Abstract
Trehalose plays an important role in metabolic regulation and abiotic stress tolerance in plants. Trehalose contents are potentially modulated by trehalose-6-phosphate synthase (TPS), which is a key enzyme in the trehalose biosynthetic pathway. Using available wheat expressed sequence tag sequence information from NCBI and two wheat genome databases, we identified 12 wheat TPS genes and performed a comprehensive study on their structural, evolutionary and functional properties. The estimated divergence time of wheat TPS gene pairs and wheat–rice orthologues suggested that wheat and rice have a common ancestor. The number of TPS genes in the wheat genome was estimated to be at least 12, which is close to the number found in rice, Arabidopsis and soybean. Moreover, it has been reported earlier in other plants that TPS genes respond to abiotic stress, however, our study mainly analysed the TPS gene family under freezing conditions in winter wheat, and determined that most of the TPS gene expression in winter wheat was induced by freezing conditions, which further suggested that wheat TPS genes were involved in winter wheat freeze-resistance signal transduction pathways. Taken together, the current study represents the first comprehensive study of TPS genes in winter wheat and provides a foundation for future functional studies of this important gene family in Triticeae.
Similar content being viewed by others
References
Akladious S. A. 2012 Influence of different soaking times with selenium on growth, metabolic activities of wheat seedlings under low temperature stress. Afr. J. Biotechnol. 11, 14792–14804.
Almeida A. M., Villalobos E., Araújo S. S., Leyman B., Van Dijck P., Alfaro-Cardoso L., et al. 2005 Transformation of tobacco with an Arabidopsis thaliana gene involved in trehalose biosynthesis increases tolerance to several abiotic stresses. Euphytica 146, 165–176.
Arora A. and Singh V. P. 2006 Polyols regulate the flower senescence by delaying programmed cell death in gladiolus. J. Plant Biochem. Biotechnol. 15, 139–142.
Avonce N., Leyman B., Mascorro-Gallardo J. O., Van Dijck P., Thevelein J. M. and Iturriaga G. 2004 The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol. 136, 3649–3659.
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.
Brenchley R., Spannagl M., Pfeifer M., Barker GL. A., D’Amore R., Allen A. M., et al. 2012 Analysis of the breadwheat genome using whole-genome shotgun sequencing. Nature 491, 705–710.
Chary S. N., Hicks G. R., Choi Y. G., Carter D. and Raikhel N. V. 2008 Trehalose-6-phosphate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis. Plant Physiol. 146, 97–107.
Dijken A. J. H., Schluepmann H. and Smeekens S. C. M. 2004 Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol. 135, 969–977.
Elbein A. D. 1974 The metabolism of alpha, alpha-trehalose. Adv. Carbohydr. Chem. Biochem. 30, 227–256.
Elbein A. D., Pan Y. T., Pastuszak I. and Carroll D. 2003 New insights on trehalose: a multifunctional molecule. Glycobiology 13, 17R–27R.
Gaut B. S., Morton B. R., McCaig B. C. and Clegg M. T. 1996 Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc. Natl. Acad. Sci. USA 93, 10274–10279.
Goddijn O. J. and van Dun K. 1999 Trehalose metabolism in plants. Trends. Plant. Sci. 4, 315–319.
Gomez L. D., Gilday A., Feil R., Lunn J. K. and Graham L. 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.
Huang X. Q. and Madan A. 1999 CAP3: A DNA sequence assembly program. Genome Res. 9, 868–877.
Iordachescu M. and Imai R. 2008 Trehalose biosynthesis in response to abiotic stresses. J. Integr. Plant. Biol. 50, 1223–1229.
Jiang W., Fu F. L., Zhang S. Z., Wu L. and Li W. C. 2010 Cloning and characterization of functional trehalose-6-phosphate synthase gene in maize. J. Plant. Biol. 53, 134–141.
Kim S. J., Jeong D. H., An G. and Kim S. R. 2005 Characterization of a drought-responsive gene, OsTPS1, identified by the T-DNA gene-trap system in rice. J. Plant. Biol. 48, 371–379.
Kosmas S. A., Argyrokastritis A., Loukas M. G., Eliopoulos E., Tsakas S. and Kaltsikes P. J. 2006 Isolation and characterization of drought-related trehalose 6-phosphate-synthase gene from cultivated cotton (Gossypium hirsutum L.) Planta 223, 329–339.
Li H. W., Zang B. S., Deng X. W. and Wang X. P. 2011 Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234, 1007–1018.
Librado P. and Rozas J. 2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
Liu L. J., Cang J., Yu J., Wang X., Huang R., Wang J. F., et al. 2013 Effects of exogenous abscisic acid on carbohydrate metabolism and the expression levels of correlative key enzymes in winter wheat under low temperature. Biosci. Biotechnol. Biochem. 77, 516–525.
Livak K. J. and Schmittgen T. D. 2001 Analysis of relative gene expression data using real-time quantitative pcr and the 2 −##Δ####Δ##ct method. Methods 25, 402–408.
Lunn J. E. 2007 Gene families and evolution of trehalose metabolism in plants. Funct. Plant. Biol. 34, 550–563.
Lyu J. I., Min S. R., Lee J. H., Lim Y. H., Kim J. K., Bae C. H., et al. 2013 Overexpression of a trehalose-6-phosphate synthase/phosphatase fusion gene enhances tolerance and photosynthesis during drought and salt stress without growth aberrations in tomato. Plant Cell Tiss. Organ Cult. 112, 257–262.
Mayer K. X., Rogers J., Dolezel J., Pozniak C., Eversole K. and Feuillet C. 2014 A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345, 1251788.
O’Hara L. E., Paul M. J. and Wingler A. 2013 How do sugars regulate plant growth and development? New insight into the role of trehalose-6-phosphate. Mol. Plant. 6, 261–274.
Redillas M. C. F. R., Park S. H., Lee J. W., Kim Y. S., Jeong J. S., Jung H., et al. 2012 Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress. Plant Biotechnol. Rep. 6, 89–96.
Saitou N. and Nei M. 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.
Singh N. K., Gupta D. K., Jayaswal P. K., Mahato M. K., Dutta S., Singh S., et al. 2012 The first draft of the pigeonpea genome sequence. J. Plant. Biochem. Biotechnol. 21, 98–112.
Suzuki N., Bajad S., Shuman J., Shulaev V. and Mittler R. 2008 The transcriptional co-activator mbf1c is a key regulator of thermotolerance in Arabidopsis thaliana. J. Biol. Chem. 283, 9269–9275.
Tamura K., Dudley J., Nei M. and Kumar S. 2007 MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.
Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F. and Higgins D. G. 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882.
Timothy L. B., Mikael B., Fabian A. B., Martin F., Charles E. G., Luca C., et al. 2009 MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202–W208.
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.
Wang X. N., Fu L. S., Li Z. F., Sun Y. L., Wang Y. B., Liu C., et al. 2009 Morphogenesis and physiological basis in wheat cultivars with different levels of cold-resistance during cold acclimation and freezing period. Acta. Agron. Sin. 35, 1313–1319 (in Chinese).
Wang Y. J., Hao Y. J., Zhang Z. G., Chne T., Zhang J. S. and Chen S. Y. 2005 Isolation of trehalose-6-phosphate phosphatase gene from tobacco and its functional analysis in yeast cells. J. Plant. Physiol. 162, 215–223.
Yang H. L., Liu Y. J., Wang C. L. and Zeng Q. Y. 2012 Molecular evolution of trehalose-6-phosphate synthase (TPS) gene family in populus, arabidopsis and rice. PLoS One 7, e42438.
Yu J., Wang J., Lin W., Li S. G., Li H., Zhou J., et al. 2005 The genomes of Oryza sativa: a history of duplications. PLoS Biol. 3, e38.
Zang B., Li H., Li W., Deng X. W. and Wang X. 2011 Analysis of trehalose-6-phosphate synthase (TPS) gene family suggests the formation of TPS complexes in rice. Plant Mol. Biol. 76, 507–522.
Zentella R., Mascorro-Gallardo J. O., Dijck P. V., Folch-Mallol J., Bonini B., Vaeck C. V., et al. 1999 Selaginella lepidophylla trehalose-6-phosphate synthase complements growth and stress-tolerance defects in a yeast tps1 mutant. Plant Physiol. 119, 1473–1482.
Acknowledgements
This work was supported by the Graduate Student Innovation Research Project in Heilongjiang Province (YJSCX2012-036HLJ) and was supported by the Doctor Research Startup Fund of Northeast Agricultural University (2010RCB17).
Author information
Authors and Affiliations
Corresponding author
Additional information
[Xie D. W., Wang X. N., Fu L. S., Sun J., Zheng W. and Li Z. F. 2015 Identification of the trehalose-6-phosphate synthase gene family in winter wheat and expression analysis under conditions of freezing. J. Genet. 94, xx–xx]
Rights and permissions
About this article
Cite this article
XIE, D.W., WANG, X.N., FU, L.S. et al. Identification of the trehalose-6-phosphate synthase gene family in winter wheat and expression analysis under conditions of freezing stress. J Genet 94, 55–65 (2015). https://doi.org/10.1007/s12041-015-0495-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12041-015-0495-z