Genome-Wide Identification, Evolution, and Expression Analysis of TPS and TPP Gene Families in Brachypodium distachyon
Abstract
:1. Introduction
2. Results
2.1. Identification of TPS and TPP Family Members in Brachypodium distachyon
2.2. Gene Structure, Multiple Sequence Alignment, and Phylogenetic Analyses of BdTPSs/BdTPPs
2.3. Protein Sequences and Motif Analysis in BdTPSs/TPPs
2.4. Chromosomal Locations and Evolution Analysis
2.5. Transcription Factor Regulatory Network and Stress-Related Cis-Elements in the Promoter Regions and Gene Interaction Expression Network Prediction of BdTPSs/BdTPPs
2.6. Expression Patterns of BdTPSs–BdTPPs in Different Tissues and Stress Conditions
3. Discussion
4. Conclusions
5. Materials and Methods
5.1. Gene Identification
5.2. Gene Structure, Protein Properties, and Conserved Motif Analysis
5.3. Prediction of Cis-Elements, Transcription Factor Regulatory Network, and Gene Interaction Network
5.4. Sequence Alignment and Phylogenetic and Evolution Analyses
5.5. Plant Growth, Stress Treatment, and qRT-PCR Analysis
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Abbreviations
References
- Pandey, G.K.; Pandey, A.; Prasad, M.; Böhmer, M. Editorial: Abiotic Stress Signaling in Plants: Functional Genomic Intervention. Front. Plant Sci. 2016, 7, 681–685. [Google Scholar] [CrossRef] [PubMed]
- Avonce, N.; Mendoza-Vargas, A.; Morett, E.; Iturriaga, G. Insights on the evolution of trehalose biosynthesis. BMC Evol. Biol. 2006, 6, 109–114. [Google Scholar] [CrossRef] [PubMed]
- Horlacher, R.; Boos, W. Characterization of TreR, the major regulator of the Escherichia coli trehalose system. J. Biol. Chem. 1997, 272, 13026–13032. [Google Scholar] [CrossRef] [PubMed]
- Hounsa, C.G.; Brandt, E.V.; Thevelein, J.; Hohmann, S.; Prior, B. Role of trehalose in survival of Saccharomyces cerevisiae under osmotic stress. Microbiology 1998, 144, 671–680. [Google Scholar] [CrossRef] [PubMed]
- StrøM, A.R.; Kaasen, I. Trehalose metabolism in Escherichia coli: Stress protection and stress regulation of gene expression. Mol. Microbiol. 2010, 8, 205–210. [Google Scholar] [CrossRef]
- Thevelein, J.M. Regulation of trehalose mobilization in fungi. Microbiol. Rev. 1984, 48, 42–59. [Google Scholar]
- Elbein, A.D.; Pan, Y.T.; Irena, P.; David, C. New insights on trehalose: a multifunctional molecule. Glycobiology 2003, 13, 17R–27R. [Google Scholar] [CrossRef]
- Zang, B.; Li, H.; Li, W.; Deng, X.W.; Wang, X. Analysis of trehalose-6-phosphate synthase (TPS) gene family suggests the formation of TPS complexes in rice. Plant Mol. Biol. 2011, 76, 507–522. [Google Scholar] [CrossRef]
- Müller, J.; Boller, T. Trehalose and trehalase in plants: Recent developments. Plant Sci. 1995, 112, 1–9. [Google Scholar]
- Bhandal, I.S.; Hauptmann, R.M.; Widholm, J. Trehalose as cryoprotectant for the freeze preservation of carrot and tobacco cells. Plant Physiol. 1985, 78, 430–432. [Google Scholar] [CrossRef]
- Hottiger, T.; De, V.C.; Hall, M.N.; Boller, T.; Wiemken, A. The role of trehalose synthesis for the acquisition of thermotolerance in yeast: II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro. Eur. J. Biochem. 2010, 219, 187–193. [Google Scholar] [CrossRef] [PubMed]
- Cai, Z.; Peng, G.; Cao, Y.; Liu, Y.; Jin, K.; Xia, Y. Bioengineering, Trehalose-6-phosphate synthase 1 from Metarhizium anisopliae: clone, expression and properties of the recombinant. J. Biosci. Bioeng. 2009, 107, 499–505. [Google Scholar] [CrossRef] [PubMed]
- Marquez-Escalante, J.A.; Figueroa-Soto, C.G.; Valenzuela-Soto, E.M. Isolation and partial characterization of trehalose 6-phosphate synthase aggregates from Selaginella lepidophylla plants. Biochimie (Paris) 2006, 88, 1505–1510. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Li, J.; Li, F.; Liu, H.; Yang, W.; Chong, K.; Xu, Y. OsMAPK3 Phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Dev. Cell. 2017, 43, 731. [Google Scholar] [CrossRef] [PubMed]
- Lyu, J.I.; Min, S.R.; Lee, J.H.; Lim, Y.H.; Kim, J.K.; Bae, C.H.; Liu, J. 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 Tissue Organ. Cult. 2013, 112, 257–262. [Google Scholar] [CrossRef]
- Figueroa, C.M.; Lunn, J. A tale of two sugars - trehalose 6-phosphate and sucrose. Plant Physiol. 2016, 172, 7. [Google Scholar] [CrossRef] [PubMed]
- Londesborough, J.; Vuorio, O.E. Purification of trehalose synthase from baker’s yeast. Its temperature-dependent activation by fructose 6-phosphate and inhibition by phosphate. Eur. J. Biochem. 1993, 216, 841–848. [Google Scholar] [CrossRef]
- Pan, Y.T.; Carroll, J.D.; Elbein, A.D. Trehalose-phosphate synthase of Mycobacterium tuberculosis. Cloning, expression and properties of the recombinant enzyme. Eur. J. Biochem. 2002, 269, 6091–6100. [Google Scholar] [CrossRef]
- Valenzuela-Soto, E.M.; Marquez-Escalante, J.A.; Iturriaga, G.; Figueroa-Soto, C.G. Trehalose 6-phosphate synthase from Selaginella lepidophylla: purification and properties. Biochem. Biophys. Res. Commun. 2004, 313, 314–319. [Google Scholar] [CrossRef]
- Pan, Y.T.; Koroth Edavana, V.; Jourdian, W.J.; Edmondson, R.; Carroll, J.D.; Pastuszak, I.; Elbein, A.D. Trehalose synthase of Mycobacterium smegmatis: purification, cloning, expression, and properties of the enzyme. Eur. J. Biochem. 2004, 271, 4259–4269. [Google Scholar] [CrossRef]
- Avonce, N.; Wuyts, J.; Verschooten, K.; Vandesteene, L.; Van Dijck, P. The Cytophaga hutchinsonii ChTPSP: First characterized bifunctional TPS-TPP protein as putative ancestor of all eukaryotic trehalose biosynthesis proteins. Mol. Biol. Evol. 2010, 27, 359–369. [Google Scholar] [CrossRef] [PubMed]
- Lunn, J.E. Gene families and evolution of trehalose metabolism in plants. Funct. Plant Biol. 2007, 34, 550–563. [Google Scholar] [CrossRef]
- Lunn, J.E.; Delorge, I.; Dijck, P. Trehalose metabolism in plants. Plant J. Cell Mol. Biol. 2015, 79, 544–567. [Google Scholar] [CrossRef] [PubMed]
- Vandesteene, L.; López-Galvis, L.; Vanneste, K.; Feil, R.; Maere, S.; Lammens, W.; Rolland, F.; Lunn, J.E.; Avonce, N.; Beeckman, T.; et al. Expansive evolution of the trehalose-6-phosphate phosphatase gene family in Arabidopsis. Plant Physiol. 2012, 160, 884–896. [Google Scholar] [CrossRef] [PubMed]
- Eastmond, P.J.; Li, Y.; Graham, I. Is trehalose-6-phosphate a regulator of sugar metabolism in plants? J. Exp. Bot. 2003, 54, 533–537. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leyman, B.; Van Dijck, P.; Thevelein, J.M. An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. Trends Plant Sci. 2001, 6, 510–513. [Google Scholar] [CrossRef]
- Yang, H.; Liu, Y.; Wang, C.; Zeng, Q. Molecular evolution of trehalose-6-phosphate synthase (TPS) gene family in Populus, Arabidopsis and rice. PLoS ONE 2012, 7, e42438. [Google Scholar] [CrossRef]
- Figueroa, C.M.; Feil, R.; Ishihara, H.; Watanabe, M.; Kölling, K.; Krause, U.; Höhne, M.; Encke, B.; Plaxton, W.C.; Zeeman, S.; et al. Trehalose 6-phosphate coordinates organic and amino acid metabolism with carbon availability. Plant J. 2016, 85, 410–423. [Google Scholar] [CrossRef]
- Yadav, U.P.; Ivakov, A.; Feil, R.; Duan, G.Y.; Walther, D.; Giavalisco, P.; Piques, M.; Carillo, P.; Hubberten, H.M.; Stitt, M.; et al. The sucrose-trehalose 6-phosphate (Tre6P) nexus: Specificity and mechanisms of sucrose signalling by Tre6P. J. Exp. Bot. 2014, 65, 1051–1068. [Google Scholar] [CrossRef]
- Kolbe, A.; Tiessen, A.; Schluepmann, H.; Paul, M.; Ulrich, S.; Geigenberger, P. Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc. Natl. Acad. Sci. USA 2005, 102, 11118–11123. [Google Scholar] [CrossRef] [Green Version]
- Wingler, A.; Fritzius, T.; Wiemken, A.; Boller, T.; Aeschbacher, R.A. Trehalose induces the ADP-glucose pyrophosphorylase gene, ApL3, and starch synthesis in Arabidopsis. Plant Physiol. 2000, 124, 105–114. [Google Scholar] [CrossRef]
- Zhang, Y.; Primavesi, L.F.; Jhurreea, D.; Andralojc, P.J.; Mitchell, R.A.; Powers, S.J.; Schluepmann, H.; Delatte, T.; Wingler, A.; Paul, M.J. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol. 2009, 149, 1860–1871. [Google Scholar] [CrossRef]
- Baena-Gonzalez, E.; Rolland, F.; Thevelein, J.M.; Sheen, J. A central integrator of transcription networks in plant stress and energy signalling. Nature 2007, 448, 938–942. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Ge, L.F.; Chao, D.Y.; Shi, M.; Zhu, M.Z.; Gao, J.P.; Lin, H.X. Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 2008, 228, 191–201. [Google Scholar] [CrossRef]
- Guo, B.T.; Weng, M.L.; Qiao, L.X.; Feng, Y.B.; Li, W.; Zhang, P.Y.; Wang, X.L.; Sui, J.M.; Tao, L.; Duan, D. Expression of Porphyra yezoensis TPS gene in transgenic rice enhanced the salt tolerance. Int. J. Plant Breed. Genet. 2014, 2, 45–55. [Google Scholar]
- Jang, I.-C.; Oh, S.J.; Seo, J.S.; Choi, W.B.; Song, S.I.; Kim, C.H.; Kim, Y.S.; Seo, H.S.; Choi, Y.D.; Nahm, B.H.; et al. 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. 2003, 131, 516–524. [Google Scholar] [CrossRef]
- Miranda, J.A.; Avonce, N.; Suárez, R.; Thevelein, J.M.; Van Dijck, P.; Iturriaga, G. A bifunctional TPS-TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 2007, 226, 1411–1421. [Google Scholar] [CrossRef]
- Romero, C.; Bellés, J.M.; Vayá, J.L.; Serrano, R.; Culiánez-Macià, F.A. Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 1997, 201, 293–297. [Google Scholar] [CrossRef]
- Avonce, N.; Leyman, B.; Mascorro-Gallardo, J.O.; Van Dijck, P.; Thevelein, J.M.; Iturriaga, G. The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol. 2004, 136, 3649–3659. [Google Scholar] [CrossRef]
- Nuccio, M.L.; Wu, J.; Mowers, R.; Zhou, H.P.; Meghji, M.; Primavesi, L.F.; Paul, M.J.; Chen, X.; Gao, Y.; Haque, E.; et al. Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nat. Biotechnol. 2015, 33, 862–869. [Google Scholar] [CrossRef] [PubMed]
- Brkljacic, J.; Grotewold, E.; Scholl, R.; Mockler, T.; Garvin, D.F.; Vain, P.; Brutnell, T.; Sibout, R.; Bevan, M.; Budak, H.; et al. Brachypodium as a model for the grasses: today and the future. Plant Physiol. 2011, 157, 3–13. [Google Scholar] [CrossRef] [PubMed]
- The International Brachypodium Initiative. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 2010, 463, 763–770. [Google Scholar]
- Jin, Q.; Hu, X.; Li, X.; Wang, B.; Wang, Y.; Jiang, H.; Mattson, N.; Xu, Y. Genome-Wide Identification and Evolution Analysis of Trehalose-6-Phosphate Synthase Gene Family in Nelumbo nucifera. Front. Plant Sci. 2016, 7, 1445–1457. [Google Scholar] [CrossRef] [PubMed]
- Lin, M.; Jia, R.; Li, J.; Zhang, M.; Chen, H.; Zhang, D.; Zhang, J.; Chen, X. Evolution and expression patterns of the trehalose-6-phosphate synthase gene family in drumstick tree (Moringa oleifera Lam.). Planta 2018, 248, 999–1015. [Google Scholar] [CrossRef]
- Mu, M.; Lu, X.K.; Wang, J.J.; Wang, D.L.; Yin, Z.J.; Wang, S.; Fan, W.L.; Ye, W. Genome-wide Identification and analysis of the stress-resistance function of the TPS (Trehalose-6-Phosphate Synthase) gene family in cotton. BMC Genet. 2016, 17, 54. [Google Scholar]
- Xu, Y.; Wang, Y.; Mattson, N.; Yang, L.; Jin, Q. Genome-wide analysis of the Solanum tuberosum (potato) trehalose-6-phosphate synthase (TPS) gene family: evolution and differential expression during development and stress. BMC Genom. 2017, 18, 926. [Google Scholar] [CrossRef]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef]
- Vandesteene, L.; Ramon, M.; Le Roy, K.; Van Dijck, P.; Rolland, F. A single active trehalose-6-P synthase (TPS) and a family of putative regulatory TPS-like proteins in Arabidopsis. Mol. Plant. 2010, 3, 406–419. [Google Scholar] [CrossRef]
- Poueymiro, M.; Cazalé, A.C.; Francois, J.M.; Parrou, J.L.; Peeters, N.; Genin, S. A Ralstonia solanacearum type III effector directs the production of the plant signal metabolite trehalose-6-phosphate. mBio 2014, 5, e02065-14. [Google Scholar] [CrossRef]
- Van Dijck, P.; Mascorro-Gallardo, J.O.; De Bus, M.; Royackers, K.; Iturriaga, G.; Thevelein, J.M. 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. 2002, 366, 63–71. [Google Scholar] [CrossRef] [PubMed]
- Gu, Z.; Cavalcanti, A.; Chen, F.C.; Bouman, P.; Li, W. Extent of Gene Duplication in the Genomes of Drosophila, Nematode, and Yeast. Mol. Biol. Evol. 2002, 19, 256–262. [Google Scholar] [CrossRef] [PubMed]
- Yuan, J.; Liu, T.; Yu, Z.; Li, Y.; Ren, H.; Hou, X.; Li, Y. Genome-wide analysis of the Chinese cabbage IQD gene family and the response of BrIQD5 in drought resistance. Plant Mol. Biol. 2019, 99, 603–620. [Google Scholar] [CrossRef] [PubMed]
- Hurst, L.D. The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet. 2002, 18, 486–487. [Google Scholar] [CrossRef]
- Van Dijken, A.J.H.; Schluepmann, H.; Smeekens, S.C.M. Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol. 2004, 135, 969–977. [Google Scholar] [CrossRef] [PubMed]
- Li, H.W.; Zang, B.S.; Deng, X.W.; Wang, X.P. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 2011, 234, 1007–1018. [Google Scholar] [CrossRef] [PubMed]
- Cao, J.; Min, J.; Peng, L.; Chu, Z. Genome-wide identification and evolutionary analyses of the PP2C gene family with their expression profiling in response to multiple stresses in Brachypodium distachyon. BMC Genom. 2016, 17, 175. [Google Scholar] [CrossRef]
- Kuromori, T.; Mizoi, J.; Umezawa, T.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Stress Signaling Networks: Drought Stress. In Molecular Biology; Springer: New York, NY, USA, 2013; pp. 1–23. [Google Scholar]
- Wei, L.; Xiao, C.; Zhaolu, M.; Xiahe, H.; Qi, X.; Heng, W.; Hailing, J.; Dabing, Z.; Wanqi, L. Transcriptional regulation of Arabidopsis MIR168a and ARGONAUTE1 homeostasis in abscisic acid and abiotic stress responses. Plant Physiol. 2012, 158, 1279–1292. [Google Scholar]
- Todaka, D.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front. Plant Sci. 2015, 6, 84–104. [Google Scholar] [CrossRef]
- Zhang, T.; Tan, D.; Li, Z.; Zhang, X.; Han, Z. Phylogenetic analysis and drought-responsive expression profiles of the WRKY transcription factor family in maize. Agri Gene. 2017, 3, 99–108. [Google Scholar] [CrossRef]
- Sibout, R.; Proost, S.; Hansen, B.O.; Vaid, N.; Giorgi, F.M.; Ho-Yue-Kuang, S.; Legee, F.; Cezart, L.; Bouchabke-Coussa, O.; Soulhat, C.; et al. Expression atlas and comparative coexpression network analyses reveal important genes involved in the formation of lignified cell wall in Brachypodium distachyon. New Phytol. 2017, 215, 1009–1025. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.C.; Luan, S. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ. 2012, 35, 53–60. [Google Scholar] [CrossRef] [PubMed]
- Xie, D.W.; Wang, X.; Sun, J.; Zheng, W. Identification of the trehalose-6-phosphate synthase gene family in winter wheat and expression analysis under conditions of freezing stress. J. Genet. 2015, 94, 55–65. [Google Scholar] [CrossRef] [PubMed]
- Nuruzzaman, M.; Manimekalai, R.; Sharoni, A.M.; Satoh, K.; Kondoh, H.; Ooka, H.; Kikuchi, S. Genome-wide analysis of NAC transcription factor family in rice. Gene 2010, 465, 30–44. [Google Scholar] [CrossRef] [PubMed]
- Koski, T. Hidden Markov models for bioinformatics. J. Roy. Statis. Soc. 2001, 167, 194–195. [Google Scholar]
- Zhang, T.; Lv, W.; Zhang, H.; Ma, L.; Li, P.; Ge, L.; Li, G. Genome-wide analysis of the basic Helix-Loop-Helix (bHLH) transcription factor family in maize. BMC Plant Biol. 2018, 18, 235. [Google Scholar] [CrossRef] [PubMed]
- Zhao, P.; Wang, D.; Wang, R.; Kong, N.; Zhang, C.; Yang, C.; Wu, W.; Ma, H.; Chen, Q. Genome-wide analysis of the potato Hsp20 gene family: identification, genomic organization and expression profiles in response to heat stress. BMC Genom. 2018, 19, 61. [Google Scholar] [CrossRef] [PubMed]
- Qi, X.; Xie, S.; Liu, Y.; Yi, F.; Yu, J. Genome-wide annotation of genes and noncoding RNAs of foxtail millet in response to simulated drought stress by deep sequencing. Plant Mol. Biol. 2013, 83, 459–473. [Google Scholar] [CrossRef] [PubMed]
- Kaur, C.; Mustafiz, A.; Sarkar, A.K.; Ariyadasa, T.U.; Singla-Pareek, S.L.; Sopory, S. Expression of abiotic stress inducible ETHE1-like protein from rice is higher in roots and is regulated by calcium. Physiol. Plant. 2014, 152, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Rajsz, A.; Warzybok, A.; Migocka, M. Genes encoding cucumber full-size ABCG proteins show different responses to plant growth regulators and sclareolide. Plant Mol. Biol. Rep. 2016, 34, 720–736. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Wang, J.; Sun, Q.; Li, W.; Yu, Y.; Zhao, M.; Meng, Z. Expression analysis of genes encoding double B-box zinc finger proteins in maize. Funct. Integr. Genom. 2017, 17, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Gao, T.; Chen, J.; Yang, J.; Huang, H.; Yu, Y. The late embryogenesis abundant gene family in tea plant (Camellia sinensis): Genome-wide characterization and expression analysis in response to cold and dehydration stress. Plant Physiol. Biochem. 2019, 135, 277–286. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.; Xia, R.; Chen, H.; He, Y. TBtools, a Toolkit for Biologists integrating various HTS-data handling tools with a user-friendly interface. bioRxiv 2018, 289660. [Google Scholar]
- Blanc, G.; Wolfe, K.H. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant cell. 2004, 16, 1667–1678. [Google Scholar] [CrossRef] [PubMed]
- Zhang, M.; Shen, Z.; Meng, G.; Lu, Y.; Wang, Y. Genome-wide analysis of the Brachypodium distachyon (L.) P. Beauv. Hsp90 gene family reveals molecular evolution and expression profiling under drought and salt stresses. PLoS ONE 2017, 12, e0189187. [Google Scholar] [CrossRef] [PubMed]
- Liu, N.; Dong, L.; Deng, X.; Liu, D.; Liu, Y.; Li, M.; Hu, Y.; Yan, Y. Genome-wide identification, molecular evolution, and expression analysis of auxin response factor (ARF) gene family in Brachypodium distachyon L. BMC Plant Biol. 2018, 18, 336. [Google Scholar] [CrossRef] [PubMed]
- Lu, K.; Li, T.; He, J.; Chang, W.; Zhang, R.; Liu, M.; Yu, M.; Fan, Y.; Ma, J.; Sun, W.; et al. qPrimerDB: A thermodynamics-based gene-specific qPCR primer database for 147 organisms. Nucleic Acids Res. 2018, 46, 1229–1236. [Google Scholar] [CrossRef] [PubMed]
- Sang, J.; Wang, Z.; Li, M.; Cao, J.; Niu, G.; Xia, L.; Zou, D.; Wang, F.; Xu, X.; Han, X.; et al. ICG: a wiki-driven knowledgebase of internal control genes for RT-qPCR normalization. Nucleic Acids Res. 2018, 46, 121–126. [Google Scholar] [CrossRef] [PubMed]
- Gay, S.; Bugeon, J.; Bouchareb, A.; Henry, L.; Montfort, J.; Cam, A.L.; Bobe, J.; Thermes, V. MicroRNA-202 (miR-202) controls female fecundity by regulating medaka oogenesis. PLoS Genet. 2018, 14, e1007593. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) Method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
Name | Gene ID | Locus | Exon Number | Gene Length | CDS (bp) | No. of AA | pI | MW (kDa) | PSL |
---|---|---|---|---|---|---|---|---|---|
BdTPS1 | Bradi2g19640 | 17272345..17280887 | 17 | 7172 | 2958 | 985 | 6.09 | 109.37 | C,P,OM |
BdTPS2 | Bradi3g37200 | 39265879..39272239 | 3 | 3409 | 2463 | 820 | 6.04 | 91.24 | C,IM |
BdTPS3 | Bradi3g53790 | 54157803..54162799 | 3 | 3375 | 2556 | 851 | 6.47 | 94.76 | C,P,IM |
BdTPS4 | Bradi3g35820 | 37837473..37842899 | 3 | 2783 | 2589 | 862 | 6.06 | 97.71 | C |
BdTPS5 | Bradi2g19710 | 17341436..17346150 | 3 | 3783 | 2709 | 902 | 5.36 | 100.85 | C,OM |
BdTPS6 | Bradi2g49870 | 49645444..49650378 | 3 | 4238 | 2730 | 909 | 5.47 | 101.74 | C,OM |
BdTPS7 | Bradi4g41580 | 45574020..45578868 | 3 | 3755 | 2634 | 877 | 5.82 | 98.58 | C |
BdTPS8 | Bradi1g69420 | 68065706..68070557 | 3 | 3067 | 2604 | 867 | 5.99 | 97.75 | C |
BdTPS9 | Bradi4g29730 | 35237459..35242687 | 3 | 2823 | 2610 | 869 | 5.99 | 97.75 | C |
BdTPPA | Bradi3g32970 | 35087863..35092068 | 11 | 2203 | 1266 | 421 | 6.24 | 47.22 | P,C |
BdTPPB | Bradi1g27470 | 22586832..22591975 | 10 | 1874 | 1056 | 351 | 6.16 | 39.19 | C |
BdTPPC | Bradi3g50810 | 51669711..51673415 | 9 | 1900 | 1119 | 372 | 5.68 | 41.06 | P,C |
BdTPPD | Bradi5g17890 | 21178294..21180648 | 10 | 1999 | 1077 | 358 | 8.52 | 39.93 | P,C |
BdTPPE | Bradi3g35590 | 37622570..37625654 | 10 | 2300 | 1098 | 365 | 9.21 | 40.52 | P |
BdTPPF | Bradi4g29030 | 34348411..34350663 | 6 | 1793 | 1158 | 385 | 8.98 | 41.79 | P |
BdTPPG | Bradi3g58960 | 58022082..58025342 | 10 | 2243 | 1101 | 366 | 8.59 | 39.92 | P |
BdTPPH | Bradi1g60950 | 60533219..60535884 | 6 | 2071 | 1080 | 359 | 6.22 | 39.08 | C |
BdTPPI | Bradi1g45480 | 43862356..43865024 | 10 | 2266 | 1101 | 366 | 6.27 | 40.05 | C |
BdTPPJ | Bradi1g21420 | 17249655..17253046 | 9 | 2835 | 1062 | 353 | 5.64 | 38.58 | C |
Gene Pairs | Identity (%) | Ka | Ks | Ka/Ks | MYA |
---|---|---|---|---|---|
BdTPS5–BDTPS6 | 81.10 | 0.1108 | 0.8821 | 0.1256 | 67.85 |
BdTPPC–BdTPPD | 63.44 | 0.2185 | 1.0765 | 0.2030 | 82.80 |
BdTPPE–BdTPPF | 74.16 | 0.1278 | 0.4258 | 0.3000 | 32.75 |
BdTPPG–BdTPPI | 63.64 | 0.2354 | 0.5406 | 0.4354 | 41.58 |
BdTPPH–BdTPPJ | 63.66 | 0.2619 | 0.8726 | 0.3001 | 67.12 |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, S.; Ouyang, K.; Wang, K. Genome-Wide Identification, Evolution, and Expression Analysis of TPS and TPP Gene Families in Brachypodium distachyon. Plants 2019, 8, 362. https://doi.org/10.3390/plants8100362
Wang S, Ouyang K, Wang K. Genome-Wide Identification, Evolution, and Expression Analysis of TPS and TPP Gene Families in Brachypodium distachyon. Plants. 2019; 8(10):362. https://doi.org/10.3390/plants8100362
Chicago/Turabian StyleWang, Song, Kai Ouyang, and Kai Wang. 2019. "Genome-Wide Identification, Evolution, and Expression Analysis of TPS and TPP Gene Families in Brachypodium distachyon" Plants 8, no. 10: 362. https://doi.org/10.3390/plants8100362