Evolution and expression patterns of the trehalose-6-phosphate synthase gene family in drumstick tree (Moringa oleifera Lam.)
Moringa oleifera TPSs were genome-wide identified for the first time, and a phylogenetic analysis was performed to investigate evolutionary divergence. The qRT-PCR data show that MoTPS genes response to different stress treatments.
The trehalose-6-phosphate synthase (TPS) family is involved in a wide range of stress-resistance processes in plants. Its direct product, trehalose-6-phosphate, acts as a specific signal of sucrose status and a regulator to modulate carbon metabolism within the plant. In this study, eight TPS genes were identified and cloned based on the M. oleifera genome; only MoTPS1 exhibited TPS activity among Group I proteins. The characteristics of the MoTPS gene family were determined by analyzing phylogenetic relationships, gene structures, conserved motifs, selective forces, and expression patterns. The Group II MoTPS genes were under relaxed purifying selection or positive selection. The glycosyltransferase family 20 domains generally had lower Ka/Ks ratios and nonsynonymous (Ka) changes compared with those of trehalose-phosphatase domains, which is consistent with stronger purifying selection due to functional constraints in performing TPS enzyme activity. Phylogenetic analyses of TPS proteins from M. oleifera and 17 other plant species indicated that TPS were present before the monocot–dicot split, whereas Group II TPSs were duplicated after the separation of dicots and monocots. Quantitative real-time PCR analysis showed that the expression patterns of TPSs displayed group specificities in M. oleifera. Particularly, Group I MoTPS genes closely relate to reproductive development and Group II MoTPS genes closely relate to high temperature resistance in leaves, stem, stem tip and roots. This work provides a scientific classification of plant TPSs, dissects the internal relationships between their evolution and expressions, and promotes functional researches.
KeywordsAbiotic stress Expression profile Phylogenetic analysis Selective force Trehalose-6-phosphate synthase
Number of non-synonymous substitutions per non-synonymous site
Number of synonymous substitutions per synonymous site
Most recent common ancestor
We would like to thank Professor P. Van Dijck and Xinsheng Hu for their help and guidance.
This study was funded by Forestry Technology Innovation Program, the Department of Forestry of Guangdong Province (2015KJCX009); Guangzhou Science Technology and Innovation Commission (201707010462); Graduate Student Overseas Study Program (2018LHPY014).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Anisimova M, Bielawski JP, Yang Z (2001) The accuracy and power of likelihood ratio tests to detect positive selection at amino acid sites. Mol Biol Evol 18(8):1585–1592. https://doi.org/10.1093/oxfordjournals.molbev.a003945 CrossRefPubMedGoogle Scholar
- Anisimova M, Bielawski JP, Yang Z (2002) Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol Biol Evol 19(6):950–958. https://doi.org/10.1093/oxfordjournals.molbev.a004152 CrossRefPubMedGoogle Scholar
- Avonce N, Wuyts J, Verschooten K, Vandesteene L, 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(2):359–369. https://doi.org/10.1093/molbev/msp241 CrossRefPubMedGoogle Scholar
- Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x CrossRefPubMedGoogle Scholar
- Jang IC, Oh SJ, Seo JS, Choi WB, Sang IS et al (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. https://doi.org/10.1104/pp.007237 CrossRefPubMedPubMedCentralGoogle Scholar
- Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17(10):1483–1498. https://doi.org/10.1093/oxfordjournals.molbev.a026248 CrossRefPubMedGoogle Scholar
- Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ et al (2013) Inhibition of Sn RK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol Biochem 63(4):89–98. https://doi.org/10.1016/j.plaphy.2012.11.011 CrossRefPubMedGoogle Scholar
- Van Dijck P, Mascorro-Gallardo JO, De Bus M, Royackers K, Iturriaga G et al (2002) Truncation of Arabidopsis thaliana and Selaginella lepidophylla trehalose-6-phosphate synthase unlocks high catalytic activity and supports high trehalose levels on expression in yeast. Biochem J 366(1):63–71. https://doi.org/10.1042/BJ20020517 CrossRefPubMedPubMedCentralGoogle Scholar
- Vandesteene L, Lopez-Galvis L, Vanneste K, Feil R, Maere S, Lammens W, Rolland F et al (2012) Expansive evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE gene family in Arabidopsis thaliana. Plant Physiol 160(2):884–896. https://doi.org/10.1104/pp.112.201400 CrossRefPubMedPubMedCentralGoogle Scholar
- Vogel G, Fiehn O, Jean-Richard-Dit-Bressel L et al (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. https://doi.org/10.1093/jexbot/52.362.1817 CrossRefPubMedGoogle Scholar
- Yang ZH, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17(1):32–43. https://doi.org/10.1093/oxfordjournals.molbev.a026236 CrossRefPubMedGoogle Scholar
- Yang ZH, Nielsen R (2002) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19(6):908–917. https://doi.org/10.1093/oxfordjournals.molbev.a004148 CrossRefPubMedGoogle Scholar
- Zhang JJ, Yang YS, Lin MF, Li SQ, Tang Y, Chen HB, Chen XY (2017) An efficient micropropagation protocol for direct organogenesis from leaf explants of an economically valuable plant, drumstick (Moringa oleifera Lam.). Ind Crop Prod 103:59–63. https://doi.org/10.1016/j.indcrop.2017.03.028 CrossRefGoogle Scholar