scholar]
  26. Cornu M, Albert V, Hall MN. 26.  2013. mTOR in aging, metabolism, and cancer. Curr. Opin. Genet. Dev. 23:53–62 [Google Scholar]
  27. Crespo JL, Díaz-Troya S, Florencio F. 27.  2005. Inhibition of target of rapamycin signaling by rapamycin in the unicellular green alga Chlamydomonas reinhardtii. Plant Physiol. 139:1736–49 [Google Scholar]
  28. Crespo JL, Powers T, Fowler B, Hall MN. 28.  2002. The TOR-controlled transcription activators GLN3, RTG1, and RTG3 are regulated in response to intracellular levels of glutamine. PNAS 99:6784–89 [Google Scholar]
  29. Crozet P, Margalha L, Confraria A, Rodrigues A, Martinho C. 29.  et al. 2014. Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases. Front. Plant Sci. 5:190 [Google Scholar]
  30. Davie E, Forte GM, Petersen J. 30.  2015. Nitrogen regulates AMPK to control TORC1 signaling. Curr. Biol. 25:445–54 [Google Scholar]
  31. Deprost D, Truong H, Robaglia C, Meyer C. 31.  2005. An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development. Biochem. Biophys. Res. Commun. 326:844–50 [Google Scholar]
  32. Deprost D, Yao L, Sormani R, Moreau M, Leterreux G. 32.  et al. 2007. The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep. 8:864–70 [Google Scholar]
  33. Díaz-Troya S, Florencio F, Crespo JL. 33.  2008. Target of rapamycin and LST8 proteins associate with membranes from the endoplasmic reticulum in the unicellular green alga Chlamydomonas reinhardtii. Eukaryot. Cell 7:212–22 [Google Scholar]
  34. Díaz-Troya S, Pérez-Pérez ME, Pérez-Martín M, Moes S, Jeno P. 34.  et al. 2011. Inhibition of protein synthesis by TOR inactivation revealed a conserved regulatory mechanism of the BiP chaperone in Chlamydomonas. Plant Physiol. 157:730–41 [Google Scholar]
  35. Dibble CC, Manning BD. 35.  2013. Signal integration by mTORC1 coordinates nutrient input with biosynthetic output. Nat. Cell Biol. 15:555–64 [Google Scholar]
  36. Dobrenel T, Marchive C, Azzopardi M, Clément G, Moreau M. 36.  et al. 2013. Sugar metabolism and the plant target of rapamycin kinase: a sweet operaTOR?. Front. Plant Sci. 4:93 [Google Scholar]
  37. Dobrenel T, Marchive C, Sormani R, Moreau M, Mozzo M. 37.  et al. 2011. Regulation of plant growth and metabolism by the TOR kinase. Biochem. Soc. Trans. 39:477–81 [Google Scholar]
  38. Dong P, Xiong F, Que Y, Wang K, Yu L. 38.  et al. 2015. Expression profiling and functional analysis reveals that TOR is a key player in regulating photosynthesis and phytohormone signaling pathways in Arabidopsis. Front. Plant Biol. 6:00677 [Google Scholar]
  39. Duan HY, Li FG, Wu XD, Ma DM, Wang M, Hou YX. 39.  2006. The cloning and sequencing of a cDNA encoding a WD repeat protein in cotton (Gossypium hirsutum L.). DNA Seq. 17:49–55 [Google Scholar]
  40. Dunlop EA, Hunt DK, Acosta-Jaquez HA, Fingar DC, Tee AR. 40.  2011. ULK1 inhibits mTORC1 signaling, promotes multisite Raptor phosphorylation and hinders substrate binding. Autophagy 7:737–47 [Google Scholar]
  41. Dunlop EA, Tee AR. 41.  2014. mTOR and autophagy: a dynamic relationship governed by nutrients and energy. Semin. Cell Dev. Biol. 36:121–29 [Google Scholar]
  42. Durán RV, Hall MN. 42.  2012. Regulation of TOR by small GTPases. EMBO Rep. 13:121–28 [Google Scholar]
  43. Durán RV, Oppliger W, Robitaille AM, Heiserich L, Skendaj R. 43.  et al. 2012. Glutaminolysis activates Rag-mTORC1 signaling. Mol. Cell 47:349–58 [Google Scholar]
  44. Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI. 44.  et al. 2010. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol. Cell 39:171–83 [Google Scholar]
  45. Efeyan A, Comb WC, Sabatini DM. 45.  2015. Nutrient-sensing mechanisms and pathways. Nature 517:302–10 [Google Scholar]
  46. Efeyan A, Zoncu R, Chang S, Gumper I, Snitkin H. 46.  et al. 2013. Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival. Nature 493:679–83 [Google Scholar]
  47. Egan D, Kim J, Shaw RJ, Guan KL. 47.  2011. The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy 7:643–44 [Google Scholar]
  48. Emanuelle S, Hossain MI, Moller IE, Pedersen HL, van de Meene AM. 48.  et al. 2015. SnRK1 from Arabidopsis thaliana is an atypical AMPK. Plant J. 82:183–92 [Google Scholar]
  49. Fan J, Yan C, Zhang X, Xu C. 49.  2013. Dual role for phospholipid:diacylglycerol acyltransferase: enhancing fatty acid synthesis and diverting fatty acids from membrane lipids to triacylglycerol in Arabidopsis leaves. Plant Cell 25:3506–18 [Google Scholar]
  50. Fonseca BD, Smith EM, Yelle N, Alain T, Bushell M, Pause A. 50.  2014. The ever-evolving role of mTOR in translation. Semin. Cell Dev. Biol. 36:102–12 [Google Scholar]
  51. François J, Parrou JL. 51.  2001. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 25:125–45 [Google Scholar]
  52. Giehl RF, von Wirén N. 52.  2014. Root nutrient foraging. Plant Physiol. 166:509–17 [Google Scholar]
  53. González A, Shimobayashi M, Eisenberg T, Merle DA, Pendl T. 53.  et al. 2015. TORC1 promotes phosphorylation of ribosomal protein S6 via the AGC kinase Ypk3 in Saccharomyces cerevisiae. PLOS ONE 10:e0120250 [Google Scholar]
  54. Guérinier T, Millan L, Crozet P, Oury C, Rey F. 54.  et al. 2013. Phosphorylation of p27KIP1 homologs KRP6 and 7 by SNF1-related protein kinase-1 links plant energy homeostasis and cell proliferation. Plant J. 75:515–25 [Google Scholar]
  55. Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C. 55.  2010. Senescence and death of plant organs: nutrient recycling and developmental regulation. C. R. Biol. 333:382–91 [Google Scholar]
  56. Gulati P, Gaspers LD, Dann SG, Joaquin M, Nobukuni T. 56.  et al. 2008. Amino acids activate mTOR complex 1 via Ca2+/CaM signaling to hVps34. Cell Metab. 7:456–65 [Google Scholar]
  57. Gwinn DM, Asara JM, Shaw RJ. 57.  2010. Raptor is phosphorylated by cdc2 during mitosis. PLOS ONE 5:e9197 [Google Scholar]
  58. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A. 58.  et al. 2008. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 30:214–26 [Google Scholar]
  59. Hannah MA, Caldana C, Steinhauser D, Balbo I, Fernie AR, Willmitzer L. 59.  2010. Combined transcript and metabolite profiling of Arabidopsis grown under widely variant growth conditions facilitates the identification of novel metabolite-mediated regulation of gene expression. Plant Physiol. 152:2120–29 [Google Scholar]
  60. Hardie DG. 60.  2011. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 25:1895–908 [Google Scholar]
  61. Harris D, Myrick T, Rundle S. 61.  1999. The Arabidopsis homolog of yeast TAP42 and mammalian α4 binds to the catalytic subunit of protein phosphatase 2A and is induced by chilling. Plant Physiol. 121:609–17 [Google Scholar]
  62. He C, Klionsky DJ. 62.  2009. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43:67–93 [Google Scholar]
  63. Heitman J, Movva NR, Hall MN. 63.  1991. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253:905–9 [Google Scholar]
  64. Henriques R, Bögre L, Horváth B, Magyar Z. 64.  2014. Balancing act: matching growth with environment by the TOR signalling pathway. J. Exp. Bot. 65:2691–701 [Google Scholar]
  65. Henriques R, Magyar Z, Monardes A, Khan S, Zalejski C. 65.  et al. 2010. Arabidopsis S6 kinase mutants display chromosome instability and altered RBR1-E2F pathway activity. EMBO J. 29:2979–93 [Google Scholar]
  66. Hindle MM, Martin SF, Noordally ZB, van Ooijen G, Barrios-Llerena ME. 66.  et al. 2014. The reduced kinome of Ostreococcus tauri: core eukaryotic signalling components in a tractable model species. BMC Genom. 15:640 [Google Scholar]
  67. Hindupur SK, González A, Hall MN. 67.  2015. The opposing actions of target of rapamycin and AMP-activated protein kinase in cell growth control. Cold Spring Harb. Perspect. Biol. 7:a019141 [Google Scholar]
  68. Hirayama T, Ishida C, Kuromori T, Obata S, Shimoda C. 68.  et al. 1997. Functional cloning of a cDNA encoding Mei2-like protein from Arabidopsis thaliana using a fission yeast pheromone receptor deficient mutant. FEBS Lett. 413:16–20 [Google Scholar]
  69. Hofius D, Mundy J, Petersen M. 69.  2009. Self-consuming innate immunity in Arabidopsis. Autophagy 5:1206–7 [Google Scholar]
  70. Hu R, Zhu Y, Shen G, Zhang H. 70.  2014. TAP46 plays a positive role in the ABSCISIC ACID INSENSITIVE5-regulated gene expression in Arabidopsis. Plant Physiol. 164:721–34 [Google Scholar]
  71. Hummel M, Cordewener JH, de Groot JC, Smeekens S, America AH, Hanson J. 71.  2012. Dynamic protein composition of Arabidopsis thaliana cytosolic ribosomes in response to sucrose feeding as revealed by label free MSE proteomics. Proteomics 12:1024–38 [Google Scholar]
  72. Hummel M, Dobrenel T, Cordewener J, Davanture M, Meyer C. 72.  et al. 2015. Proteomic LC–MS analysis of Arabidopsis cytosolic ribosomes: identification of ribosomal protein paralogs and re-annotation of the ribosomal protein genes. J. Proteom 128:436–49 [Google Scholar]
  73. Imamura S, Kawase Y, Kobayashi I, Sone T, Era A. 73.  et al. 2015. Target of rapamycin (TOR) plays a critical role in triacylglycerol accumulation in microalgae. Plant Mol. Biol. 89:309–18 [Google Scholar]
  74. Jeffares DC, Phillips MJ, Moore S, Veit B. 74.  2004. A description of the Mei2-like protein family; structure, phylogenetic distribution and biological context. Dev. Genes Evol. 214:149–58 [Google Scholar]
  75. Jewell JL, Guan KL. 75.  2013. Nutrient signaling to mTOR and cell growth. Trends Biochem. Sci. 38:233–42 [Google Scholar]
  76. Jewell JL, Kim YC, Russell RC, Yu FX, Park HW. 76.  et al. 2015. Differential regulation of mTORC1 by leucine and glutamine. Science 347:194–98 [Google Scholar]
  77. John F, Roffler S, Wicker T, Ringli C. 77.  2011. Plant TOR signaling components. Plant Signal. Behav. 6:1700–5 [Google Scholar]
  78. Jossier M, Bouly J, Meimoun P, Arjmand A, Lessard P. 78.  et al. 2009. SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J. 59:316–28 [Google Scholar]
  79. Juhász G, Hill JH, Yan Y, Sass M, Baehrecke EH. 79.  et al. 2008. The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J. Cell Biol. 181:655–66 [Google Scholar]
  80. Kim D, Sarbassov D, Ali S, Latek R, Guntur K. 80.  et al. 2003. GβL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol. Cell 11:895–904 [Google Scholar]
  81. Kim J, Guan KL. 81.  2011. Amino acid signaling in TOR activation. Annu. Rev. Biochem. 80:1001–32 [Google Scholar]
  82. Kim J, Kundu M, Viollet B, Guan KL. 82.  2011. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13:132–41 [Google Scholar]
  83. Kleessen S, Irgang S, Klie S, Giavalisco P, Nikoloski Z. 83.  2015. Integration of transcriptomics and metabolomics data specifies the metabolic response of Chlamydomonas to rapamycin treatment. Plant J. 81:822–35 [Google Scholar]
  84. Krapp A, David LC, Chardin C, Girin T, Marmagne A. 84.  et al. 2014. Nitrate transport and signalling in Arabidopsis. J. Exp. Bot. 65:789–98 [Google Scholar]
  85. Kravchenko A, Citerne S, Jéhanno I, Bersimbaev RI, Veit B. 85.  et al. 2015. Mutations in the Arabidopsis Lst8 and Raptor genes encoding partners of the TOR complex, or inhibition of TOR activity decrease abscisic acid (ABA) synthesis. Biochem. Biophys. Res. Commun. 467:992–97 [Google Scholar]
  86. Krebs M, Beyhl D, Görlich E, Al-Rasheid KA, Marten I. 86.  et al. 2010. Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. PNAS 107:3251–56 [Google Scholar]
  87. Laplante M, Sabatini DM. 87.  2012. mTOR signaling in growth control and disease. Cell 149:274–93 [Google Scholar]
  88. Lastdrager J, Hanson J, Smeekens S. 88.  2014. Sugar signals and the control of plant growth and development. J. Exp. Bot. 65:799–807 [Google Scholar]
  89. Leiber R, John F, Verhertbruggen Y, Diet A, Knox J, Ringli C. 89.  2010. The TOR pathway modulates the structure of cell walls in Arabidopsis. Plant Cell 22:1898–908 [Google Scholar]
  90. Lengeler KB, Davidson RC, D'souza C, Harashima T, Shen WC. 90.  et al. 2000. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64:746–85 [Google Scholar]
  91. Leprince AS, Magalhaes N, De Vos D, Bordenave M, Crilat E. 91.  et al. 2014. Involvement of phosphatidylinositol 3-kinase in the regulation of proline catabolism in Arabidopsis thaliana. Front. Plant Sci. 5:772 [Google Scholar]
  92. Levin DE. 92.  2011. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189:1145–75 [Google Scholar]
  93. Li R, Sun R, Hicks GR, Raikhel NV. 93.  2015. Arabidopsis ribosomal proteins control vacuole trafficking and developmental programs through the regulation of lipid metabolism. PNAS 112:E89–98 [Google Scholar]
  94. Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V. 94.  et al. 2013. Acyl-lipid metabolism. Arabidopsis Book 11:e0161 [Google Scholar]
  95. Liu Y, Bassham D. 95.  2010. TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLOS ONE 5:e11883 [Google Scholar]
  96. Ljung K, Nemhauser JL, Perata P. 96.  2015. New mechanistic links between sugar and hormone signalling networks. Curr. Opin. Plant Biol. 25:130–37 [Google Scholar]
  97. Lloyd JR, Kossmann J. 97.  2015. Transitory and storage starch metabolism: two sides of the same coin?. Curr. Opin. Biotechnol. 32:143–48 [Google Scholar]
  98. Loewith R, Hall MN. 98.  2011. Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189:1177–201 [Google Scholar]
  99. Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M. 99.  2014. Trehalose metabolism in plants. Plant J. 79:544–67 [Google Scholar]
  100. Ma XM, Blenis J. 100.  2009. Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10:307–18 [Google Scholar]
  101. Maegawa K, Takii R, Ushimaru T, Kozaki A. 101.  2015. Evolutionary conservation of TORC1 components, TOR, Raptor, and LST8, between rice and yeast. Mol. Genet. Genom. 290:2019–30 [Google Scholar]
  102. Mahfouz M, Kim S, Delauney A, Verma D. 102.  2006. Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18:477–90 [Google Scholar]
  103. Mair A, Pedrotti L, Wurzinger B, Anrather D, Simeunovic A. 103.  et al. 2015. SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants. eLife 4:e05828 [Google Scholar]
  104. Marchive C, Roudier F, Castaings L, Bréhaut V, Blondet E. 104.  et al. 2013. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat. Commun. 4:1713 [Google Scholar]
  105. Masclaux-Daubresse C, Clément G, Anne P, Routaboul JM, Guiboileau A. 105.  et al. 2014. Stitching together the multiple dimensions of autophagy using metabolomics and transcriptomics reveals impacts on metabolism, development, and plant responses to the environment in Arabidopsis. Plant Cell 26:1857–77 [Google Scholar]
  106. Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA. 106.  2014. Sugar demand, not auxin, is the initial regulator of apical dominance. PNAS 111:6092–97 [Google Scholar]
  107. Medici A, Krouk G. 107.  2014. The primary nitrate response: a multifaceted signalling pathway. J. Exp. Bot. 65:5567–76 [Google Scholar]
  108. Menand B, Desnos T, Nussaume L, Berger F, Bouchez D. 108.  et al. 2002. Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. PNAS 99:6422–27 [Google Scholar]
  109. Menand B, Meyer C, Robaglia C. 109.  2004. Plant growth and the TOR pathway. Curr. Top. Microbiol. Immunol. 279:97–113 [Google Scholar]
  110. Minina EA, Bozhkov PV, Hofius D. 110.  2014. Autophagy as initiator or executioner of cell death. Trends Plant Sci. 19:692–97 [Google Scholar]
  111. Montané MH, Menand B. 111.  2013. ATP-competitive mTOR kinase inhibitors delay plant growth by triggering early differentiation of meristematic cells but no developmental patterning change. J. Exp. Bot. 64:4361–74 [Google Scholar]
  112. Moreau M, Azzopardi M, Clément G, Dobrenel T, Marchive C. 112.  et al. 2012. 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 24:463–81 [Google Scholar]
  113. Munnik T, Nielsen E. 113.  2011. Green light for polyphosphoinositide signals in plants. Curr. Opin. Plant Biol. 14:489–97 [Google Scholar]
  114. Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ. 114.  et al. 2013. Inhibition of SnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol. Biochem. 63:89–98 [Google Scholar]
  115. Nunes-Nesi A, Fernie AR, Stitt M. 115.  2010. Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol. Plant 3:973–96 [Google Scholar]
  116. Osuna D, Usadel B, Morcuende R, Gibon Y, Bläsing OE. 116.  et al. 2007. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J. 49:463–91 [Google Scholar]
  117. Otsubo Y, Yamashita A, Ohno H, Yamamoto M. 117.  2014. S. pombe TORC1 activates the ubiquitin-proteasomal degradation of the meiotic regulator Mei2 in cooperation with Pat1 kinase. J. Cell Sci. 127:2639–46 [Google Scholar]
  118. Ouibrahim L, Rubio AG, Moretti A, Montané MH, Menand B. 118.  et al. 2015. Potyviruses differ in their requirement for TOR signalling. J. Gen. Virol. 96:2898–903 [Google Scholar]
  119. Panchaud N, Péli-Gulli MP, De Virgilio C. 119.  2013. SEACing the GAP that nEGOCiates TORC1 activation: evolutionary conservation of Rag GTPase regulation. Cell Cycle 12:2948–52 [Google Scholar]
  120. Paquet N, Bernadet M, Morin H, Traas J, Dron M, Charon C. 120.  2005. Expression patterns of TEL genes in Poaceae suggest a conserved association with cell differentiation. J. Exp. Bot. 56:1605–14 [Google Scholar]
  121. Paul MJ, Primavesi LF, Jhurreea D, Zhang Y. 121.  2008. Trehalose metabolism and signaling. Annu. Rev. Plant Biol. 59:417–41 [Google Scholar]
  122. Pérez-Pérez ME, Florencio FJ, Crespo JL. 122.  2010. Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii. Plant Physiol. 152:1874–88 [Google Scholar]
  123. Polge C, Thomas M. 123.  2007. SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control?. Trends Plant Sci. 12:20–28 [Google Scholar]
  124. Raiborg C, Schink KO, Stenmark H. 124.  2013. Class III phosphatidylinositol 3-kinase and its catalytic product PtdIns3P in regulation of endocytic membrane traffic. FEBS J. 280:2730–42 [Google Scholar]
  125. Rebsamen M, Pochini L, Stasyk T, de Araújo ME, Galluccio M. 125.  et al. 2015. SLC38A9 is a component of the lysosomal amino acid sensing machinery that controls mTORC1. Nature 519:477–81 [Google Scholar]
  126. Ren M, Qiu S, Venglat P, Xiang D, Feng L. 126.  et al. 2011. Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiol. 155:1367–82 [Google Scholar]
  127. Ren M, Venglat P, Qiu S, Feng L, Cao Y. 127.  et al. 2012. Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis. Plant Cell 24:4850–74 [Google Scholar]
  128. Rexin D, Meyer C, Robaglia C, Veit B. 128.  2015. TOR signalling in plants. Biochem. J. 470:1–14 [Google Scholar]
  129. Robaglia C, Thomas M, Meyer C. 129.  2012. Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr. Opin. Plant Biol. 15:301–7 [Google Scholar]
  130. Roy B, von Arnim AG. 130.  2013. Translational regulation of cytoplasmic mRNAs. Arabidopsis Book 11:e0165 [Google Scholar]
  131. Ruan YL. 131.  2014. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu. Rev. Plant Biol. 65:33–67 [Google Scholar]
  132. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. 132.  2010. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141:290–303 [Google Scholar]
  133. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC. 133.  et al. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496–501 [Google Scholar]
  134. Schepetilnikov M, Dimitrova M, Mancera-Martínez E, Geldreich A, Keller M, Ryabova LA. 134.  2013. TOR and S6K1 promote translation reinitiation of uORF-containing mRNAs via phosphorylation of eIF3h. EMBO J. 32:1087–102 [Google Scholar]
  135. Schepetilnikov M, Kobayashi K, Geldreich A, Caranta C, Robaglia C. 135.  et al. 2011. Viral factor TAV recruits TOR/S6K1 signalling to activate reinitiation after long ORF translation. EMBO J. 30:1343–56 [Google Scholar]
  136. Schmelzle T, Beck T, Martin DE, Hall MN. 136.  2004. Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol. Cell Biol. 24:338–51 [Google Scholar]
  137. Schumacher K, Krebs M. 137.  2010. The V-ATPase: small cargo, large effects. Curr. Opin. Plant Biol. 13:724–30 [Google Scholar]
  138. Serfontein J, Nisbet RE, Howe CJ, de Vries PJ. 138.  2010. Evolution of the TSC1/TSC2-TOR signaling pathway. Sci. Signal. 3:ra49 [Google Scholar]
  139. Shemi A, Ben-Dor S, Vardi A. 139.  2015. Elucidating the composition and conservation of the autophagy pathway in photosynthetic eukaryotes. Autophagy 11:701–15 [Google Scholar]
  140. Shinozaki-Yabana S, Watanabe Y, Yamamoto M. 140.  2000. Novel WD-repeat protein Mip1p facilitates function of the meiotic regulator Mei2p in fission yeast. Mol. Cell Biol. 20:1234–42 [Google Scholar]
  141. Sormani R, Masclaux-Daubresse C, Daniel-Vedele F, Chardon F. 141.  2011. Transcriptional regulation of ribosome components are determined by stress according to cellular compartments in Arabidopsis thaliana. PLOS ONE 6:e28070 [Google Scholar]
  142. Sormani R, Yao L, Menand B, Ennar N, Lecampion C. 142.  et al. 2007. Saccharomyces cerevisiae FKBP12 binds Arabidopsis thaliana TOR and its expression in plants leads to rapamycin susceptibility. BMC Plant Biol. 7:26 [Google Scholar]
  143. Steffen KK, MacKay VL, Kerr EO, Tsuchiya M, Hu D. 143.  et al. 2008. Yeast life span extension by depletion of 60s ribosomal subunits is mediated by Gcn4. Cell 133:292–302 [Google Scholar]
  144. Stitt M, Zeeman SC. 144.  2012. Starch turnover: pathways, regulation and role in growth. Curr. Opin. Plant Biol. 15:282–92 [Google Scholar]
  145. Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M. 145.  et al. 2009. Starch as a major integrator in the regulation of plant growth. PNAS 106:10348–53 [Google Scholar]
  146. Suttangkakul A, Li F, Chung T, Vierstra RD. 146.  2011. The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. Plant Cell 23:3761–79 [Google Scholar]
  147. Templeton GW, Moorhead GB. 147.  2005. The phosphoinositide-3-OH-kinase-related kinases of Arabidopsis thaliana. EMBO Rep. 6:723–28 [Google Scholar]
  148. Testerink C, Munnik T. 148.  2011. Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J. Exp. Bot. 62:2349–61 [Google Scholar]
  149. Thomas JD, Zhang YJ, Wei YH, Cho JH, Morris LE. 149.  et al. 2014. Rab1A is an mTORC1 activator and a colorectal oncogene. Cancer Cell 26:754–69 [Google Scholar]
  150. Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J. 150.  et al. 2009. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 284:8023–32 [Google Scholar]
  151. Toschi A, Lee E, Xu L, Garcia A, Gadir N, Foster DA. 151.  2009. Regulation of mTORC1 and mTORC2 complex assembly by phosphatidic acid: competition with rapamycin. Mol. Cell Biol. 29:1411–20 [Google Scholar]
  152. Troncoso-Ponce MA, Cao X, Yang Z, Ohlrogge JB. 152.  2013. Lipid turnover during senescence. Plant Sci. 205–206:13–19 [Google Scholar]
  153. Turck F, Kozma SC, Thomas G, Nagy F. 153.  1998. A heat-sensitive Arabidopsis thaliana kinase substitutes for human p70s6k function in vivo. Mol. Cell Biol. 18:2038–44 [Google Scholar]
  154. Turck F, Zilbermann F, Kozma S, Thomas G, Nagy F. 154.  2004. Phytohormones participate in an S6 kinase signal transduction pathway in Arabidopsis. Plant Physiol. 134:1527–35 [Google Scholar]
  155. Turkina MV, Klang Årstrand H, Vener AV. 155.  2011. Differential phosphorylation of ribosomal proteins in Arabidopsis thaliana plants during day and night. PLOS ONE 6:e29307 [Google Scholar]
  156. Urban J, Soulard A, Huber A, Lippman S, Mukhopadhyay D. 156.  et al. 2007. Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol. Cell 26:663–74 [Google Scholar]
  157. Valluru R, Van den Ende W. 157.  2011. Myo-inositol and beyond—emerging networks under stress. Plant Sci. 181:387–400 [Google Scholar]
  158. van Dam TJ, Zwartkruis FJ, Bos JL, Snel B. 158.  2011. Evolution of the TOR pathway. J. Mol. Evol. 73:209–20 [Google Scholar]
  159. Veit B, Briggs SP, Schmidt RJ, Yanofsky MF, Hake S. 159.  1998. Regulation of leaf initiation by the terminal ear 1 gene of maize. Nature 393:166–68 [Google Scholar]
  160. von Arnim AG, Jia Q, Vaughn JN. 160.  2014. Regulation of plant translation by upstream open reading frames. Plant Sci. 214:1–12 [Google Scholar]
  161. Wang S, Tsun ZY, Wolfson RL, Shen K, Wyant GA. 161.  et al. 2015. Lysosomal amino acid transporter SLC38A9 signals arginine sufficiency to mTORC1. Science 347:188–94 [Google Scholar]
  162. Warner JR. 162.  1999. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24:437–40 [Google Scholar]
  163. Watanabe Y, Yamamoto M. 163.  1994. S. pombe mei2+ encodes an RNA-binding protein essential for premeiotic DNA synthesis and meiosis I, which cooperates with a novel RNA species meiRNA. Cell 78:487–98 [Google Scholar]
  164. Williams AJ, Werner-Fraczek J, Chang IF, Bailey-Serres J. 164.  2003. Regulated phosphorylation of 40S ribosomal protein S6 in root tips of maize. Plant Physiol. 132:2086–97 [Google Scholar]
  165. Wullschleger S, Loewith R, Hall MN. 165.  2006. TOR signaling in growth and metabolism. Cell 124:471–84 [Google Scholar]
  166. Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J. 166.  2013. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496:181–86 [Google Scholar]
  167. Xiong Y, Sheen J. 167.  2012. Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. J. Biol. Chem. 287:2836–42 [Google Scholar]
  168. Xiong Y, Sheen J. 168.  2014. The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiol. 164:499–512 [Google Scholar]
  169. Xu Q, Liang S, Kudla J, Luan S. 169.  1998. Molecular characterization of a plant FKBP12 that does not mediate action of FK506 and rapamycin. Plant J. 15:511–19 [Google Scholar]
  170. Yang H, Rudge DG, Koos JD, Vaidialingam B, Yang HJ, Pavletich NP. 170.  2013. mTOR kinase structure, mechanism and regulation. Nature 497:217–23 [Google Scholar]
  171. Yang Y, Yu X, Song L, An C. 171.  2011. ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiol. 156:873–83 [Google Scholar]
  172. Yip CK, Murata K, Walz T, Sabatini DM, Kang SA. 172.  2010. Structure of the human mTOR complex I and its implications for rapamycin inhibition. Mol. Cell 38:768–74 [Google Scholar]
  173. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C. 173.  et al. 2009. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21:2914–27 [Google Scholar]
  174. Zeeman SC, Kossmann J, Smith AM. 174.  2010. Starch: its metabolism, evolution, and biotechnological modification in plants. Annu. Rev. Plant Biol. 61:209–34 [Google Scholar]
  175. Zhang S, Lawton M, Hunter T, Lamb C. 175.  1994. atpk1, a novel ribosomal protein kinase gene from Arabidopsis. I. Isolation, characterization, and expression. J. Biol. Chem. 269:17586–92 [Google Scholar]
  176. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RA. 176.  et al. 2009. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol. 149:1860–71 [Google Scholar]
  177. Zhou F, Roy B, Dunlap JR, Enganti R, von Arnim AG. 177.  2014. Translational control of Arabidopsis meristem stability and organogenesis by the eukaryotic translation factor eIF3h. PLOS ONE 9:e95396 [Google Scholar]
  178. Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM. 178.  2011. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H+-ATPase. Science 334:678–83 [Google Scholar]
/content/journals/10.1146/annurev-arplant-043014-114648
Loading
/content/journals/10.1146/annurev-arplant-043014-114648
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error