TCP family genes control leaf development and its responses to gibberellin in celery

• Autorzy: Duan A.-Q. , Wang Y.-W. , Feng K. , Liu J.-X. , Xu Z.-S. , Xiong A.-S.
• Języki publikacji: EN

Abstrakty

EN

Celery is a biennial herb of the Apiaceae family and is a leafy vegetable crop widely cultivated worldwide. TCP (teosinte branched1/cycloidea/proliferating cell factors), a transcription factor family, is involved in cell growth and leaf tissue proliferation. In this study, 32 AgTCP transcription factors were identified and analyzed based on the celery transcriptome and genome database and divided into two classes. Analysis of structural feature, phylogenetic tree, interaction network, and subcellular localization of AgTCP proteins was performed. It is shown that the AgTCP2 protein was positioned in the nucleus, and TCP proteins in the same group had higher similarity. Heatmap clusters of AgTCP genes expression levels during different celery leaf developmental stages suggested that the genes from the same evolutionary branch tended to form a cluster. The expression profiles of four AgTCP genes were detected at celery leaf developmental stages and under gibberellin (GA₃) treatment. As a CYC-type gene, AgTCP4 showed significantly increased expression levels under developmental stage and GA₃ treatment in ‘Liuhe Huangxinqin’. The results of this work give potential helpful information for further analysis of the role of AgTCP transcription factors in leaf development and hormone regulation in celery.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2019
• Tom: 41
• Numer: 09
• Opis fizyczny: Article 153 [12p.], fig.,ref.

Twórcy

autor

Duan A.-Q.

• State Key Laboratory of Crop Genetics and Germplasm Enhancement, Ministry of Agriculture and Rural Affairs Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, College of Horticulture, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China

autor

Wang Y.-W.

• State Key Laboratory of Crop Genetics and Germplasm Enhancement, Ministry of Agriculture and Rural Affairs Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, College of Horticulture, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China

autor

Feng K.

• State Key Laboratory of Crop Genetics and Germplasm Enhancement, Ministry of Agriculture and Rural Affairs Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, College of Horticulture, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China

autor

Liu J.-X.

• State Key Laboratory of Crop Genetics and Germplasm Enhancement, Ministry of Agriculture and Rural Affairs Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, College of Horticulture, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China

autor

Xu Z.-S.

• State Key Laboratory of Crop Genetics and Germplasm Enhancement, Ministry of Agriculture and Rural Affairs Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, College of Horticulture, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China

autor

Xiong A.-S.

• State Key Laboratory of Crop Genetics and Germplasm Enhancement, Ministry of Agriculture and Rural Affairs Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, College of Horticulture, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China

Bibliografia

• Aguilar-Martinez JA, 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
• Balsemão-Pires E, Andrade LR, Sachetto-Martins G (2013) Functional study of TCP23 in Arabidopsis thaliana during plant development. Plant Physiol Biochem 67:120–125
• Braun N, de Saint Germain A, Pillot JP, Boutet-Mercey S, Dalmais M, Antoniadi I, Li X, Maia-Grondard A, Le Signor C, Bouteiller N, Luo D, Bendahmane A, Turnbull C, Rameau C (2012) The pea TCP transcription factor PsBRC1 acts downstream of Strigolactones to control shoot branching. Plant Physiol 158(1):225–238
• Broholm SK, Tahtiharju S, Laitinen RA, Albert VA, Teeri TH, Elomaa P (2008) A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. Proc Natl Acad Sci USA 105(26):9117–9122
• Craig WJ (1999) Health-promoting properties of common herbs. Am J Clin Nutr 70(3 Suppl):491S–499S
• Cubas P, Lauter N, Doebley J, Coen E (2010) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18(2):215–222
• Dal Santo S, Vannozzi A, Tornielli GB, Fasoli M, Venturini L, Pezzotti M, Zenoni S (2013) Genome-wide analysis of the expansin gene superfamily reveals grapevine-specific structural and functional characteristics. PLoS One 8(4):e62206
• Danisman S, van Dijk AD, Bimbo A, van der Wal F, Hennig L, de Folter S, Angenent GC, Immink RG (2013) Analysis of functional redundancies within the Arabidopsis TCP transcription factor family. J Exp Bot 64(18):5673–5685
• Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386(6624):485–488
• Efroni I, Blum E, Goldshmidt A, Eshed Y (2008) A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20(9):2293–2306
• Feng K, Hou XL, Li MY, Jiang Q, Xu ZS, Liu JX, Xiong AS (2018a) CeleryDB: a genomic database for celery. Database (Oxford). https://doi.org/10.1093/database/bay070
• Feng K, Liu JX, Duan AQ, Li T, Yang QQ, Xu ZS, Xiong AS (2018b) AgMYB2 transcription factor is involved in the regulation of anthocyanin biosynthesis in purple celery (Apium graveolens L.). Planta 248(5):1249–1261
• Guo Z, Fujioka S, Blancaflor EB, Miao S, Gou X, Li J (2010) TCP1 modulates brassinosteroid biosynthesis by regulating the expression of the key biosynthetic gene DWARF4 in Arabidopsis thaliana. Plant Cell 22(4):1161–1173
• Herve C, Dabos P, Bardet C, Jauneau A, Auriac MC, Ramboer A, Lacout F, Tremousaygue D (2009) In vivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development. Plant Physiol 149(3):1462–1477
• Horn S, Pabónmora N, Theuß VS, Busch A, Zachgo S (2015) Analysis of the CYC/TB1 class of TCP transcription factors in basal angiosperms and magnoliids. Plant J 81(4):559–571
• Huang T, Irish VF (2015) Temporal control of plant organ growth by TCP transcription factors. Curr Biol 25(13):1765–1770
• Jia XL, Wang GL, Xiong F, Yu XR, Xu ZS, Wang F, Xiong AS (2015a) De novo assembly, transcriptome characterization, lignin accumulation, and anatomic characteristics: novel insights into lignin biosynthesis during celery leaf development. Sci Rep 5:8259
• Jia XL, Li MY, Jiang Q, Xu ZS, Wang F, Xiong AS (2015b) High-throughput sequencing of small RNAs and anatomical characteristics associated with leaf development in celery. Sci Rep 5:11093
• Jiang CJ, Imamoto N, Matsuki R, Yoneda Y, Yamamoto N (1998) Functional characterization of a plant importin alpha homologue. Nuclear localization signal (NLS)-selective binding and mediation of nuclear import of nls proteins in vitro. J Bio Chem 273(37):24083–24087
• Jones NR, Lazarus P (2014) UGT2B gene expression analysis in multiple tobacco carcinogen-targeted tissues. Drug Metab Dispos 42(4):529–536
• Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9(9):1607–1619
• Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30(3):337–348
• Koyama T, Furutani M, Tasaka M, Ohme-Takagi M (2007) TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. Plant Cell 19(2):473–484
• Koyama T, Sato F, Ohme-Takagi M (2017) Roles of miR319 and TCP transcription factors in leaf development. Plant Physiol 175(2):874–885
• Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874
• Li MY, Wang F, Jiang Q, Ma J, Xiong AS (2014) Identification of SSRs and differentially expressed genes in two cultivars of celery (Apium graveolens L.) by deep transcriptome sequencing. Hortic Res 1:10
• Li MY, Wang F, Jiang Q, Wang GL, Tian C, Xiong AS (2016) Validation and comparison of reference genes for qPCR normalization of celery (Apium graveolens) at different development stages. Front Plant Sci 7:313
• Li H, Liu ZW, Wu ZJ, Wang YX, Teng RM, Zhuang J (2018a) Differentially expressed protein and gene analysis revealed the effects of temperature on changes in ascorbic acid metabolism in harvested tea leaves. Hortic Res 5:65
• Li MY, Hou XL, Wang F, Tan GF, Xu ZS, Xiong AS (2018b) Advances in the research of celery, an important Apiaceae vegetable crop. Crit Rev Biotechnol 38(2):172–183
• Li C, Qiu J, Huang S, Yin J, Yang G (2019) AaMYB3 interacts with AabHLH1 to regulate proanthocyanidin accumulation in Anthurium andraeanum (Hort.)-another strategy to modulate pigmentation. Hortic Res 6:14
• Lucero LE, Manavella PA, Gras DE, Ariel FD, Gonzalez DH (2017) Class I and class II TCP transcription factors modulate SOC1-dependent flowering at multiple levels. Mol plant 10(12):1571–1574
• Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383(6603):794–799
• Martíntrillo M, Cubas P (2010) TCP genes: a family snapshot 10 years later. Trends Plant Sci 15(1):31–39
• Navaud O, Dabos P, Carnus E, Tremousaygue D, Herve C (2007) TCP transcription factors predate the emergence of land plants. J Mol Evol 65(1):23–33
• Olofsson L, Engström A, Lundgren A, Brodelius PE (2011) Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biol 11:45
• Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, Menda N, Amsellem Z, Efroni I, Pekker I (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39(6):787–791
• Perez-Rodriguez P, Riano-Pachon DM, Correa LG, Rensing SA, Kersten B, Mueller-Roeber B (2010) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38(Dasebase issue):D822–D827
• Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(9):e45
• Raffo A, Sinesio F, Moneta E, Nardo N, Peparaio M, Paoletti F (2006) Internal quality of fresh and cold stored celery petioles described by sensory profile, chemical and instrumental measurements. Eur Food Res Technol 222(5):590–599
• Sun CH, Yu JQ, Duan X, Wang JH, Zhang QY, Gu KD, Hu DG, Zheng CS (2018) The MADS transcription factor CmANR1 positively modulates root system development by directly regulating CmPIN2 in chrysanthemum. Hortic Res 5:52
• Suzuki T, Sakurai K, Ueguchi C, Mizuno T (2001) Two types of putative nuclear factors that physically interact with histidine-containing phosphotransfer (Hpt) domains, signaling mediators in His-to-Asp phosphorelay, in Arabidopsis thaliana. Plant Cell Physiol 42(1):37–45
• Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C (2015) STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43(Database issue):D447–D452
• Tan XL, Fan ZQ, Shan W, Yin XR, Kuang JF, Lu WJ, Chen JY (2018) Association of BrERF72 with methyl jasmonate-induced leaf senescence of Chinese flowering cabbage through activating JA biosynthesis-related genes. Hortic Res 5:22
• Tatematsu K, Nakabayashi K, Kamiya Y, Nambara E (2010) Transcription factor AtTCP14 regulates embryonic growth potential during seed germination in Arabidopsis thaliana. Plant J 53(1):42–52
• Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680
• Viola IL, Uberti Manassero NG, Ripoll R, Gonzalez DH (2011) The Arabidopsis class I TCP transcription factor AtTCP11 is a developmental regulator with distinct DNA-binding properties due to the presence of a threonine residue at position 15 of the TCP domain. Biochem J 435(1):143–155
• Wei B, Zhang J, Pang C, Yu H, Guo D, Jiang H, Ding M, Chen Z, Tao Q, Gu H (2015) The molecular mechanism of SPOROCYTELESS/NOZZLE in controlling Arabidopsis ovule development. Cell Res 25(1):121–134
• Wu ZJ, Wang WL, Zhuang J (2017) TCP family genes control leaf development and its responses to hormonal stimuli in tea plant [Camellia sinensis (L.) O. Kuntze]. Plant Growth Regul 83:43–53
• Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M (2005) Transcription Factors in Rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59(1):191–203
• Zhou Y, Zhang D, An J, Yin H, Fang S, Chu J, Zhao Y, Li J (2017) TCP transcription factors regulate shade avoidance via directly mediating the expression of both PHYTOCHROME INTERACTING FACTORs and auxin biosynthetic genes. Plant Physiol 176(2):1850–1861

Identyfikatory

DOI

10.1007/s11738-019-2945-3