Transcriptome-wide Profiling of the TCP Gene Family in Lagerstroemia indica
ZHANG Ye, LIU Jie-Ru, FENG Lu, ZHOU Yang, CAI Ming, CHENG Tang-Ren, WANG Jia, ZHANG Qi-Xiang, PAN Hui-Tang*
Beijing Forestry University, College of Landscape Architecture, Beijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding, National Engineering Research Center for Floriculture, Beijing Laboratory of Urban and Rural Ecological Environment, Beijing 100083, China
Abstract：TCP (teosinte branched 1, cycloidea, proliferating cell factors) transcription factors are widely involved in plants, which play an important role in regulating plant growth and development, morphogenesis, abiotic stress and other physiological processes as a kind of plant-specific transcription factor. They can regulate the expression of downstream target genes to transform the cell division process, and play a role in a variety of hormone regulatory pathways. Lagerstroemia indica, as an excellent kind of summer flowering woody plant, is commonly used in gardens. Because of its rich germplasm resources and diverse plant architecture, it is a good material for investigating woody plant architecture. In order to clarify the role of the TCP gene family in Lagerstroemia, a total of 44 TCP genes were identified in Lagerstroemia based on transcriptome data. The bioinformatics and gene expression analyses were used to analyze the characters and expression patterns of LfiTCPs. The results showed that the proteins encoded by the LfiTCPs were uniform and stable in physical and chemical properties, and were mostly localized in the nucleus. Phylogenetic analysis showed that the LfiTCPs were divided into 2 branches, and the number and proportion of which were similar to other species. LfiTCPs had a relatively conservative structure, which could maintain the TCP domain intact, and those LfiTCPs in 2 branches had obvious structural differences. Most of the LfiTCPs were similarly expressed in standard and dwarf crapemyrtles,14 of them were initially screened out based on the differential expression results. Among which, LfiTCP12;2 and LfiTCP15;2 showed significant differences between non-dwarf and dwarf progenies. The result of qRT-PCR confirmed that they were highly expressed and lowly expressed in dwarf progenies, respectively. This study provides the information for further research on the plant architecture of Lagerstroemia indica, potentially promoting the molecular breeding process of woody plant architecture.
[1] 刘文文, 李文学. 2013. 植物bHLH转录因子研究进展[J]. 生物技术进展, 3(1): 7-11. (Liu W W, Li W X.2013. Progress of plant bHLH transcription factor[J]. Current Biotechnology, 3(1): 7-11.) [2] 石俊, 陈之琳, 秦波, 等. 2016. 紫薇匍匐平展性状相关表型遗传分析[C]//. 中国观赏园艺研究进展, 100-109. (Shi J, Chen Z L, Qin B, et al.2016. Phenotypic and genetic analysis of reptant plant type, applanate branch and other related characters in Lagerstroemia indica[C]//. Advances in Ornamental Horticulture of China, 100-109.) [3] 张启翔. 1991. 紫薇品种分类及其在园林中的应用(英文)[J]. 北京林业大学学报, 13(4): 59-68. (Zhang Q X.1991. Studies on cultivars of crape-myrtle (Lagerstroemia indica) and their uses in urban greening[J]. Journal of Beijing Forestry University, 13(4): 59-68.) [4] Aggarwal P, Padmanabhan B, Bhat A, et al.2011. The TCP4 transcription factor of Arabidopsis blocks cell division in yeast at G1→S transition[J]. Biochemical and Biophysical Research Communications, 410(2): 276-281. [5] Aguilar-Martinez J A, Poza-Carrion C, Cubas P.2007. Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds[J]. The Plant Cell, 19(2): 458-472. [6] Aguilar-Martínez J A, Sinha N.2013. Analysis of the role of Arabidopsis class I TCP genes AtTCP7, AtTCP8, AtTCP22, and AtTCP23 in leaf development[J]. Frontiers in Plant Science, 4: 406. [7] Chen C, Chen H, Zhang Y, et al.2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data[J]. Molecular Plant, 13(8): 1194-1202. [8] Cubas P, Lauter N, Doebley J, et al.1999. The TCP domain a motif found in proteins regulating plant growth and development[J]. The Plant Journal, 18(2): 215-222. [9] Ferrero L V, Gastaldi V, ArielF D, et al.2021. Class I TCP proteins TCP14 and TCP15 are required for elongation and gene expression responses to auxin[J]. Plant Molecular biology, 105(1-2): 147-159. [10] Finlayson S A, Krishnareddy S R, Kebrom T H, et al.2010. Phytochrome regulation of branching in Arabidopsis[J]. Plant Physiology, 152(4): 1914-1927. [11] Gaudin V R, Lunness P A, Fobert P R, et al.2000. The expression of D-cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea gene[J]. Plant Physiology, 122(4): 1137-1148. [12] González-Grandío E, Cubas P.2016. Plant Transcription Factors. TCP transcription Factors: Evolution, Structure, and Biochemical Function[M]. Academic Press, The USA, pp. 139-151. [13] Guo Z, Fujioka S, Blancaflor E B, et al.2010. TCP1 modulates brassinosteroid biosynthesis by regulating the expression of the key biosynthetic gene DWARF4 in Arabidopsis thaliana[J]. The Plant Cell, 22(4): 1161-1173. [14] Hervé C, Dabos P, Bardet C, et al.2009. In vivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development[J]. Plant Physiology, 149(3): 1462-1477. [15] Howarth D G, Donoghue M J.2006. Phylogenetic analysis of the 'ECE' (CYC/TB1) clade reveals duplications predating the core eudicots[J]. Proceedings of the National Academy of Sciences of the USA, 103(24): 9101-9106. [16] Ju Y, Feng L, Wu J, et al.2018. Transcriptome analysis of the genes regulating phytohormone and cellular patterning in Lagerstroemia plant architecture[J]. Scientific Reports, 8(1): 15162. [17] Kieffer M, Master V, Waites R, et al.2011. TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis[J].The Plant Journal, 68(1): 147-158. [18] Lan T, Yang Z-L, Yang X, et al.2009. Extensive functional diversification of the Populus glutathione S-transferase supergene family[J]. The Plant Cell, 21(12): 3749-3766. [19] Li S.2015. The Arabidopsis thaliana TCP transcription factors: A broadening horizon beyond development[J]. Plant Signal & Behavior, 10(7): e1044192. [20] Li W, Li D D, Han L H, et al.2017. Genome-wide identification and characterization of TCP transcription factor genes in upland cotton (Gossypium hirsutum)[J]. Scientific Reports, 7(1): 10118. [21] Li Z Y, Li B, Dong A W.2012. The Arabidopsis transcription factor AtTCP15 regulates endoreduplication by modulating expression of key cell-cycle genes[J]. Molecular Plant, 5(1): 270-280. [22] Livak K J, Schmittgen T D.2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method[J]. Methods, 25(4): 402-408. [23] Long T A, Tsukagoshi H, Busch W, et al.2010. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots[J]. The Plant Cell, 22(7): 2219-2236. [24] Luo D, Carpenter R, Copsey L, et al.1999. Control of organ asymmetry in flowers of Antirrhinum[J]. Cell, 99(4): 367-376. [25] Luo D, Carpenter R, Vincent C, et al.1996. Origin of floral asymmetry in Antirrhinum[J]. Nature (London), 383(6603): 794-799. [26] Manassero N G U, Viola I L, Welchen E, et al.2013. TCP transcription factors: Architectures of plant form[J]. Biomolecular Concepts, 4(2): 111-127. [27] Martín-Trillo M, Cubas P.2010. TCP genes: a family snapshot ten years later[J].Trends in Plant Science, 15(1): 31-39. [28] Menges M, Jager S M D, Gruissem W, et al.2005. Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control[J].The Plant Journal, 41(4): 546-566. [29] Navaud O, Dabos P, Carnus E, et al.2007. TCP transcription factors predate the emergence of land plants[J]. Journal of Molecular Evolution, 65(1): 23-33. [30] Nicolas M, Cubas P.2016a. Plant Transcription Factors. The Role of TCP Transcription Factors in Shaping Flower Structure, Leaf Morphology, and Plant Architecture[M]. Academic Press, , The USA, pp. 249-267. [31] Nicolas M, Cubas P.2016b. TCP factors: New kids on the signaling block[J]. Current Opinion Plant Biology, 33: 33-41. [32] Swaminathan K, Yang Y, Grotz N, et al.2000. An enhancer trap line associated with a D-class cyclin gene in Arabidopsis[J]. Plant Physiology, 124(4): 1658-1667. [33] Uberti-Manassero N G, Lucero L E, Viola I L, et al.2012. The class Ⅰ protein AtTCP15 modulates plant development through a pathway that overlaps with the one affected by CIN-like TCP proteins[J]. Journal of Experimental Botany, 63(2): 809-823. [34] Vadde B V L, Challa k R, Sunkara P, et al.2019. The TCP4 transcription factor directly activates TRICHOMELESS1 and 2 and suppresses trichome initiation[J]. Plant Physiology, 181(4): 1587-1599. [35] Wang Z C, Cui D Y, Hu Y X.2017. CIN-like TCP transcription factors: The key regulators of plant development and immunity[J].Progress in Biochemistry and Biophysics, 43(3): 215-223. [36] Wilkins O, Nahal H, Foong J, et al.2009. Expansion and diversification of the Populus R2R3-MYB family of transcription factors[J]. Plant Physiology, 149(2): 981-993. [37] Yao X, Ma H, Wang J, et al.2007. Genome-wide comparative analysis and expression pattern of TCP gene families in Arabidopsis thaliana and Oryza sativa[J]. Journal of Integrative Plant Biology, 49(6): 885-897. [38] Ye Y J, Cai M, Ju Y Q, et al.2016. Identification and validation of SNP markers linked to dwarf traits using SLAF-seq technology in Lagerstroemia[J]. PLOS ONE, 11(7): e0158970. [39] Ye Y J, Wu J Y, Feng L, et al.2017a. Heritability and gene effects for plant architecture traits of crape myrtle using major gene plus polygene inheritance analysis[J]. Scientia Horticulturae, 225: 335-342. [40] Ye Y J, Feng L, Ju Y Q, et al.2017b. Genetic evaluation and core collection construction of crape myrtle accessions using newly developed EST-SSR markers[J]. PeerJ Preprints,(5): e3141v1. [41] Ye Y J, Liu Y, Cai M, et al.2015. Screening of molecular markers linked to dwarf trait in crape myrtle by bulked segregant analysis[J]. Genetics and Molecular Research, 14(2): 4369-4380. [42] Zhang G, Zhao H, Zhang C, et al.2019. TCP7 functions redundantly with several Class I TCPs and regulates endoreplication in Arabidopsis[J]. Journal of Integrative Plant Biology, 61(11): 1151-1170. [43] Zheng T, Chen Z, Ju Y, et al.2018. Reference gene selection for qRT-PCR analysis of flower development in Lagerstroemia indica and L. speciosa[J]. PLOS ONE, 13(3): e0195004.
