Research Article
BibTex RIS Cite

Genome-wide Analysis and Characterization of Eucalyptus grandis TCP Transcription Factors

Year 2023, Volume: 29 Issue: 2, 413 - 426, 31.03.2023
https://doi.org/10.15832/ankutbd.1104949

Abstract

Teosinte branched/Cycloidea/Proliferating cell factors (TCPs), a small transcription gene family, serve in developmental processes such as branching, flowering, and growth of plants. In this study, the TCP transcription gene family of eucalyptus, which is considered important for its medicinal and industrial uses, was bioinformatically investigated. A total of 16 Eucalyptus grandis TCP (Egra-TCP) genes were found to be distributed on chromosomes 1, 2, 4, 6, 7, 9, 10 and 11. Several segmentally-duplicated gene couples including Egra-TCP-7/Egra-TCP-11, -13 and -16, Egra-TCP-6/Egra-TCP-12 and -15, Egra-TCP-12/Egra-TCP-15 and Egra-TCP-11/Egra-TCP-13 were discovered. Egra-TCPs were divided into three main clades based on phylogenetic analysis, motif, and gene structure. While Egra-TCP-10 has the highest molecular weight with 47.19 kDa, the lowest was Egra-TCP-1 with 21.68 kDa. Twelve Egra-TCP genes were found to have no introns, while the Egra-TCP-7, -15, and -16 genes had a single intron. The orthologous relationships among E. grandis/Arabidopsis thaliana and E. grandis/Vitis vinifera were identified through a synteny analysis. Digital gene expression profiles of Egra-TCP genes in tissues such as xylem, phloem, shoot tips, young and mature leaf revealed a high expression pattern. The findings of this study contributes to existing knowledge in the biotechnology field by providing contributing to our understanding of the molecular basis of the TCP gene family in the eucalyptus plant.

Thanks

This study was presented at the International Conference on Food, Agriculture and Animal Sciences (ICOFAAS 2018) and published in the Abstract Book as an abstract.

References

  • Aguilar-Martinez J A & Sinha N (2013). Analysis of the role of Arabidopsis class I TCP genes AtTCP7, AtTCP8, AtTCP22, and AtTCP23 in leaf development. Front Plant Sci 4:406. doi.org/10.3389/fpls.2013.00406
  • Aygören A S, Muslu S, Isıyel M, Öner B M, Kasapoğlu A G, Aydınyurt R, Yaprak E, Uçar S, İlhan E & Aydın M (2022). Genome-Wide Analysis and Characterization of the VPE Gene Family under Salt and Drought Stress in Common Bean Genotypes. European Journal of Science and Technology, Ejosat Special Issue 2022 (ICAENS) 553-560. doi.org/10.31590/ejosat.1083440
  • Bailey T L, Williams N, Misleh C & Li W W (2006). MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research 34: W369-W373. doi.org/10.1093/nar/gkl198
  • Cao P B, Le T, Chu H D, Le L, L, T, Aza, S, La V, Tran T & Vu X (2021). Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods. Asian Journal of Plant Sciences 20(2): 210-219. doi.org/10.3923/ajps.2021.210.219
  • Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y & Xia R (2020). TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol Plant 13(8): 1194-1202. doi.org/10.1016/j.molp.2020.06.009
  • Chen L, Chen Y Q, Ding A M, Chen H, Xia F, Wang W F & Sun Y H (2016). Genome-wide analysis of TCP family in tobacco. Genet Mol Res 15(2): doi.org/10.4238/gmr.15027728.
  • Citerne H L, Le Guilloux M, Sannier J, Nadot S & Damerval C (2013). Combining Phylogenetic and Syntenic Analyses for Understanding the Evolution of TCP ECE Genes in Eudicots. PLoS One 8(9): e74803. doi.org/10.1371/journal.pone.0074803
  • Crooks G E, Hon G, Chandonia J M & Brenner S E (2004). WebLogo: A sequence logo generator. Genome Res 14(6): 1188-1190. doi.org/10.1101/gr.849004
  • Danisman S, van der Wal F, Dhondt S, Waites R, de Folter S, Bimbo A, van Dijk A D, Muino J M, Cutri L, Dornelas M C, Angenent G C & Immink R G H (2012). Arabidopsis Class I and Class II TCP Transcription Factors Regulate Jasmonic Acid Metabolism and Leaf Development Antagonistically. Plant Physiol 159(4): 1511-1523. doi.org/10.1104/pp.112.200303
  • Ding S, Cai Z, Du H & Wang H (2019). Genome-Wide Analysis of TCP Family Genes in Zea mays L. Identified a Role for ZmTCP42 in Drought Tolerance. Int J Mol Sci 20(11): 2762. doi.org/10.3390/ijms20112762
  • Doebley J, Stec A & Hubbard L (1997). The evolution of apical dominance in maize. Nature 386(6624): 485-488. doi.org/10.1038/386485a0
  • Feng K, Hao J N, Liu J X, Huang W, Wang G L, Xu Z S, Huang Y & Xiong A S (2019). Genome-wide identification, classification, and expression analysis of TCP transcription factors in carrot. Canadian Journal of Plant Science 99(4): 525-535. doi.org/10.1139/cjps-2018-0232
  • Feng Z J, Xu S C, Liu N, Zhang G W, Hu Q Z & Gong Y M (2018). Soybean TCP transcription factors: Evolution, classification, protein interaction and stress and hormone responsiveness. Plant Physiol Biochem 127: 129-142. doi.org/10.1016/j.plaphy.2018.03.020
  • Francis A, Dhaka N, Bakshi M, Jung K H, Sharma M K & Sharma R (2016). Comparative phylogenomic analysis provides insights into TCP gene functions in Sorghum. Sci Rep 6:38488. Erratum in: Sci Rep 2017;7:45801. doi.org/10.1038/srep38488
  • He J, He X, Chang P, Jiang H, Gong D & Sun Q (2020). Genome-wide identification and characterization of TCP family genes in Brassica juncea var. tumida. PeerJ 8: e9130. doi.org/10.7717/peerj.9130
  • Horton P, Park K J, Obayashi T, Fujita N, Harada H, Adams-Collier C J & Nakai K (2007). WoLF PSORT: protein localization predictor. Nucleic Acids Res 35: W585-W587. doi.org/10.1093/nar/gkm259
  • Hu B, Jin J, Guo A Y, Zhang H, Luo J C & Gao G (2015). GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8): 1296-1297. doi.org/10.1093/bioinformatics/btu817
  • Huo, N, Zhang S, Zhu T, Dong L, Wang Y, Mohr T, Hu T, Liu Z, Dvorak J, Luo M C, Wang D, Lee J Y,Altenbach S & Gu Y Q (2018). Gene duplication and evolution dynamics in the homeologous regions harboring multiple prolamin and resistance gene families in hexaploid wheat. Front Plant Sci 9: 673. doi.org/10.3389/fpls.2018.00673
  • İlhan E (2018). Genome-wide analysis of Eucalyptus grandis YABBY transcription factors. Turkish Journal of Agricultural Research 5(2): 158-166. doi.org/10.19159/tutad.408654
  • Ilhan E, Buyuk I & Inal B (2018). Transcriptome - Scale characterization of salt responsive bean TCP transcription factors. Gene 642: 64-73. doi.org/10.1016/j.gene.2017.11.021
  • Jaillon O, Aury J M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pè M E, Valle G, Morgante M, Caboche M, Adam-Blondon A F, Weissenbach J, Quétier F, Wincker P (2007). The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161): 463-467. doi.org/10.1038/nature06148
  • Jiu S, Xu Y, Wang J, Wang L, Wang S, Ma C, Guan L, Abdullah M, Zhao M, Xu W, Ma W & Zhang C (2019). Genome-Wide Identification, Characterization, and Transcript Analysis of the TCP Transcription Factors in Vitis vinifera. Front Genet 10. doi.org/10.3389/fgene.2019.01276
  • Juretic N, Hoen D R, Huynh M L, Harrison P M & Bureau T E (2005). The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15(9): 1292-1297. doi.org/10.1101/gr.4064205
  • Kasapoğlu A G, İlhan E, Kızılkaya D, Hossein-Pour A & Haliloğlu K (2020). Genome-Wide Analysis of BES1 Transcription Factor Family in Sorghum [Sorghum bicolor (L.) Moench] Genome. Turkish Journal of Agricultural Research 7(1): 85-95. doi.org/10.19159/tutad.671605
  • Kizilkaya D, Kasapoğlu A G, Hossein-pour A, Haliloğlu K, Muslu S & Ilhan E (2020). Genome wide analysis of Sorghum bicolor L. CAMTA transcription factors. Atatürk University Journal of Agricultural Faculty 51(3): 267-278. doi.org/10.17097/ataunizfd.690138
  • Kondrashov F A, Rogozin I B, Wolf Y I & Koonin E V (2002). Selection in the evolution of gene duplications. Genome Biology 3(2): RESEARCH0008. doi.org/10.1186/gb-2002-3-2-research0008
  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones S J & Marra M A (2009). Circos: An information aesthetic for comparative genomics. Genome Research 19(9): 1639-1645. doi.org/10.1101/gr.092759.109
  • Kumar S, Stecher G & Tamura K (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33(7): 1870-1874. doi.org/10.1093/molbev/msw054
  • Lamesch P, Berardini T Z, Li D H, Swarbreck D, Wilk, C, Sasidharan R, Muller R, Dreher K, Alexander D L, Garcia-Hernandez M, Karthikeyan A S, Lee C H, Nelson W D, Ploetz L, Singh S, Wensel A & Huala E (2012). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Research 40(D1): D1202-D1210. doi.org/10.1093/nar/gkr1090
  • Leng X, Wei H, Xu X, Ghuge SA, Jia D, Liu G, Wang Y & Yuan Y (2019). Genome-wide identification and transcript analysis of TCP transcription factors in grapevine. Bmc Genomics 20(1): 786. doi.org/10.1186/s12864-019-6159-2
  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P & Rombauts S (2002). PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30(1): 325-327. doi.org/10.1093/nar/30.1.325
  • Letunic I & Bork P (2011). Interactive Tree of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39: W475-W478. doi.org/10.1093/nar/gkr201
  • Li C, Potuschak T, Colón-Carmona A, Gutiérrez RA & Doerner P (2005). Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci U S A 102(36): 12978-12983. doi.org/10.1073/pnas.0504039102
  • Li S (2015). The Arabidopsis thaliana TCP transcription factors: a broadening horizon beyond development. Plant Signal Behav 10(7): e1044192. doi.org/10.1080/15592324.2015.1044192
  • Lin J S, Zhu M T, Cai M X, Zhang W P, Fatima M, Jia H F, Li F F & Ming R (2019). Identification and Expression Analysis of TCP Genes in Saccharum spontaneum L. Tropical Plant Biology 12(3): 206-218. doi.org/10.1007/s12042-019-09238-y
  • Ling L, Zhang W R, An Y M, Du B H, Wang D & Guo C H (2020). Genome-wide analysis of the TCP transcription factor genes in five legume genomes and their response to salt and drought stresses. Functional & Integrative Genomics 20(4): 537-550. doi.org/10.1007/s10142-020-00733-0
  • Liu Y, Guan X, Liu S, Yang M, Ren J, Guo M, Huang Z & Zhang Y (2018). Genome-Wide Identification and Analysis of TCP Transcription Factors Involved in the Formation of Leafy Head in Chinese Cabbage. International Journal of Molecular Sciences 19(3): 847. doi.org/10.3390/ijms19030847
  • Macphail M & Thornhill A H (2016). How old are the eucalypts? A review of the microfossil and phylogenetic evidence. Australian Journal of Botany 64(8): 579-599.
  • Makeyev A V, Chkheidze A N & Liebhaber S A (1999). A set of highly conserved RNA-binding proteins, αCP-1 and αCP-2, implicated in mRNA stabilization, are coexpressed from an intronless gene and its intron-containing paralog. J Biol Chem 274(35): 24849-24857. doi.org/10.1074/jbc.274.35.24849
  • Makova K D & Li W H (2003). Divergence in the spatial pattern of gene expression between human duplicate genes. Genome Res 13(7): 1638-1645. doi.org/10.1101/gr.1133803
  • Martin-Trillo M & Cubas P (2010). TCP genes: a family snapshot ten years later. Trends Plant Sci 15(1): 31-39. doi.org/10.1016/j.tplants.2009.11.003
  • Min Z, Zhang Y, Li R, Liu M, Ju Y, Fang Y & Meng J (2018). Genome-wide Analysis and Expression Profiling Suggest Diverse Roles of TCP Genes During Development and Stress Responses in Grapevine (Vitis vinifera L). South African Journal of Enology and Viticulture 39(2): 216-226. doi.org/10.21548/39-2-2769
  • Mondragon-Palomino M & Trontin C (2011). High time for a roll call: gene duplication and phylogenetic relationships of TCP-like genes in monocots. Ann Bot 107(9): 1533-1544. doi.org/10.1093/aob/mcr059
  • Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, Jenkins J, Lindquist E, Tice H, Bauer D, Goodstein DM, Dubchak I, Poliakov A, Mizrachi E, Kullan AR, Hussey SG, Pinard D, van der Merwe K, Singh P, van Jaarsveld I, Silva-Junior OB, Togawa RC, Pappas MR, Faria DA, Sansaloni CP, Petroli CD, Yang X, Ranjan P, Tschaplinski TJ, Ye CY, Li T, Sterck L, Vanneste K, Murat F, Soler M, Clemente HS, Saidi N, Cassan-Wang H, Dunand C, Hefer CA, Bornberg-Bauer E, Kersting AR, Vining K, Amarasinghe V, Ranik M, Naithani S, Elser J, Boyd AE, Liston A, Spatafora JW, Dharmwardhana P, Raja R, Sullivan C, Romanel E, Alves-Ferreira M, Külheim C, Foley W, Carocha V, Paiva J, Kudrna D, Brommonschenkel SH, Pasquali G, Byrne M, Rigault P, Tibbits J, Spokevicius A, Jones RC, Steane DA, Vaillancourt RE, Potts BM, Joubert F, Barry K, Pappas GJ, Strauss SH, Jaiswal P, Grima-Pettenati J, Salse J, Van de Peer Y, Rokhsar DS & Schmutz J (2014). The genome of Eucalyptus grandis. Nature 510(7505): 356-362. doi.org/10.1038/nature13308
  • Nag A, King S & Jack T (2009). miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci U S A 106(52): 22534-22539. doi.org/10.1073/pnas.0908718106
  • Navaud O, Dabos P, Carnus E, Tremousaygue D & Hervé C (2007). TCP transcription factors predate the emergence of land plants. J Mol Evol 65(1): 23-33. doi.org/10.1007/s00239-006-0174-z
  • Palatnik J F, Allen E, Wu X L, Schommer C, Schwab R, Carrington J C & Weigel D (2003). Control of leaf morphogenesis by microRNAs. Nature 425(6955): 257-263. doi.org/10.1038/nature01958
  • Parapunova V, Busscher M, Busscher-Lange J, Lammers M, Karlova R, Bovy A G, Angenent G C & de Maagd R A (2014). Identification, cloning and characterization of the tomato TCP transcription factor family. Bmc Plant Biology 14: 157. doi.org/10.1186/1471-2229-14-157
  • Pestana-Calsa MC, Pacheco CM, de Castro RC, de Almeida RR, de Lira NP & Junior TC (2012). Cell wall, lignin and fatty acid-related transcriptome in soybean: Achieving gene expression patterns for bioenergy legume. Genet Mol Biol 35(1): 322-330. doi.org/10.1590/S1415-47572012000200013
  • Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R & Lopez R (2005). InterProScan: protein domains identifier. Nucleic Acids Res 33: W116-W120. doi.org/10.1093/nar/gki442
  • Sugiyama A, Noguchi K, Kitanaka C, Katou N, Tashiro F, Ono T & Kuchino Y (1999). Molecular cloning and chromosomal mapping of mouse intronless myc gene acting as a potent apoptosis inducer. Gene 226(2); 273-283. doi.org/10.1016/S0378-1119(98)00547-2
  • Thompson J D, Gibson T J, Plewniak F, Jeanmougin F & Higgins D G (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24): 4876-4882. doi.org/10.1093/nar/25.24.4876
  • Trapnell C, Hendrickson D G, Sauvageau M, Goff L, Rinn J L & Pachter L (2013). Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31(1): 46-53. doi.org/10.1038/nbt.2450
  • Wang H, Wang H, Liu R, Xu Y, Lu Z & Zhou C (2018). Genome-Wide Identification of TCP Family Transcription Factors in Medicago truncatula Reveals Significant Roles of miR319-Targeted TCPs in Nodule Development. Front Plant Sci 9: 774. doi.org/10.3389/fpls.2018.00774
  • Wang Y, Tang H, Debarry J D, Tan X, Li J, Wang X, Lee T H, Jin H, Marler B, Guo H, Kissinger J C & Paterson A H (2012). MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40(7): e49. doi.org/10.1093/nar/gkr1293
  • Xu R, Sun P, Jia F, Lu L, Li Y, Zhang S & Huang J (2014). Genomewide analysis of TCP transcription factor gene family in Malus domestica. J Genet 93(3): 733-746. doi.org/10.1007/s12041-014-0446-0
  • Yang X, Jawdy S, Tschaplinski T J, & Tuskan G A (2009). Genome-wide identification of lineage-specific genes in Arabidopsis, Oryza and Populus. Genomics 93(5); 473-480. doi.org/10.1016/j.ygeno.2009.01.002
  • Yao X, Ma H, Wang J & Zhang D B (2007). Genome-wide comparative analysis and expression pattern of TCP gene families in Arabidopsis, thaliana and Oryza sativa. Journal of Integrative Plant Biology 49(6): 885-897. doi.org/10.1111/j.1744-7909.2007.00509.x
  • Zhang Y, Wu Y, Liu Y, & Han B (2005). Computational identification of 69 retroposons in Arabidopsis. Plant Physiol 138(2); 935-948. doi.org/10.1104/pp.105.060244
  • Zhao J, Zhai Z, Li Y, Geng S, Song G, Guan J, Jia M, Wang F, Sun G, Feng N, Kong X, Chen L, Mao L & Li A (2018). Genome-Wide Identification and Expression Profiling of the TCP Family Genes in Spike and Grain Development of Wheat (Triticum aestivum L.). Front Plant Sci 9: 1282. doi.org/10.3389/fpls.2018.01282
  • Zheng K, Ni Z, Qu Y, Cai Y, Yang Z, Sun G & Chen Q (2018). Genome-wide identification and expression analyses of TCP transcription factor genes in Gossypium barbadense. Sci Rep 8(1): 14526. doi.org/10.1038/s41598-018-32626-5
  • Zhou Y, Xu Z, Zhao K, Yang W, Cheng T, Wang J & Zhang Q (2016). Genome-Wide Identification, Characterization and Expression Analysis of the TCP Gene Family in Prunus mume. Front Plant Sci 7: 1301. doi.org/10.3389/fpls.2016.01301
Year 2023, Volume: 29 Issue: 2, 413 - 426, 31.03.2023
https://doi.org/10.15832/ankutbd.1104949

Abstract

References

  • Aguilar-Martinez J A & Sinha N (2013). Analysis of the role of Arabidopsis class I TCP genes AtTCP7, AtTCP8, AtTCP22, and AtTCP23 in leaf development. Front Plant Sci 4:406. doi.org/10.3389/fpls.2013.00406
  • Aygören A S, Muslu S, Isıyel M, Öner B M, Kasapoğlu A G, Aydınyurt R, Yaprak E, Uçar S, İlhan E & Aydın M (2022). Genome-Wide Analysis and Characterization of the VPE Gene Family under Salt and Drought Stress in Common Bean Genotypes. European Journal of Science and Technology, Ejosat Special Issue 2022 (ICAENS) 553-560. doi.org/10.31590/ejosat.1083440
  • Bailey T L, Williams N, Misleh C & Li W W (2006). MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research 34: W369-W373. doi.org/10.1093/nar/gkl198
  • Cao P B, Le T, Chu H D, Le L, L, T, Aza, S, La V, Tran T & Vu X (2021). Genome-wide Analysis of Aldehyde Dehydrogenase (ALDH) Gene Superfamily in Eucalyptus grandis by Using Bioinformatics Methods. Asian Journal of Plant Sciences 20(2): 210-219. doi.org/10.3923/ajps.2021.210.219
  • Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y & Xia R (2020). TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol Plant 13(8): 1194-1202. doi.org/10.1016/j.molp.2020.06.009
  • Chen L, Chen Y Q, Ding A M, Chen H, Xia F, Wang W F & Sun Y H (2016). Genome-wide analysis of TCP family in tobacco. Genet Mol Res 15(2): doi.org/10.4238/gmr.15027728.
  • Citerne H L, Le Guilloux M, Sannier J, Nadot S & Damerval C (2013). Combining Phylogenetic and Syntenic Analyses for Understanding the Evolution of TCP ECE Genes in Eudicots. PLoS One 8(9): e74803. doi.org/10.1371/journal.pone.0074803
  • Crooks G E, Hon G, Chandonia J M & Brenner S E (2004). WebLogo: A sequence logo generator. Genome Res 14(6): 1188-1190. doi.org/10.1101/gr.849004
  • Danisman S, van der Wal F, Dhondt S, Waites R, de Folter S, Bimbo A, van Dijk A D, Muino J M, Cutri L, Dornelas M C, Angenent G C & Immink R G H (2012). Arabidopsis Class I and Class II TCP Transcription Factors Regulate Jasmonic Acid Metabolism and Leaf Development Antagonistically. Plant Physiol 159(4): 1511-1523. doi.org/10.1104/pp.112.200303
  • Ding S, Cai Z, Du H & Wang H (2019). Genome-Wide Analysis of TCP Family Genes in Zea mays L. Identified a Role for ZmTCP42 in Drought Tolerance. Int J Mol Sci 20(11): 2762. doi.org/10.3390/ijms20112762
  • Doebley J, Stec A & Hubbard L (1997). The evolution of apical dominance in maize. Nature 386(6624): 485-488. doi.org/10.1038/386485a0
  • Feng K, Hao J N, Liu J X, Huang W, Wang G L, Xu Z S, Huang Y & Xiong A S (2019). Genome-wide identification, classification, and expression analysis of TCP transcription factors in carrot. Canadian Journal of Plant Science 99(4): 525-535. doi.org/10.1139/cjps-2018-0232
  • Feng Z J, Xu S C, Liu N, Zhang G W, Hu Q Z & Gong Y M (2018). Soybean TCP transcription factors: Evolution, classification, protein interaction and stress and hormone responsiveness. Plant Physiol Biochem 127: 129-142. doi.org/10.1016/j.plaphy.2018.03.020
  • Francis A, Dhaka N, Bakshi M, Jung K H, Sharma M K & Sharma R (2016). Comparative phylogenomic analysis provides insights into TCP gene functions in Sorghum. Sci Rep 6:38488. Erratum in: Sci Rep 2017;7:45801. doi.org/10.1038/srep38488
  • He J, He X, Chang P, Jiang H, Gong D & Sun Q (2020). Genome-wide identification and characterization of TCP family genes in Brassica juncea var. tumida. PeerJ 8: e9130. doi.org/10.7717/peerj.9130
  • Horton P, Park K J, Obayashi T, Fujita N, Harada H, Adams-Collier C J & Nakai K (2007). WoLF PSORT: protein localization predictor. Nucleic Acids Res 35: W585-W587. doi.org/10.1093/nar/gkm259
  • Hu B, Jin J, Guo A Y, Zhang H, Luo J C & Gao G (2015). GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8): 1296-1297. doi.org/10.1093/bioinformatics/btu817
  • Huo, N, Zhang S, Zhu T, Dong L, Wang Y, Mohr T, Hu T, Liu Z, Dvorak J, Luo M C, Wang D, Lee J Y,Altenbach S & Gu Y Q (2018). Gene duplication and evolution dynamics in the homeologous regions harboring multiple prolamin and resistance gene families in hexaploid wheat. Front Plant Sci 9: 673. doi.org/10.3389/fpls.2018.00673
  • İlhan E (2018). Genome-wide analysis of Eucalyptus grandis YABBY transcription factors. Turkish Journal of Agricultural Research 5(2): 158-166. doi.org/10.19159/tutad.408654
  • Ilhan E, Buyuk I & Inal B (2018). Transcriptome - Scale characterization of salt responsive bean TCP transcription factors. Gene 642: 64-73. doi.org/10.1016/j.gene.2017.11.021
  • Jaillon O, Aury J M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pè M E, Valle G, Morgante M, Caboche M, Adam-Blondon A F, Weissenbach J, Quétier F, Wincker P (2007). The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161): 463-467. doi.org/10.1038/nature06148
  • Jiu S, Xu Y, Wang J, Wang L, Wang S, Ma C, Guan L, Abdullah M, Zhao M, Xu W, Ma W & Zhang C (2019). Genome-Wide Identification, Characterization, and Transcript Analysis of the TCP Transcription Factors in Vitis vinifera. Front Genet 10. doi.org/10.3389/fgene.2019.01276
  • Juretic N, Hoen D R, Huynh M L, Harrison P M & Bureau T E (2005). The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15(9): 1292-1297. doi.org/10.1101/gr.4064205
  • Kasapoğlu A G, İlhan E, Kızılkaya D, Hossein-Pour A & Haliloğlu K (2020). Genome-Wide Analysis of BES1 Transcription Factor Family in Sorghum [Sorghum bicolor (L.) Moench] Genome. Turkish Journal of Agricultural Research 7(1): 85-95. doi.org/10.19159/tutad.671605
  • Kizilkaya D, Kasapoğlu A G, Hossein-pour A, Haliloğlu K, Muslu S & Ilhan E (2020). Genome wide analysis of Sorghum bicolor L. CAMTA transcription factors. Atatürk University Journal of Agricultural Faculty 51(3): 267-278. doi.org/10.17097/ataunizfd.690138
  • Kondrashov F A, Rogozin I B, Wolf Y I & Koonin E V (2002). Selection in the evolution of gene duplications. Genome Biology 3(2): RESEARCH0008. doi.org/10.1186/gb-2002-3-2-research0008
  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones S J & Marra M A (2009). Circos: An information aesthetic for comparative genomics. Genome Research 19(9): 1639-1645. doi.org/10.1101/gr.092759.109
  • Kumar S, Stecher G & Tamura K (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33(7): 1870-1874. doi.org/10.1093/molbev/msw054
  • Lamesch P, Berardini T Z, Li D H, Swarbreck D, Wilk, C, Sasidharan R, Muller R, Dreher K, Alexander D L, Garcia-Hernandez M, Karthikeyan A S, Lee C H, Nelson W D, Ploetz L, Singh S, Wensel A & Huala E (2012). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Research 40(D1): D1202-D1210. doi.org/10.1093/nar/gkr1090
  • Leng X, Wei H, Xu X, Ghuge SA, Jia D, Liu G, Wang Y & Yuan Y (2019). Genome-wide identification and transcript analysis of TCP transcription factors in grapevine. Bmc Genomics 20(1): 786. doi.org/10.1186/s12864-019-6159-2
  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P & Rombauts S (2002). PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30(1): 325-327. doi.org/10.1093/nar/30.1.325
  • Letunic I & Bork P (2011). Interactive Tree of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39: W475-W478. doi.org/10.1093/nar/gkr201
  • Li C, Potuschak T, Colón-Carmona A, Gutiérrez RA & Doerner P (2005). Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci U S A 102(36): 12978-12983. doi.org/10.1073/pnas.0504039102
  • Li S (2015). The Arabidopsis thaliana TCP transcription factors: a broadening horizon beyond development. Plant Signal Behav 10(7): e1044192. doi.org/10.1080/15592324.2015.1044192
  • Lin J S, Zhu M T, Cai M X, Zhang W P, Fatima M, Jia H F, Li F F & Ming R (2019). Identification and Expression Analysis of TCP Genes in Saccharum spontaneum L. Tropical Plant Biology 12(3): 206-218. doi.org/10.1007/s12042-019-09238-y
  • Ling L, Zhang W R, An Y M, Du B H, Wang D & Guo C H (2020). Genome-wide analysis of the TCP transcription factor genes in five legume genomes and their response to salt and drought stresses. Functional & Integrative Genomics 20(4): 537-550. doi.org/10.1007/s10142-020-00733-0
  • Liu Y, Guan X, Liu S, Yang M, Ren J, Guo M, Huang Z & Zhang Y (2018). Genome-Wide Identification and Analysis of TCP Transcription Factors Involved in the Formation of Leafy Head in Chinese Cabbage. International Journal of Molecular Sciences 19(3): 847. doi.org/10.3390/ijms19030847
  • Macphail M & Thornhill A H (2016). How old are the eucalypts? A review of the microfossil and phylogenetic evidence. Australian Journal of Botany 64(8): 579-599.
  • Makeyev A V, Chkheidze A N & Liebhaber S A (1999). A set of highly conserved RNA-binding proteins, αCP-1 and αCP-2, implicated in mRNA stabilization, are coexpressed from an intronless gene and its intron-containing paralog. J Biol Chem 274(35): 24849-24857. doi.org/10.1074/jbc.274.35.24849
  • Makova K D & Li W H (2003). Divergence in the spatial pattern of gene expression between human duplicate genes. Genome Res 13(7): 1638-1645. doi.org/10.1101/gr.1133803
  • Martin-Trillo M & Cubas P (2010). TCP genes: a family snapshot ten years later. Trends Plant Sci 15(1): 31-39. doi.org/10.1016/j.tplants.2009.11.003
  • Min Z, Zhang Y, Li R, Liu M, Ju Y, Fang Y & Meng J (2018). Genome-wide Analysis and Expression Profiling Suggest Diverse Roles of TCP Genes During Development and Stress Responses in Grapevine (Vitis vinifera L). South African Journal of Enology and Viticulture 39(2): 216-226. doi.org/10.21548/39-2-2769
  • Mondragon-Palomino M & Trontin C (2011). High time for a roll call: gene duplication and phylogenetic relationships of TCP-like genes in monocots. Ann Bot 107(9): 1533-1544. doi.org/10.1093/aob/mcr059
  • Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, Jenkins J, Lindquist E, Tice H, Bauer D, Goodstein DM, Dubchak I, Poliakov A, Mizrachi E, Kullan AR, Hussey SG, Pinard D, van der Merwe K, Singh P, van Jaarsveld I, Silva-Junior OB, Togawa RC, Pappas MR, Faria DA, Sansaloni CP, Petroli CD, Yang X, Ranjan P, Tschaplinski TJ, Ye CY, Li T, Sterck L, Vanneste K, Murat F, Soler M, Clemente HS, Saidi N, Cassan-Wang H, Dunand C, Hefer CA, Bornberg-Bauer E, Kersting AR, Vining K, Amarasinghe V, Ranik M, Naithani S, Elser J, Boyd AE, Liston A, Spatafora JW, Dharmwardhana P, Raja R, Sullivan C, Romanel E, Alves-Ferreira M, Külheim C, Foley W, Carocha V, Paiva J, Kudrna D, Brommonschenkel SH, Pasquali G, Byrne M, Rigault P, Tibbits J, Spokevicius A, Jones RC, Steane DA, Vaillancourt RE, Potts BM, Joubert F, Barry K, Pappas GJ, Strauss SH, Jaiswal P, Grima-Pettenati J, Salse J, Van de Peer Y, Rokhsar DS & Schmutz J (2014). The genome of Eucalyptus grandis. Nature 510(7505): 356-362. doi.org/10.1038/nature13308
  • Nag A, King S & Jack T (2009). miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci U S A 106(52): 22534-22539. doi.org/10.1073/pnas.0908718106
  • Navaud O, Dabos P, Carnus E, Tremousaygue D & Hervé C (2007). TCP transcription factors predate the emergence of land plants. J Mol Evol 65(1): 23-33. doi.org/10.1007/s00239-006-0174-z
  • Palatnik J F, Allen E, Wu X L, Schommer C, Schwab R, Carrington J C & Weigel D (2003). Control of leaf morphogenesis by microRNAs. Nature 425(6955): 257-263. doi.org/10.1038/nature01958
  • Parapunova V, Busscher M, Busscher-Lange J, Lammers M, Karlova R, Bovy A G, Angenent G C & de Maagd R A (2014). Identification, cloning and characterization of the tomato TCP transcription factor family. Bmc Plant Biology 14: 157. doi.org/10.1186/1471-2229-14-157
  • Pestana-Calsa MC, Pacheco CM, de Castro RC, de Almeida RR, de Lira NP & Junior TC (2012). Cell wall, lignin and fatty acid-related transcriptome in soybean: Achieving gene expression patterns for bioenergy legume. Genet Mol Biol 35(1): 322-330. doi.org/10.1590/S1415-47572012000200013
  • Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R & Lopez R (2005). InterProScan: protein domains identifier. Nucleic Acids Res 33: W116-W120. doi.org/10.1093/nar/gki442
  • Sugiyama A, Noguchi K, Kitanaka C, Katou N, Tashiro F, Ono T & Kuchino Y (1999). Molecular cloning and chromosomal mapping of mouse intronless myc gene acting as a potent apoptosis inducer. Gene 226(2); 273-283. doi.org/10.1016/S0378-1119(98)00547-2
  • Thompson J D, Gibson T J, Plewniak F, Jeanmougin F & Higgins D G (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24): 4876-4882. doi.org/10.1093/nar/25.24.4876
  • Trapnell C, Hendrickson D G, Sauvageau M, Goff L, Rinn J L & Pachter L (2013). Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31(1): 46-53. doi.org/10.1038/nbt.2450
  • Wang H, Wang H, Liu R, Xu Y, Lu Z & Zhou C (2018). Genome-Wide Identification of TCP Family Transcription Factors in Medicago truncatula Reveals Significant Roles of miR319-Targeted TCPs in Nodule Development. Front Plant Sci 9: 774. doi.org/10.3389/fpls.2018.00774
  • Wang Y, Tang H, Debarry J D, Tan X, Li J, Wang X, Lee T H, Jin H, Marler B, Guo H, Kissinger J C & Paterson A H (2012). MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40(7): e49. doi.org/10.1093/nar/gkr1293
  • Xu R, Sun P, Jia F, Lu L, Li Y, Zhang S & Huang J (2014). Genomewide analysis of TCP transcription factor gene family in Malus domestica. J Genet 93(3): 733-746. doi.org/10.1007/s12041-014-0446-0
  • Yang X, Jawdy S, Tschaplinski T J, & Tuskan G A (2009). Genome-wide identification of lineage-specific genes in Arabidopsis, Oryza and Populus. Genomics 93(5); 473-480. doi.org/10.1016/j.ygeno.2009.01.002
  • Yao X, Ma H, Wang J & Zhang D B (2007). Genome-wide comparative analysis and expression pattern of TCP gene families in Arabidopsis, thaliana and Oryza sativa. Journal of Integrative Plant Biology 49(6): 885-897. doi.org/10.1111/j.1744-7909.2007.00509.x
  • Zhang Y, Wu Y, Liu Y, & Han B (2005). Computational identification of 69 retroposons in Arabidopsis. Plant Physiol 138(2); 935-948. doi.org/10.1104/pp.105.060244
  • Zhao J, Zhai Z, Li Y, Geng S, Song G, Guan J, Jia M, Wang F, Sun G, Feng N, Kong X, Chen L, Mao L & Li A (2018). Genome-Wide Identification and Expression Profiling of the TCP Family Genes in Spike and Grain Development of Wheat (Triticum aestivum L.). Front Plant Sci 9: 1282. doi.org/10.3389/fpls.2018.01282
  • Zheng K, Ni Z, Qu Y, Cai Y, Yang Z, Sun G & Chen Q (2018). Genome-wide identification and expression analyses of TCP transcription factor genes in Gossypium barbadense. Sci Rep 8(1): 14526. doi.org/10.1038/s41598-018-32626-5
  • Zhou Y, Xu Z, Zhao K, Yang W, Cheng T, Wang J & Zhang Q (2016). Genome-Wide Identification, Characterization and Expression Analysis of the TCP Gene Family in Prunus mume. Front Plant Sci 7: 1301. doi.org/10.3389/fpls.2016.01301
There are 62 citations in total.

Details

Primary Language English
Journal Section Research Article
Authors

Emre İlhan 0000-0002-8404-7900

Ayşe Gül Kasapoğlu 0000-0002-6447-4921

Selman Muslu 0000-0003-4777-0726

Ahmed Sidar Aygören 0000-0002-6264-9935

Murat Aydın 0000-0003-1091-0609

Publication Date March 31, 2023
Submission Date April 24, 2022
Acceptance Date August 17, 2022
Published in Issue Year 2023 Volume: 29 Issue: 2

Cite

APA İlhan, E., Kasapoğlu, A. G., Muslu, S., Aygören, A. S., et al. (2023). Genome-wide Analysis and Characterization of Eucalyptus grandis TCP Transcription Factors. Journal of Agricultural Sciences, 29(2), 413-426. https://doi.org/10.15832/ankutbd.1104949

Journal of Agricultural Sciences is published open access journal. All articles are published under the terms of the Creative Commons Attribution License (CC BY).