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Expression and Functional Analysis of the ZCN1(ZmTFL1) Gene, a TERMINAL FLOWER 1 Homologue that Regulates the Vegetative to Reproductive Transition in Maize

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Abstract

TERMINAL FLOWER 1 (TFL1) homologs play critical roles in regulating flowering time and/or maintaining flowering of meristems. In this study, the gene of maize TFL1 ortholog ZmTFL1 (ZCN1) was cloned from both the tropical inbred line CML288 and temperate inbred line Huangzao 4, and the function of ZmTFL1 (ZCN1) was determined during different periods of floral development. Spatial and temporal expression patterns revealed that ZCN1 was predominantly localized in shoot apical meristems that develop into flowers, and only at low levels in leaves. To further identify the role of ZCN1 in floral development of maize, the morphology of shoot apices in maize during floral development was investigated using laser scanning confocal microscopy. Moreover, the relative levels of expression of ZCN1, ZCN8, DLF1, and ZAP1 genes were determined. Over-expression of ZCN1 partially complemented the late flowering phenotype in the tfl1-14 Arabidopsis mutant. Moreover, transgenic Arabidopsis plants exhibited indeterminate inflorescence with increased shoot length and higher numbers of trichomes on leaves. In addition, expression levels of AP1 were significantly down-regulated in 35S::ZCN1 transgenic Arabidopsis plants. These results indicated that ZCN1 as well as its homolog TFL1 in Arabidopsis are involved in the regulation of floral transition in maize.

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References

  • Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056

    Article  PubMed  CAS  Google Scholar 

  • Ahn JH, Miller D, Winter VJ, Banfield MJ, JLee H, Yoo SY, Henz SR, Brady RL, Weigel D (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25:605–614

    Article  PubMed  CAS  Google Scholar 

  • An H, Roussot C, Suárez-López P, Corbesier L, Vincent C, Piñeiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131:3615–3626

    Article  PubMed  CAS  Google Scholar 

  • Ausin I, Carlos AB, Martinea-Zapater JM (2005) Environmental regulation of flowering. Int J Dev Biol 49:689–705

    Article  PubMed  CAS  Google Scholar 

  • Blazquez MA, Soowal LN, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124:3835–3844

    PubMed  CAS  Google Scholar 

  • Bomblies K, Doebley JF (2005) Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication. Genetics 172:519–531

    Article  PubMed  Google Scholar 

  • Bomblies K, Wang RL, Ambrose BA, Schmidt RJ, Meeley RB, Doebley J (2003) Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130:2385–2395

    Article  PubMed  CAS  Google Scholar 

  • Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E (1996) Control of inflorescence architecture in Antirrhinum. Nature 379:791–797

    Article  PubMed  CAS  Google Scholar 

  • Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80–83

    Article  PubMed  CAS  Google Scholar 

  • Christensen AH, Quail PH (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res 5:213–218

    Article  PubMed  CAS  Google Scholar 

  • Colasanti J, Sundaresan V (2000) ‘Florigen’ enters the molecular age: long-distance signals that cause plants to flower. Trends Biochem Sci 25:236–240

    Article  PubMed  CAS  Google Scholar 

  • Colasanti J, Tremblay R, Wong AY, Coneva V, Kozaki A, Mable BK (2006) The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants. BMC Genomics 7:158

    Article  PubMed  Google Scholar 

  • Colasanti J, Yuan Z, Sundaresan V (1998) The indeterminate gene encodes a zinc finger protein and regulates a leaf-generated signal required for the transition to flowering in maize. Cell 93:593–603

    Article  PubMed  CAS  Google Scholar 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033

    Article  PubMed  CAS  Google Scholar 

  • Danilevskaya ON, Meng X, Ananiev EV (2010) Concerted modification of flowering time and inflorescence architecture by ectopic expression of tfl1-like genes in maize. Plant Physiol 153:238–251

    Article  PubMed  CAS  Google Scholar 

  • Danilevskaya ON, Meng X, Hou ZL, Ananiev EV, Simmons CR (2008a) A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol 146:250–264

    Article  PubMed  CAS  Google Scholar 

  • Danilevskaya ON, Meng X, Selinger DA, Deschamps S, Hermon P, Vansant G, Gupta R, Ananiev EV, Muszynski MG (2008b) Involvement of the MADS-box gene ZMM4 in floral induction and inflorescence development in maize. Plant Physiol 147:2054–2069

    Article  PubMed  CAS  Google Scholar 

  • Giauffret C, Lothrop J, Dorvillez D, Gouesnard B, Derieux M (2000) Genotype × environment interactions in maize hybrids from temperate or highland tropical origin. Crop Sci 40:1004–1012

    Article  Google Scholar 

  • Goodman MM (1985) Exotic maize germplasm: status, prospects, and remedies. Iowa State J Res 59:497–527

    Google Scholar 

  • Gouesnard B, Rebourg C, Welcker C, Charcosset A (2002) Analysis of photoperiod sensitivity within a collection of tropical maize populations. Genet Resour Crop Evol 49:471–481

    Article  Google Scholar 

  • Guo QF, Wang QC, Wang LM (2004) Shandong Academy of Agricultural Sciences. China maize cultivation science. Shanghai Sciences and Technology Press, Shanghai (in Chinese)

    Google Scholar 

  • Heuer S, Hansen S, Bantin J, Brettschneider R, Kranz E, Lörz H, Dresselhaus T (2001) The maize MADS Box gene ZmMADS3 affects node number and spikelet development and is co-expressed with ZmMADS1 during flower development, in egg cells, and early embryogenesis. Plant Physiol 127:33–45

    Article  PubMed  CAS  Google Scholar 

  • Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 12:1050–1054

    Article  Google Scholar 

  • Jensen CS, Salchert K, Nielsen KK (2001) A TERMINAL FLOWER1-like gene from perennial ryegrass involved in floral transition and axillary meristem identity. Plant Physiol 125:1517–1528

    Article  PubMed  CAS  Google Scholar 

  • Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi R, Kawahigashi H, Ando T, Tonooka T, Handa H (2009) Molecular and functional characterization of pebp genes in barley reveal the diversification of their roles in flowering. Plant Physiol 149:1341–1353

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962

    Article  PubMed  CAS  Google Scholar 

  • Kozaki A, Hake S, Colasanti J (2004) The maize ID1 flowering time regulator is a zinc finger protein with novel DNA binding properties. Nucleic Acids Res 32:1710–1720

    Article  PubMed  CAS  Google Scholar 

  • Li GP, Huang Q (2005) Whole stain-clearing technique for observation for pollen grain structure of Keleteeria fortunei. J Zhengzhou Univ Nat Sci Ed 37:44–47 (in Chinese)

    Google Scholar 

  • Li H, Luo J, Wang JT, Wang JT, Gould JH (2001) A rapid and high yielding DNA miniprep for cotton (Gossypium spp.). Plant Mol Biol Report 19:183 a–e

    Google Scholar 

  • Liljegren SJ, Gustafson-Brown C, Pinyopich A, Dittaa GS, Yanofsky MF (1999) Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell 11:1007–1018

    Article  PubMed  CAS  Google Scholar 

  • Lin MK, Belanger H, Lee YJ, Varkonyi-Gasic E, Taoka KI, Miura E, Xoconostle-Cázares B, Gendler K, Jorgensen RA, Phinney B, Lough TJ, Lucas WJ (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19:1488–1506

    Article  PubMed  CAS  Google Scholar 

  • Liu JL (1991) Maize breeding. Agriculture Press, Beijing (in Chinese)

    Google Scholar 

  • Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377:522–524

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Trujillo M, Limones-BrioneV Cabrera-Ponce JL, Herrera-Estrella L (2004) Improving transformation efficiency of Arabidopsis thaliana by modifying the floral dip method. Plant Mol Biol Report 22:63–70

    Article  CAS  Google Scholar 

  • Mena M, Mandel MA, Lerner DR, Yanofsky MF, Schmidt RJ (1995) A characterization of the MADS-box gene family in maize. Plant J 8:845–854

    Article  PubMed  CAS  Google Scholar 

  • Meng X, Muszynski MG, Danilevskaya ON (2011) The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23:942–960

    Article  PubMed  CAS  Google Scholar 

  • Muszynski MG, Dam T, Li B, Shirbroun DM, Hou ZL, Bruggemann E, Archibald R, Ananiev EV, Danilevskaya ON (2006) Delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant Physiol 142:1523–1536

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa M, Shimamoto K, Kyozuka J (2002) Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. Plant J 29:743–750

    Article  PubMed  CAS  Google Scholar 

  • Ohshima S, Murata M, Sakamoto W, Ogura Y, Motoyoshi F (1997) Cloning and molecular analysis of the Arabidopsis gene Terminal Flower 1. Mol Gen Genet 254:186–194

    Article  PubMed  CAS  Google Scholar 

  • Pan Y (2005) MADS-box genes play diverse roles in flowering time regulation of Arabidopsis and maize. Dissertations, Marquette University

  • Parcy F (2005) Flowering: a time for integration. Int J Dev Biol 49:585–593

    Article  PubMed  Google Scholar 

  • Pelaz S, Gustafson-Brown C, Kohalmi SE, Crosby WL, Yanofsky MF (2001) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26:385–394

    Article  PubMed  CAS  Google Scholar 

  • Pillitteri LJ, Lovatt CJ, Walling LL (2004) Isolation and characterization of a terminal flower homolog and its correlation with juvenility in citrus. Plant Physiol 135:1540–1551

    Article  PubMed  CAS  Google Scholar 

  • Ratcliffe OJ, Bradley DJ, Coen ES (1999) Separation of shoot and floral meristem identity in Arabidopsis. Development 126:1109–1120

    PubMed  CAS  Google Scholar 

  • Susan S, Meeks-Wagner OR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892

    Google Scholar 

  • Tamaki S, Matsuo S, Wong H, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036

    Article  PubMed  CAS  Google Scholar 

  • Telfer A, Bollman KM, Poethig RS (1997) Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124:645–654

    PubMed  CAS  Google Scholar 

  • Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059

    Article  PubMed  CAS  Google Scholar 

  • Wu LC, Wang TG, Ku LX, Huang QC, Sun ZH, Xia ZL, Chen YH (2008) Determination of the photoperiod-sensitive inductive phase in maize with leaf numbers and morphologies of stem apical meristem. Agricultural Sciences in China 7:554–560

    Article  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (No. 30971789) and the National Basic Research Program of China (No. 2009CB118400).We thank Tiegu Wang for help with microscope imaging and Xiangsheng Qi for field technical assistance. The manuscript was significantly improved due to critical comments from Xuchu Wang and Yong Tan.

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Authors and Affiliations

  1. Zhengzhou Sub-center of Chinese National Maize Improvement Center, Agronomy College of Henan Agricultural University, Zhengzhou, 450002, Henan, China

    Lili Chang, Liancheng Wu, Yanhui Chen, Lixia Ku, Shuang Yang, Shaofang Zhang, Xintao Wang & Xiaomin Wei

  2. The breeding base of national key lab supported by Henan province and Ministry of Science and Technology, Zhengzhou, 450002, Henan, China

    Liancheng Wu, Yanhui Chen & Lixia Ku

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  1. Lili Chang
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Correspondence to Yanhui Chen.

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Lili Chang and Liancheng Wu contributed equally to this work.

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Chang, L., Wu, L., Chen, Y. et al. Expression and Functional Analysis of the ZCN1(ZmTFL1) Gene, a TERMINAL FLOWER 1 Homologue that Regulates the Vegetative to Reproductive Transition in Maize. Plant Mol Biol Rep 30, 55–66 (2012). https://doi.org/10.1007/s11105-011-0317-2

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