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. 2020 Sep 23;10(10):1358.
doi: 10.3390/biom10101358.

Characteristics and Expression Analyses of Trehalose-6-Phosphate Synthase Family in Prunus mume Reveal Genes Involved in Trehalose Biosynthesis and Drought Response

Yongjuan Yang  1   2   3   4   5   6   7 , Kaifeng Ma  2   3   4   5   6   7 , Tengxun Zhang  1   2   3   4   5   6   7 , Lulu Li  1   2   3   4   5   6   7 , Jia Wang  2   3   4   5   6   7 , Tangren Cheng  2   3   4   5   6   7 , Qixiang Zhang  1   2   3   4   5   6   7
Affiliations

Characteristics and Expression Analyses of Trehalose-6-Phosphate Synthase Family in Prunus mume Reveal Genes Involved in Trehalose Biosynthesis and Drought Response

Yongjuan Yang et al. Biomolecules. .

Abstract

Trehalose and its key synthase (trehalose-6-phosphate synthase, TPS) can improve the drought tolerance of plants. However, little is known about the roles of trehalose and the TPS family in Prunus mume response to drought. In our study, we discovered that the trehalose content in leaf, root, and stem tissues significantly increased in P. mume in response to drought. Therefore, the characteristics and functions of the TPS family are worth investigating in P. mume. We identified nine TPS family members in P. mume, which were divided into two sub-families and characterized by gene structure, promoter elements, protein conserved domains, and protein motifs. We found that the Hydrolase_3 domain and several motifs were highly conserved in Group II instead of Group I. The distinctions between the two groups may result from selective constraints, which we estimated by the dN/dS (ω) ratio. The ω values of all the PmTPS family gene pairs were evaluated as less than 1, indicating that purity selection facilitated their divergence. A phylogenetic tree was constructed using 92 TPSs from 10 Rosaceae species, which were further divided into five clusters. Based on evolutionary analyses, the five clusters of TPS family proteins mainly underwent varied purity selection. The expression patterns of PmTPSs under drought suggested that the TPS family played an important role in the drought tolerance of P. mume. Combining the expression patterns of PmTPSs and the trehalose content changes in leaf, stem, and root tissues under normal conditions and drought stress, we found that the PmTPS2 and PmTPS6 mainly function in the trehalose biosynthesis in P. mume. Our findings not only provide valuable information about the functions of trehalose and TPSs in the drought response of P. mume, but they also contribute to the future drought breeding of P. mume.

Keywords: drought stress; evolution analysis; expression pattern; trehalose biosynthesis; trehalose-6-phosphate synthase.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
The relative water content changes of soil (a) and leaf tissues (b) during the drought period. Value is the mean of three replicates ± standard error.
Figure 2
Figure 2
The trehalose content in the tissues (a) of Prunus mume and leaves (b), stems (c), and roots (d) in response to drought. Value is the mean of three replicates ± standard error. Lowercase letter represents the significant level.
Figure 3
Figure 3
Chromosomal location of trehalose-6-phosphate synthase (TPS) family genes in Prunus mume. Nine TPS genes were located in four chromosomes. Pm1, Pm2, Pm3, Pm4, Pm5, Pm6, Pm7, and Pm8 represent eight chromosomes of P. mume, respectively.
Figure 4
Figure 4
Gene structure and promoter elements of TPS genes within P. mume. (a) Exons and introns structure of TPSs in P. mume. The orange round-corner rectangle represents exons, the blue rectangle depicts untranslated region (UTR) regions, the black line shows introns, and numbers (0, 1, 2) represent the intron phase. (b) Cis-acting elements of the TPSs promoter in P. mume. Two thousand bp upstream regions of PmTPS genes were used for predicting cis-acting elements. Different color rectangles represent distinct cis-acting elements in response to abiotic stress, phytohormone, circadian regulation, and plant development.
Figure 5
Figure 5
Protein conserved domains and motifs distribution of TPS family members in P. mume. (a) The protein conserved domains, glycosyltransferase 20 family (Glyco_transf_20), trehalose phosphatase (Trehalose_PPase), and haloacid dehalogenase-like hydrolase (Hydrolase_3) domains are presented by green, yellow, and pink round-corner rectangle, respectively. (b) Motif compositions of TPSs in P. mume. The distributions of 20 conserved motifs are represented by different colored boxes.
Figure 6
Figure 6
The selection pressure assessment with TPS gene pairs, genes domains, and two groups of the TPS family in Prunus mume. The frequency distributions of dN/dS for (a) the full length of PmTPSs, (b) glycosyltransferase 20 family, (c) trehalose phosphatase, and (d) outside domains, respectively. The black triangle represents the average value of dN/dS ratio. (e) The average value of dN, dS, and dN/dS in the Group I and Group II TPS family genes. (f) The frequency distribution of dS for TPS gene pairs in P. mume.
Figure 7
Figure 7
The phylogenetic tree of TPS family members from Prunus mume (PmTPS), P. persica (PpTPS), P. yedoensis (PyTPS), P. armeniaca (PaTPS), Fragaria vesca (FvTPS), Malus domestica (MdTPS), P. dulcis (PdTPS), Pyrus bretschneideri (PbTPS), Rosa chinensis (RcTPS), and Rubus occidentalis (RoTPS). The pink, #A3DFC8, violet, #E9C031, and #FF8E54 colored regions represent Groups I, II1, II2, II3, and II4, respectively. TPSs from 10 Rosaceae species are labeled by circles of red, fuchsia, lime, coral, cadet blue, sienna, green, blue violet, yellow, and blue colors, respectively. All of the referred TPS genes are listed in Table S3.
Figure 8
Figure 8
Type I functional divergence among the TPS family members of Rosacaea. Posterior probability analysis of specific amino acid sites was used for identifying critical amino acid residues. The cutoff = 0.95 is shown by the dotted line.
Figure 9
Figure 9
Expression patterns of PmTPSs among leaf, stem, and root tissues of Prunus mume. (a) The heat map represents the expression levels of nine PmTPSs among leaf, stem, and root tissues. Data of gene expression levels (RPKM, Reads Per Kilobase of exon model per Million mapped reads) was normalized by log2 transformed data. Red and blue indicate high- and low-expression profiles, respectively. (b) The scatter plot figure shows RPKM values of nine PmTPSs in leaf, stem, and root tissues.
Figure 10
Figure 10
Expression patterns of TPS family genes in leaf (a), stem (b), and root (c) tissues of Prunus mume under drought stress by qRT-PCR. The abscissa axis represents water deficiency for 0d, 3d, 7d, 12d, and 15d. All qRT-PCR results are presented as mean value ± standard error from three biological replicates.
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References

    1. Elbein A.D., Pan Y.T., Pastuszak I., Carroll D. New insights on trehalose: A multifunctional molecule. Glycobiology. 2003;13:17R–27R. doi: 10.1093/glycob/cwg047. - DOI - PubMed
    1. Garg A.K., Kim J.K., Owens T.G., Ranwala A.P., Choi Y.D., Kochian L.V., Wu R.J. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc. Natl. Acad. Sci. USA. 2002;99:15898–15903. doi: 10.1073/pnas.252637799. - DOI - PMC - PubMed
    1. Bell W., Sun W., Hohmann S., Wera S., Reinders A., De Virgilio C., Wiemken A., Thevelein J.M. Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. J. Biol. Chem. 1998;273:33311–33319. doi: 10.1074/jbc.273.50.33311. - DOI - PubMed
    1. 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., et al. A Selaginella lepidophylla trehalose-6-phosphate synthase complements growth and stress-tolerance defects in a yeast tps1 mutant. Plant Physiol. 1999;119:1473–1482. doi: 10.1104/pp.119.4.1473. - DOI - PMC - PubMed
    1. El-Bashiti T., Hamamcı H., Öktem H.A., Yücel M. Biochemical analysis of trehalose and its metabolizing enzymes in wheat under abiotic stress conditions. Plant Sci. 2005;169:47–54. doi: 10.1016/j.plantsci.2005.02.024. - DOI

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