Trehalose-6-phosphate synthase 1 is not the only active TPS in Arabidopsis thaliana

Biochemical Journal

Volumn 466, Issue , 2015, Pages 283-290

  Delorge, Ines ^a   Figueroa, Carlos M ^b   Feil, Regina ^b   Lunn, John E ^b   Van Dijck, Patrick ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

Arabidopsis thaliana; Saccharomyces cerevisiae; Trehalose; Trehalose 6 phosphate; Trehalose phosphatase (TPP); Trehalose 6 phosphate synthase (TPS)

Indexed keywords

ENZYME; GLUCOSE; TREHALOSE; TREHALOSE 6 PHOSPHATE; TREHALOSE 6 PHOSPHATE SYNTHASE 1; TREHALOSE 6 PHOSPHATE SYNTHASE 11; TREHALOSE 6 PHOSPHATE SYNTHASE 2; TREHALOSE 6 PHOSPHATE SYNTHASE 4; TREHALOSE 6 PHOSPHATE SYNTHASE 5; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; GLUCOSYLTRANSFERASE; ISOENZYME; MUTANT PROTEIN; RECOMBINANT PROTEIN; SUGAR PHOSPHATE; TREHALOSE-6-PHOSPHATE; TREHALOSE-6-PHOSPHATE SYNTHASE;

ARABIDOPSIS THALIANA; ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FLOWERING; MUTANT; NONHUMAN; PHENOTYPE; PLANT GENE; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; TPS GENE; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ARABIDOPSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; TWO HYBRID SYSTEM;

ARABIDOPSIS THALIANA; EMBRYOPHYTA; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CONSERVED SEQUENCE; GLUCOSYLTRANSFERASES; ISOENZYMES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SUGAR PHOSPHATES; TREHALOSE; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84923165698     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20141322     Document Type: Article

References (44)

1. Drennan, P.M., Smith, M.T., Goldsworthy, D. and Van Staden, J. (1993) The occurrence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius Welw. J. Plant Physiol. 142, 493-496 CrossRef
2. Pampurova, S. and Van Dijck, P. (2014) The desiccation tolerant secrets of Selaginella lepidophylla : what we have learned so far? Plant Physiol. Biochem. 80, 285-290 CrossRef PubMed
3. Leyman, B., Van Dijck, P. and Thevelein, J.M. (2001) An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. Trends Plant Sci. 6, 510-513 CrossRef PubMed
4. Lunn, J.E. (2007) Gene families and evolution of trehalose metabolism in plants. Funct. Plant Biol. 34, 550-563 CrossRef
5. Avonce, N., Wuyts, J., Verschooten, K., Vandesteene, L. and Van Dijck, P. (2010) The Cytophaga hutchinsonii ChTPSP: first characterized bifunctional TPS-TPP protein as putative ancestor of all eukaryotic trehalose biosynthesis proteins. Mol. Biol. Evol. 27, 359-369 CrossRef PubMed
6. Eastmond, P.J., van Dijken, A. J. H., Spielman, M., Kerr, A., Tissier, A.F., Dickinson, H.G., Jones, J. D. G., Smeekens, S.C. and Graham, I.A. (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J. 29, 225-235 CrossRef PubMed
7. Schluepmann, H., Pellny, T., van Dijken, A., Smeekens, S. and Paul, M. (2003) Trehalose 6-phosphate is indispensible for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 100, 6849-6854 CrossRef PubMed
8. van Dijken, A.J., Schluepmann, H. and Smeekens, S.C. (2004) Arabidopsis trahalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol. 135, 969-977 CrossRef PubMed
9. Satoh-Nagasawa, N., Nagasawa, N., Malcomber, S., Sakai, H. and Jackson, D. (2006) A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441, 227-230 CrossRef PubMed
10. Gómez, L.D., Baud, S., Gilday, A., Li, Y. and Graham, I.A. (2006) Delayed embryo development in the Arabidopsis trehalose-6-phosphate synthase 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation. Plant J. 46, 69-84 CrossRef PubMed
11. Gómez, L.D., Gilday, A., Feil, R., Lunn, J.E. and Graham, I.A. (2010) AtTPS1-mediated trehalose 6-phosphate synthesis is essential for embryogenic and vegetative growth and responsiveness to ABA in germinating seeds and stomatal guard cells. Plant J. 64, 1-13 PubMed
12. Wahl, V., Ponnu, J., Schlereth, A., Arrivault, S., Langenecker, T., Franke, A., Feil, R., Lunn, J.E., Stitt, M. and Schmid, M. (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339, 704-707 CrossRef PubMed
13. Vandesteene, L., Lopez-Galvis, L., Vanneste, K., Feil, R., Maere, S., Lammens, W., Rolland, F., Lunn, J.E., Avonce, N., Beeckman, T. and Van Dijck, P. (2012) Expansive evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE gene family in Arabidopsis thaliana. Plant Physiol. 160, 884-896 CrossRef PubMed
14. Van Houtte, H., Lopez-Galvis, L., Vandesteene, L., Beeckman, T. and Van Dijck, P. (2013) Redundant and non-redundant roles of the trehalose-6 phosphate phosphatases in leave growth, root hair specification and energy-responses in Arabidopsis. Plant Signal. Behav. 8, e23209 CrossRef PubMed
15. Martins, M.C., Hejazi, M., Fettke, J., Steup, M., Feil, R., Krause, U., Arrivault, S., Vosloh, D., Figueroa, C.M., Ivakov, A. et al. (2013) Feedback inhibition of starch degradation in Arabidopsis leaves mediated by trehalose 6-phosphate. Plant Physiol. 163, 1142-1163 CrossRef PubMed
16. Lunn, J.E., Feil, R., Hendriks, J. H. M., Gibon, Y., Morcuende, R., Osuna, D., Scheible, W.-R., Carillo, P., Hajirezae, M.-R. and Stitt, M. (2006) Sugar-induced increases in trehalose-6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem. J. 397, 139-148 CrossRef PubMed
17. Yadav, U.P., Ivakov, A., Feil, R., Duan, G.Y., Walthe, D., Giavalisco, P., Piques, M., Carillo, P., Hubberten, H.M., Stitt, M. and Lunn, J.E. (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J. Exp. Bot. 65, 1051-1068 CrossRef PubMed
18. Lunn, J.E., Delorge, I., Figueroa, C.M., Van Dijck, P. and Stitt, M. (2014) Trehalose metabolism in plants. Plant J. 79, 544-567 CrossRef PubMed
19. Avonce, N., Mendoza-Vargas, A., Morett, E. and Iturriaga, G. (2006) Insights on the evolution of trehalose biosynthesis. BMC Evol. Biol. 6, 109 CrossRef PubMed
20. Vandesteene, L., Ramon, M., Le Roy, K., Van Dijck, P. and Rolland, F. (2010) A single active trehalose-6-P synthase (TPS) and a family of putative regulatory TPS-like proteins in Arabidopsis. Mol. Plant 3, 406-419 CrossRef PubMed
21. Blazquez, M.A., Santos, E., Flores, C.L., Martinez Zapater, J.M., Salinas, J. and Gancedo, C. (1998) Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J. 13, 685-689 CrossRef PubMed
22. Zentella, R., Mascorro-Gallardo, J.O., Van Dijck, P., Folch-Mallol, J., Bonini, B., Van Vaeck, C., Gaxiola, R., Covarrubias, A.A., Nieto-Sotelo, J., Thevelein, J.M. and Iturriaga, G. (1999) A Selaginella lepidophylla trehalose-6-phosphate synthase complements growth and stress-tolerance defects in a yeast tps1 mutant. Plant Physiol. 119, 1473-1482 CrossRef PubMed
23. Van Dijck, P., Mascorro-Gallardo, J.O., De Bus, M., Royackers, K., Iturriaga, G. and Thevelein, J.M. (2002) Truncation of Arabidopsis thaliana and Selaginella lepidophylla trehalose-6-phosphate synthase (TPS) unlocks high catalytic activity and supports high trehalose levels upon expression in yeast. Biochem. J. 366, 63-71 PubMed
24. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Sch ölkopf, B., Weigel, D. and Lohmann, J.U. (2005) A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506 CrossRef PubMed
25. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 CrossRef PubMed
26. Gibson, R.P., Turkenburg, J.P., Charnock, S.J., Lloyd, R.M. and Davies, G.J. (2002) Insights into trehalose synthesis provided by the structure of the retaining glucosyltransferase OtsA. Chem. Biol. 9, 1337-1346 CrossRef PubMed
27. Hohmann, S., Neves, M.J., de Koning, W., Alijo, R., Ramos, J. and Thevelein, J.M. (1993) The growth and signalling defects of the ggs1 (fdp1/byp1) deletion mutant on glucose are suppressed by a deletion of the gene encoding hexokinase PII. Curr. Genet. 23, 281-289 CrossRef PubMed
28. Gietz, R.D., Schliestl, R.H., Willems, A.R. and Woods, R.A. (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11, 355-360 CrossRef PubMed
29. Carillo, P., Feil, R., Gibon, Y., Satoh-Nagasawa, N., Jackson, D., Bläsing, O.E., Stitt, M. and Lunn, J.E. (2013) A fluorometric assay for trehalose in the picomole range. Plant Methods 9, 21 CrossRef PubMed
30. Gibson, R.P., Lloyd, R.M., Charnock, S.J. and Davies, G.J. (2002) Characterization of Escherichia coli OtsA, a trehalose-6-phosphate synthase from glycosyltransferase family 20. Acta Crystallogr. D Biol. Crystallogr. 58, 349-351 CrossRef PubMed
31. Bonini, B.M., Van Dijck, P. and Thevelein, J.M. (2003) Uncoupling of the glucose growth defect and the deregulation of glycolysis in Saccharomyces cerevisiae Tps1 mutants expressing trehalose-6-phosphate-insensitive hexokinase from Schizosaccharomyces pombe. Biochim. Biophys. Acta 1606, 83-93 CrossRef PubMed
32. Bonini, B.M., Van Vaeck, C., Larsson, C., Gustafsson, L., Ma, P., Winderickx, J., Van Dijck, P. and Thevelein, J.M. (2000) Expression of Escherichia coli otsA in a Saccharomyces cerevisiae tps1 mutant restores trehalose-6-phosphate levels and partly restores growth and fermentation with glucose and control of glucose influx into glycolysis. Biochem. J. 350, 261-268 CrossRef PubMed
33. Geelen, D., Royackers, K., Vanstraelen, M., Inzé, D., Van Dijck, P., Thevelein, J.M. and Leyman, B. (2007) Trehalose-6-P synthase: AtTPS1 high molecular weight complexes in yeast and Arabidopsis. Plant Sci. 173, 426-437 CrossRef
34. Ramon, M., De Smet, I., Vandesteene, L., Naudts, M., Leyman, B., Van Dijck, P., Rolland, F., Beeckman, T. and Thevelein, J.M. (2009) Extensive expression regulation and lack of heterologous enzymatic acivity of the Class II trehalose metabolism proteins from Arabidopsis thaliana. Plant Cell Environ. 32, 1015-1032 CrossRef PubMed
35. Martin, M. and Heredia, C.F. (1977) Characterization of a phosphatase specific for 2-deoxyglucose-6-phosphate in a yeast mutant. FEBS Lett. 83, 245-248 CrossRef PubMed
36. Randez-Gil, F., Prieto, J.A. and Sanz, P. (1995) The expression of a specific 2-deoxyglucose-6P phosphatase prevents catabolite repression mediated by 2-deoxyglucose in yeast. Curr. Genet. 28, 101-107 CrossRef PubMed
37. Toivari, M.H., Ruohonen, L., Miasnikov, A.N., Richard, P. and Penttilä, M. (2007) Metabolic engineering of Saccharomyces cerevisiae for conversion of D-glucose to xylitol and other five-carbon sugars and sugar alcohols. Appl. Environ. Microbiol. 73, 5471-5476 CrossRef PubMed
38. Lutfiyya, L.L., Iyer, V.R., DeRisi, J., DeVit, M.J., Brown, P.O. and Johnston, M. (1998) Characterization of three related glucose repressors and genes they regulate in Saccharomyces cerevisiae. Genetics 150, 1377-1391 PubMed
39. Vyas, V.K., Kuchin, S. and Carlson, M. (2001) Interaction of the repressors Nrg1 and Nrg2 with the Snf1 protein kinase in Saccharomyces cerevisiae. Genetics 158, 563-572 PubMed
40. Tsujimoto, Y., Izawa, S. and Inoue, Y. (2000) Cooperative regulation of DOG2, encoding 2-deoxyglucose-6-phophate phosphatase, by Snf1 kinase and the high-osmolarity glycerol-mitogen-activated protein kinase cascade in stress responses of Saccharomyces cerevisiae. J. Bacteriol. 182, 5121-5126 CrossRef PubMed
41. Bell, W., Sun, W., Hohmann, S., Wera, S., Reinders, A., De Virgilio, C., Wiemken, A. and Thevelein, J.M. (1998) Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. J. Biol. Chem. 273, 33311-33319 CrossRef PubMed
42. Schneitz, K., Hulskamp, M. and Pruitt, R.E. (1995) Wild-type ovule development in Arabidopsis thaliana : a light microscope study of cleared whole-mount tissue. Plant J. 7, 731-749 CrossRef
43. Brown, R.C., Lemmon, B.E. and Nguyen, H. (2002) Endosperm development. In Annual Plant Reviews: Plant Reproduction (O'Neill, S.D. and Roberts, J.A., eds), pp. 193-220, Sheffield University Press, Sheffield
44. Nguyen, H., Brown, R.C. and Lemmon, B.E. (2000) The specialized chalazal endosperm in Arabidopsis thaliana and Lepidium virginicum (Brassicaceae). Protoplasma 212, 99-110 CrossRef