Sugar metabolism and the plant target of rapamycin kinase: A sweet operaTOR?

Frontiers in Plant Science

Volumn 4, Issue APR, 2013, Pages

  Dobrenel, Thomas ^a   Marchive, Chloé ^a   Azzopardi, Marianne ^a   Clément, Gilles ^a   Moreau, Manon ^a,b   Sormani, Rodnay ^a   Robaglia, Christophe ^b   Meyer, Christian ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b DIF   (France)

Author keywords

Myo inositol 1 phosphate synthase; Raffinose; Starch; Target of rapamycin; TOR serine threonine kinases

Indexed keywords

EID: 84893497909     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00093     Document Type: Review

References (56)

1. Anderson, G., Veit, B., and Hanson, M. (2005). The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth. BMC Biol. 3:12. doi: 10.1186/1741-7007-3-12
2. Ball, S., Colleoni, C., Cenci, U., Raj, J. N., and Tirtiaux, C. (2011). The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J. Exp. Bot. 62, 1775-1801.
3. Binda, M., Peli-Gulli, M. P., Bonfils, G., Panchaud, N., Urban, J., Sturgill, T. W., et al. (2009). The Vam6 GEF controls TORC1 by activating the EGO complex. Mol. Cell 35, 563-573.
4. Broach, J. R. (2012). Nutritional control of growth and development in yeast. Genetics 192, 73-105.
5. Caldana, C., Li, Y., Leisse, A., Zhang, Y., Bartholomaeus, L., Fernie, A. R., et al. (2013). Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. Plant J. 73, 897-909.
6. Cornu, M., Albert, V., and Hall, M. N. (2013). mTOR in aging, metabolism, and cancer. Curr. Opin. Genet. Dev. doi: 10.1016/j.gde.2012.12.005 [Epub ahead of print].
7. Crespo, J., Díaz-Troya, S., and Florencio, F. (2005). Inhibition of target of rapamycin signaling by rapamycin in the unicellular green alga Chlamydomonas reinhardtii. Plant Physiol. 139, 1736-1749.
8. Deprost, D., Truong, H., Robaglia, C., and Meyer, C. (2005). An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development. Biochem. Biophys. Res. Commun. 326, 844-850.
9. Deprost, D., Yao, L., Sormani, R., Moreau, M., Leterreux, G., Nicolaï, M., et al. (2007). The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep. 8, 864-870.
10. De Virgilio, C., and Loewith, R. (2006). The TOR signalling network from yeast to man. Int. J. Biochem. Cell Biol. 38, 1476-1481.
11. Díaz-Troya, S., Florencio, F., and Crespo, J. (2008). Target of rapamycin and LST8 proteins associate with membranes from the endoplasmic reticulum in the unicellular green alga Chlamydomonas reinhardtii. Eukaryot. Cell 7, 212-222.
12. Dobrenel, T., Marchive, C., Sormani, R., Moreau, M., Mozzo, M., Montané, M. H., et al. (2011). Regulation of plant growth and metabolism by the TOR kinase. Biochem. Soc. Trans. 39, 477-481.
13. Düvel, K., Yecies, J. L., Menon, S., Raman, P., Lipovsky, A. I., Souza, A. L., et al. (2010). Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol. Cell 39, 171-183.
14. Efeyan, A., Zoncu, R., Chang, S., Gumper, I., Snitkin, H., Wolfson, R. L., et al. (2013). Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival. Nature 493, 679-683.
15. Feldman, M. E., Apsel, B., Uotila, A., Loewith, R., Knight, Z. A., Ruggero, D., et al. (2009). Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol. 7:e38. doi: 10.1371/journal.pbio.1000038
16. Guertin, D. A., and Sabatini, D. M. (2009). The pharmacology of mTOR inhibition. Sci. Signal. 2, pe24.
17. Gulati, P., Gaspers, L. D., Dann, S. G., Joaquin, M., Nobukuni, T., Natt, F., et al. (2008). Amino acids activate mTOR complex 1 via Ca2+/CaM signaling to hVps34. Cell Metab. 7, 456-465.
18. Heitman, J., Movva, N. R., and Hall, M. N. (1991). Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253, 905-909.
19. John, F., Roffler, S., Wicker, T., and Ringli, C. (2011). Plant TOR signaling components. Plant Signal. Behav. 6, 1700-1705.
20. Keunen, E., Peshev, D., Vangronsveld, J., Van den Ende, W., and Cuypers, A. (2013). Plant sugars are crucial players in the oxidative challenge during abiotic stress. Extending the traditional concept. Plant Cell Environ. doi: 10.1111/pce.12061 [Epub ahead of print].
21. Laplante, M., and Sabatini, D. M. (2012). mTOR signaling in growth control and disease. Cell 149, 274-293.
22. Lee, M. N., Ha, S. H., Kim, J., Koh, A., Lee, C. S., Kim, J. H., et al. (2009). Glycolytic flux signals to mTOR through glyceraldehyde-3-phosphate dehydrogenase-mediated regulation of Rheb. Mol. Cell. Biol. 29, 3991-4001.
23. Leiber, R., John, F., Verhertbruggen, Y., Diet, A., Knox, J., and Ringli, C. (2010). The TOR pathway modulates the structure of cell walls in Arabidopsis. Plant Cell 22, 1898-1908.
24. Liu, Y., and Bassham, D. (2010). TOR is a negative regulator of autophagy in Arabidopsis thaliana. PLoS ONE 5:e11883. doi: 10.1371/journal.pone.0011883
25. Loewith, R., and Hall, M. N. (2011). Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189, 1177-1201.
26. Ma, J., Hanssen, M., Lundgren, K., Hernandez, L., Delatte, T., Ehlert, A., et al. (2011). The sucrose-regulated Arabidopsis transcription factor bZIP11 reprograms metabolism and regulates trehalose metabolism. New Phytol. 191, 733-745.
27. Ma, X. M., and Blenis, J. (2009). Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10, 307-318.
28. Mahfouz, M., Kim, S., Delauney, A., and Verma, D. (2006). Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18, 477-490.
29. Menand, B., Desnos, T., Nussaume, L., Berger, F., Bouchez, D., Meyer, C., et al. (2002). Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc. Natl. Acad. Sci. U.S.A. 99, 6422-6427.
30. Meng, P. H., Raynaud, C., Tcherkez, G., Blanchet, S., Massoud, K., Domenichini, S., et al. (2009). Crosstalks between myo-inositol metabolism, programmed cell death and basal immunity in Arabidopsis. PLoS ONE 4:e7364. doi: 10.1371/journal.pone.0007364
31. Moreau, M., Azzopardi, M., Clément, G., Dobrenel, T., Marchive, C., Renne, C., et al. (2012). Mutations in the Arabidopsis homolog of LST8/Gβ L, a partner of the target of Rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 24, 463-481.
32. Nishizawa, A., Yabuta, Y., and Shigeoka, S. (2008). Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 1251-1263.
33. Peters, S., Egert, A., Stieger, B., and Keller, F. (2010). Functional identification of Arabidopsis ATSIP2 (At3g57520) as an alkaline alpha-galactosidase with a substrate specificity for raffinose and an apparent sink-specific expression pattern. Plant Cell Physiol. 51, 1815-1819.
34. Ren, M., Qiu, S., Venglat, P., Xiang, D., Feng, L., Selvaraj, G., et al. (2011). Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiol. 155, 1367-1382.
35. Ren, M., Venglat, P., Qiu, S., Feng, L., Cao, Y., Wang, E., et al. (2012). Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis. Plant Cell 24, 4850-4874.
36. Robaglia, C., Thomas, M., and Meyer, C. (2012). Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr. Opin. Plant Biol. 15, 301-307.
37. Rohde, J. R., Bastidas, R., Puria, R., and Cardenas, M. E. (2008). Nutritional control via Tor signaling in Saccharomyces cerevisiae. Curr. Opin. Microbiol. 11, 153-160.
38. Saux, C., Lemoine, Y., Marion-Poll, A., Valadier, M. H., Deng, M., and Morot-Gaudry, J. F. (1987). Consequence of absence of nitrate reductase activity on photosynthesis in Nicotiana plumbaginifolia plants. Plant Physiol. 84, 67-72.
39. Schepetilnikov, M., Kobayashi, K., Geldreich, A., Caranta, C., Robaglia, C., Keller, M., et al. (2011). Viral factor TAV recruits TOR/S6K1 signalling to activate reinitiation after long ORF translation. EMBO J. 6, 1343-1356.
40. Schmelzle, T., Beck, T., Martin, D. E., and Hall, M. N. (2004). Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol. Cell. Biol. 24, 338-351.
41. Schumacher, K., and Krebs, M. (2010). The V-ATPase: small cargo, large effects. Curr. Opin. Plant Biol 13, 724-730.
42. Siaut, M., Cuine, S., Cagnon, C., Fessler, B., Nguyen, M., Carrier, P., et al. (2011). Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol. 11:7. doi: 10.1186/1472-6750-11-7
43. Sormani, R., Yao, L., Menand, B., Ennar, N., Lecampion, C., Meyer, C., et al. (2007). Saccharomyces cerevisiae FKBP12 binds Arabidopsis thaliana TOR and its expression in plants leads to rapamycin susceptibility. BMC Plant Biol. 7:26. doi: 10.1186/1471-2229-7-26
44. Stitt, M., and Zeeman, S. C. (2012). Starch turnover: pathways, regulation and role in growth. Curr. Opin. Plant Biol. 15, 282-292.
45. Sulpice, R., Pyl, E. T., Ishihara, H., Trenkamp, S., Steinfath, M., Witucka-Wall, H., et al. (2009). Starch as a major integrator in the regulation of plant growth. Proc. Natl. Acad. Sci. U.S.A. 106, 10348-10353.
46. Sulpice, R., Trenkamp, S., Steinfath, M., Usadel, B., Gibon, Y., Witucka-Wall, H., et al. (2010). Network analysis of enzyme activities and metabolite levels and their relationship to biomass in a large panel of Arabidopsis accessions. Plant Cell 22, 2872-2893.
47. Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., et al. (2002). Important roles of drought-and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29, 417-426.
48. Thoreen, C. C., Kang, S. A., Chang, J. W., Liu, Q., Zhang, J., Gao, Y., et al. (2009). An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 284, 8023-8032.
49. Turck, F., Zilbermann, F., Kozma, S., Thomas, G., and Nagy, F. (2004). Phytohormones participate in an S6 kinase signal transduction pathway in Arabidopsis. Plant Physiol. 134, 1527-1535.
50. Valluru, R., and Van den Ende, W. (2011). Myo-inositol and beyond-emerging networks under stress. Plant Sci. 181, 387-400.
51. Wang, X., and Proud, C. G. (2011). mTORC1 signaling: what we still don't know. J. Mol. Cell Biol. 3, 206-220.
52. Wullschleger, S., Loewith, R., and Hall, M. (2006). TOR signaling in growth and metabolism. Cell 124, 471-484.
53. Xiong, Y., and Sheen, J. (2012). Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. J. Biol. Chem. 287, 2836-2842.
54. Xu, Q., Liang, S., Kudla, J., and Luan, S. (1998). Molecular characterization of a plant FKBP12 that does not mediate action of FK506 and rapamycin. Plant J. 15, 511-519.
55. Yecies, J. L., and Manning, B. D. (2011). Transcriptional control of cellular metabolism by mTOR signaling. Cancer Res. 71, 2815-2820.
56. Zoncu, R., Bar-Peled, L., Efeyan, A., Wang, S., Sancak, Y., and Sabatini, D. M. (2011). mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H+-ATPase. Science 334, 678-683