Analysis of trehalose-6-phosphate synthase (TPS) gene family suggests the formation of TPS complexes in rice (original) (raw)

• Adams RP, Kendall E, Kartha KK (1990) Comparison of Free Sugars in Growing Desiccated Plants of Selaginella-Lepidophylla. Biochem Systemat Ecol 18(2–3):107–110
  Article CAS Google Scholar
• Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136(3):3649–3659
  Article PubMed CAS Google Scholar
• Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G (2006) Insights on the evolution of trehalose biosynthesis. BMC Evol Biol 6:109
  Article PubMed Google Scholar
• Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448(7156):938–942
  Article PubMed CAS Google Scholar
• Bart R, Chern M, Park C-J, Bartley L, Ronald PC (2006) A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Meth 2:13
  Article Google Scholar
• Bell W, Klaassen P, Ohnacker M, Boller T, Herweijer M, Schoppink P, Van der Zee P, Wiemken A (1992) Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation. Eur J Biochem 209(3):951–959
  Article PubMed CAS Google Scholar
• Bell W, Sun W, Hohmann S, Wera S, Reinders A, De Virgilio C, Wiemken A, Thevelein JM (1998) Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. J Biol Chem 273(50):33311–33319
  Article PubMed CAS Google Scholar
• Blazquez MA, Santos E, Flores CL, Martinez-Zapater JM, Salinas J, Gancedo C (1998) Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J 13(5):685–689
  Article PubMed CAS Google Scholar
• Chary SN, Hicks GR, Choi YG, Carter D, Raikhel NV (2007) Trehalose-6-phosphate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis. Plant Physiol
• Contento AL, Kim SJ, Bassham DC (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol 135(4):2330–2347
  Article PubMed CAS Google Scholar
• De Virgilio C, Burckert N, Bell W, Jeno P, Boller T, Wiemken A (1993) Disruption of TPS2, the gene encoding the 100-kDa subunit of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae, causes accumulation of trehalose-6-phosphate and loss of trehalose-6-phosphate phosphatase activity. Eur J Biochem 212(2):315–323
  Article PubMed Google Scholar
• Drennan PM, Smith MT, Goldsworthy D, Vanstaden J (1993) The Occurrence of Trehalose in the Leaves of the Desiccation-Tolerant Angiosperm Myrothamnus-Flabellifolius Welw. J Plant Physiol 142(4):493–496
  CAS Google Scholar
• Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JD, Smeekens SC, Graham IA (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29(2):225–235
  Article PubMed CAS Google Scholar
• Elbein AD (1974) The metabolism of alpha, alpha-trehalose. Adv Carbohydr Chem Biochem 30:227–256
  Article PubMed CAS Google Scholar
• Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13(4):17R–27R
  Article PubMed CAS Google Scholar
• Elble R (1992) A simple and efficient procedure for transformation of yeasts. Biotechniques 13(1):18–20
  PubMed CAS Google Scholar
• Felsenstein J (1993) PHYLIP: phylogenetic inference package. Distributed by the author: Department of Genetics, University of WashingtonSeattle, WA
• Garcia AB, Engler J, Iyer S, Gerats T, Van Montagu M, Caplan AB (1997) Effects of Osmoprotectants upon NaCl Stress in Rice. Plant Physiol 115(1):159–169
  PubMed CAS Google Scholar
• Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci U S A 99(25):15898–15903
  Article PubMed CAS Google Scholar
• Ge LF, Chao DY, Shi M, Zhu MZ, Gao JP, Lin HX (2008) Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228(1):191–201
  Article PubMed CAS Google Scholar
• Geelen D, Royackers K, Vanstraelen M, De Bus M, Inze D, Van Dijck P, Thevelein JM, Leyman B (2007) Trehalose-6-P synthase AtTPS1 high molecular weight complexes in yeast and Arabidopsis. Plant Sci 173(4):426–437
  Article CAS Google Scholar
• Gibson RP, Turkenburg JP, Charnock SJ, Lloyd R, Davies GJ (2002) Insights into trehalose synthesis provided by the structure of the retaining glucosyltransferase OtsA. Chem Biol 9(12):1337–1346
  Article PubMed CAS Google Scholar
• Glinski M, Weckwerth W (2005) Differential multisite phosphorylation of the trehalose-6-phosphate synthase gene family in Arabidopsis thaliana: a mass spectrometry-based process for multiparallel peptide library phosphorylation analysis. Mol Cell Proteomics 4(10):1614–1625
  Article PubMed CAS Google Scholar
• Goddijn OJ, van Dun K (1999) Trehalose metabolism in plants. Trends Plant Sci 4(8):315–319
  Article PubMed Google Scholar
• Goddijn OJ, Verwoerd TC, Voogd E, Krutwagen RW, de Graaf PT, van Dun K, Poels J, Ponstein AS, Damm B, Pen J (1997) Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol 113(1):181–190
  Article PubMed CAS Google Scholar
• Gomez LD, Baud S, Gilday A, Li Y, Graham IA (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(1):69–84
  Article PubMed CAS Google Scholar
• Gonzalez MI, Stucka R, Blazquez MA, Feldmann H, Gancedo C (1992) Molecular cloning of CIF1, a yeast gene necessary for growth on glucose. Yeast 8(3):183–192
  Article PubMed CAS Google Scholar
• Harthill JE, Meek SE, Morrice N, Peggie MW, Borch J, Wong BH, Mackintosh C (2006) Phosphorylation and 14–3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose. Plant J 47(2):211–223
  Article PubMed CAS Google Scholar
• Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6(2):271–282
  Article PubMed CAS Google Scholar
• Holmstrom KO, Mantyla E, Welin B, Mandal A, Palva ET (1996) Drought tolerance in tobacco. Nature 379(6567):683–684
  Article Google Scholar
• Hottiger T, Boller T, Wiemken A (1987) Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett 220(1):113–115
  Article PubMed CAS Google Scholar
• Hounsa CG, Brandt EV, Thevelein J, Hohmann S, Prior BA (1998) Role of trehalose in survival of Saccharomyces cerevisiae under osmotic stress. Microbiology 144(Pt 3):671–680
  Article PubMed CAS Google Scholar
• Jang IC, Oh SJ, Seo JS, Choi WB, Song SI, Kim CH, Kim YS, Seo HS, Choi YD, Nahm BH, Kim JK (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131(2):516–524
  Article PubMed CAS Google Scholar
• Karim S, Aronsson H, Ericson H, Pirhonen M, Leyman B, Welin B, Mantyla E, Palva ET, Van Dijck P, Holmstrom KO (2007) Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol Biol 64(4):371–386
  Article PubMed CAS Google Scholar
• Karimi M, Inze D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7(5):193–195
  Article PubMed CAS Google Scholar
• Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci U S A 102(31):11118–11123
  Article PubMed CAS Google Scholar
• Lewis JG, Learmonth RP, Attfield PV, Watson K (1997) Stress co-tolerance and trehalose content in baking strains of Saccharomyces cerevisiae. J Ind Microbiol Biotechnol 18(1):30–36
  Article PubMed CAS Google Scholar
• Leyman B, Van Dijck P, Thevelein JM (2001) An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. Trends Plant Sci 6(11):510–513
  Article PubMed CAS Google Scholar
• Londesborough J, Vuorio O (1991) Trehalose-6-phosphate synthase/phosphatase complex from bakers’ yeast: purification of a proteolytically activated form. J Gen Microbiol 137(2):323–330
  PubMed CAS Google Scholar
• Lorenz MC, Muir RS, Lim E, McElver J, Weber SC, Heitman J (1995) Gene disruption with PCR products in Saccharomyces cerevisiae. Gene 158(1):113–117
  Article PubMed CAS Google Scholar
• Lunn JE (2007) Gene families and evolution of trehalose metabolism in plants. Funct Plant Biol 34(6):550–563. doi:10.1071/FP06315
  Article CAS Google Scholar
• Lunn JE, Feil R, Hendriks JH, Gibon Y, Morcuende R, Osuna D, Scheible WR, Carillo P, Hajirezaei MR, 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(1):139–148
  Article PubMed CAS Google Scholar
• Marquez-Escalante JA, Figueroa-Soto CG, Valenzuela-Soto EM (2006) Isolation and partial characterization of trehalose 6-phosphate synthase aggregates from Selaginella lepidophylla plants. Biochimie 88(10):1505–1510
  Article PubMed CAS Google Scholar
• Miranda JA, Avonce N, Suarez R, Thevelein JM, Van Dijck P, Iturriaga G (2007) A bifunctional TPS-TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226(6):1411–1421
  Article PubMed CAS Google Scholar
• Muller J, Boller T, Wiemken A (1995) Trehalose and trehalase in plants: Recent developments. Plant Sci 112(1):1–9
  Article Google Scholar
• Osuna D, Usadel B, Morcuende R, Gibon Y, Blasing OE, Hohne M, Gunter M, Kamlage B, Trethewey R, Scheible WR, Stitt M (2007) Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 49(3):463–491
  Article PubMed CAS Google Scholar
• Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35(Database issue):D883–D887
  Article PubMed CAS Google Scholar
• Pellny TK, Ghannoum O, Conroy JP, Schluepmann H, Smeekens S, Andralojc J, Krause KP, Goddijn O, Paul MJ (2004) Genetic modification of photosynthesis with E. coli genes for trehalose synthesis. Plant Biotechnol J 2(1):71–82
  Article PubMed CAS Google Scholar
• Peng Z, Serino G, Deng XW (2001) Molecular characterization of subunit 6 of the COP9 signalosome and its role in multifaceted developmental processes in Arabidopsis. Plant Cell 13(11):2393–2407
  Article PubMed CAS Google Scholar
• Pramanik MH, Imai R (2005) Functional identification of a trehalose 6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Mol Biol 58(6):751–762
  Article PubMed CAS Google Scholar
• Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16(8):2128–2150
  Article PubMed CAS Google Scholar
• Ramon M, De Smet I, Vandesteene L, Naudts M, Leyman B, Van Dijck P, Rolland F, Beeckman T, Thevelein JM (2009) Extensive expression regulation and lack of heterologous enzymatic activity of the Class II trehalose metabolism proteins from Arabidopsis thaliana. Plant Cell Environ 32(8):1015–1032
  Article PubMed CAS Google Scholar
• Reinders A, Burckert N, Hohmann S, Thevelein JM, Boller T, Wiemken A, De Virgilio C (1997) Structural analysis of the subunits of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae and their function during heat shock. Mol Microbiol 24(4):687–695
  Article PubMed CAS Google Scholar
• Romero C, Belles JM, Vaya JL, Serrano R, CulianezMacia FA (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: Pleiotropic phenotypes include drought tolerance. Planta 201(3):293–297
  Article PubMed CAS Google Scholar
• Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D (2006) A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441(7090):227–230
  Article PubMed CAS Google Scholar
• Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci U S A 100(11):6849–6854
  Article PubMed CAS Google Scholar
• Schluepmann H, van Dijken A, Aghdasi M, Wobbes B, Paul M, Smeekens S (2004) Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol 135(2):879–890
  Article PubMed CAS Google Scholar
• Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95(11):5857–5864
  Article PubMed CAS Google Scholar
• Sheen J (2002) A transient expression assay using Arabidopsis mesophyll protoplasts. http://geneticsmghharvardedu/sheenweb/
• Shima S, Matsui H, Tahara S, Imai R (2007) Biochemical characterization of rice trehalose-6-phosphate phosphatases supports distinctive functions of these plant enzymes. Febs J 274(5):1192–1201
  Article PubMed CAS Google Scholar
• Thaller MC, Schippa S, Rossolini GM (1998) Conserved sequence motifs among bacterial, eukaryotic, and archaeal phosphatases that define a new phosphohydrolase superfamily. Protein Sci 7(7):1647–1652
  Article PubMed CAS Google Scholar
• Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882
  Article PubMed CAS Google Scholar
• Valenzuela-Soto EM, Marquez-Escalante JA, Iturriaga G, Figueroa-Soto CG (2004) Trehalose 6-phosphate synthase from Selaginella lepidophylla: purification and properties. Biochem Biophys Res Commun 313(2):314–319
  Article PubMed CAS Google Scholar
• van Dijken AJ, Schluepmann H, Smeekens SC (2004) Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135(2):969–977
  Article PubMed Google Scholar
• Vandesteene L, Ramon M, Le Roy K, Van Dijck P, 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(2):406–419
  Article PubMed CAS Google Scholar
• Vogel G, Aeschbacher RA, Muller J, Boller T, Wiemken A (1998) Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant J 13(5):673–683
  Article PubMed CAS Google Scholar
• Vogel G, Fiehn O, Jean-Richard-dit-Bressel L, Boller T, Wiemken A, Aeschbacher RA, Wingler A (2001) Trehalose metabolism in Arabidopsis: occurrence of trehalose and molecular cloning and characterization of trehalose-6-phosphate synthase homologues. J Exp Bot 52(362):1817–1826
  Article PubMed CAS Google Scholar
• Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40(3):428–438
  Article PubMed CAS Google Scholar
• Wang YJ, Hao YJ, Zhang ZG, Chen T, Zhang JS, Chen SY (2005) Isolation of trehalose-6-phosphate phosphatase gene from tobacco and its functional analysis in yeast cells. J Plant Physiol 162(2):215–223
  Article PubMed CAS Google Scholar
• Wang HJ, Wan AR, Hsu CM, Lee KW, Yu SM, Jauh GY (2007) Transcriptomic adaptations in rice suspension cells under sucrose starvation. Plant Mol Biol 63(4):441–463
  Article PubMed CAS Google Scholar
• Wingler A, Fritzius T, Wiemken A, Boller T, Aeschbacher RA (2000) Trehalose induces the ADP-glucose pyrophosphorylase gene, ApL3, and starch synthesis in Arabidopsis. Plant Physiol 124(1):105–114
  Article PubMed CAS Google Scholar
• Zentella R, Mascorro-Gallardo JO, Van Dijck P, Folch-Mallol J, Bonini B, Van Vaeck C, Gaxiola R, Covarrubias AA, Nieto-Sotelo J, Thevelein JM, Iturriaga G (1999) A Selaginella lepidophylla trehalose-6-phosphate synthase complements growth and stress-tolerance defects in a yeast tps1 mutant. Plant Physiol 119(4):1473–1482
  Article PubMed CAS Google Scholar
• Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of Snf1-related protein kinase (SnRK1) activity and regulation of metabolic pathways by trehalose 6-phosphate. Plant Physiol. doi:10.1104/pp.108.133934
• Zhao W, Wang J, He X, Huang X, Jiao Y, Dai M, Wei S, Fu J, Chen Y, Ren X, Zhang Y, Ni P, Zhang J, Li S, Wang J, Wong GK, Zhao H, Yu J, Yang H, Wang J (2004) BGI-RIS: an integrated information resource and comparative analysis workbench for rice genomics. Nucleic Acids Res 32(Database issue):D377–D382
  Article PubMed CAS Google Scholar