Journal of Plant Biology

, Volume 61, Issue 6, pp 410–423 | Cite as

Molecular and Functional Characterization of ZmNF-YC14 in Transgenic Arabidopsis

  • Xiupeng Mei
  • Ping Li
  • Lu Wang
  • Chaoxian Liu
  • Lian Zhou
  • Yilin CaiEmail author
Original Article


The optimum transition stage from vegetative to reproductive development is important for flowering plants to obtain the desired plant architecture to maximize yield. In this study, we overexpressed the maize NUCLEAR FACTOR Y, SUBUNIT C 14 (ZmNF-YC14) gene in Arabidopsis to investigate its potential functions in the regulation of plant transition. Overexpression of ZmNF-YC14 in Arabidopsis inhibited plant flowering and retarded the duration of the branch-producing inflorescence phase 1 (I1). These plants exhibited increased length of I1 and higher ratio of inflorescence phase 1 to inflorescence phase (I) (I1:I) under long-day conditions. As a consequence, these transgenic plants exhibited dramatic changes in their overall inflorescence morphology. In addition, the phenotypes of inflorescence morphology caused by ZmNF-YC14 overexpression were enhanced by exogenous gibberellin (GA) treatment, which obtained a significant increase in I1:I, inflorescence phase 1 to inflorescence phase 2 (I2) (I1:I2), and remarkable decrease in I2 and I2:I in transgenic plants compared to those under normal conditions. Taken together, the results of this study suggest that ZmNFYC14 negatively regulates flowering and controls flower formation under long-day conditions in Arabidopsis and may be involved in a GA regulation pathway.


Flowering time GA pathway Maize NF-YC Inflorescence architecture 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

12374_2018_162_MOESM1_ESM.pdf (957 kb)
Supplementary Figures


  1. Blázquez MA, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404:889–892CrossRefGoogle Scholar
  2. Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR (1993) Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Dev 119:721–743Google Scholar
  3. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735CrossRefGoogle Scholar
  4. De LM, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480CrossRefGoogle Scholar
  5. Dill A, Sun T (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genet 159:777–785Google Scholar
  6. Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesiaspedraz JM, Kircher S (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475CrossRefGoogle Scholar
  7. Fornara F, Panigrahi KC, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86CrossRefGoogle Scholar
  8. Fu X, Richards DE, Fleck B, Xie D, Burton N, Harberd NP (2004) The Arabidopsis mutant sleepy1 gar2-1 protein promotes plant growth by increasing the affinity of the SCF SLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16:1406–1418CrossRefGoogle Scholar
  9. Galvão VC, Horrer D, Küttner F, Schmid M (2012) Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Dev 139:4072–4082CrossRefGoogle Scholar
  10. Gustafsonbrown C, Savidge B, Yanofsky, F. M (1994) Regulation of the Arabidopsis floral homeotic gene. Cell 76:131CrossRefGoogle Scholar
  11. Hackenberg D, Wu Y, Voigt A, Adams R, Schramm P, Grimm B (2012) Studies on differential nuclear translocation mechanism and assembly of the three subunits of the Arabidopsis thaliana transcription factor NF-Y. Mol Plant 5:876–888CrossRefGoogle Scholar
  12. Han X, Tang S, An Y, Zheng DC, Xia XL, Yin WL (2013) Overexpression of the poplar NF-YB7 transcription factor confers drought tolerance and improves water-use efficiency in Arabidopsis. J Exp Bot 64:4589–4601CrossRefGoogle Scholar
  13. Hempel FD, Weigel D, Mandel MA, Ditta G, Zambryski PC, Feldman LJ, Yanofsky MF (1997) Floral determination and expression of floral regulatory genes in Arabidopsis. Dev 124:3845–3853Google Scholar
  14. Hou X, Lee LY, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19:884CrossRefGoogle Scholar
  15. Hou X, Zhou J, Liu C, Liu L, Shen L, Yu H (2014) Nuclear factor Ymediated H3K27me3 demethylation of the SOC1 locus orchestrates flowering responses of Arabidopsis. Nat Commun 5:4601CrossRefGoogle Scholar
  16. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchishinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in coldresponsive gene expression in transgenic rice. Plant Cell Physiol 47:141CrossRefGoogle Scholar
  17. Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267:522–525CrossRefGoogle Scholar
  18. Kim SK, Park HY, Jang YH, Lee KC, Chung YS, Lee JH, Kim JK (2016) OsNF-YC2 and OsNF-YC4 proteins inhibit flowering under long-day conditions in rice. Planta 243:563CrossRefGoogle Scholar
  19. Koornneef M, Hanhart CJ, Jh VDV (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57CrossRefGoogle Scholar
  20. Kumimoto RW, Adam L, Hymus GJ, Repetti PP, Reuber TL, Marion CM, Hempel FD, Ratcliffe OJ (2008) The Nuclear Factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis. Planta 228:709–723CrossRefGoogle Scholar
  21. Kumimoto RW, Zhang Y, Siefers N, Rd HB (2010) NF-YC3, NFYC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. Plant J 63:379–391CrossRefGoogle Scholar
  22. Lee H, Suh SS, Park E, Cho E, Ji HA, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Gene Dev 14:2366–2376CrossRefGoogle Scholar
  23. Liu JX, Howell SH (2010) bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell 22:782–796CrossRefGoogle Scholar
  24. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060CrossRefGoogle Scholar
  25. Liu C, Chen H, Hong LE, Hui MS, Kumar PP, Han JH, Liou YC, Yu H (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Dev 135:1481CrossRefGoogle Scholar
  26. Liu S, Wang X, Wang H, Xin H, Yang X, Yan J, Li J, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K, Qin F (2013). Genomewide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. Plos Genetics 9:e1003790CrossRefGoogle Scholar
  27. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277CrossRefGoogle Scholar
  28. Mandel MA, Yanofsky M (1995) A gene triggering flower formation in Arabidopsis. Nature 377:522–524CrossRefGoogle Scholar
  29. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956CrossRefGoogle Scholar
  30. Miyoshi K, Ito Y, Serizawa A, Kurata N (2003) OsHAP3 genes regulate chloroplast biogenesis in rice. Plant J 36:532–540CrossRefGoogle Scholar
  31. Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623CrossRefGoogle Scholar
  32. Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. P Natl Acad Sci USA 104:16450–16455CrossRefGoogle Scholar
  33. Ni Z, Zheng H, Jiang Q, Hui Z (2013) GmNFYA3, a target gene of miR169, is a positive regulator of plant tolerance to drought stress. Plant Mol Biol 82:113–129CrossRefGoogle Scholar
  34. Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, Rd HB, Mantovani R (2012) The promiscuous life of plant NUCLEAR FACTOR Y transcription factors. Plant Cell 24:4777–4792CrossRefGoogle Scholar
  35. Porri A, Torti S, Romera-Branchat M, Coupland G (2012) Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Dev 139: 2198–2209CrossRefGoogle Scholar
  36. Putterill, Joanna, Robson, Frances, Lee, Karen, Simon, Rüdiger, Coupland, George (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847CrossRefGoogle Scholar
  37. Qu B, He X, Wang J, Zhao Y, Teng W, Shao A, Zhao X, Ma W, Wang J, Li B (2015) A wheat CCAAT-box binding transcription factor increases grain yield of wheat with less fertilizer input. Plant Physiol 167:411–423CrossRefGoogle Scholar
  38. Rédei GP (1962) Supervital Mutants of Arabidopsis. Genet 47:443Google Scholar
  39. Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Dev 125:1609Google Scholar
  40. Ratcliffe OJ, Bradley DJ, Coen ES (1999) Separation of shoot and floral identity in Arabidopsis. Dev 126:1109–1120Google Scholar
  41. Reeves PH, Coupland G (2001) Analysis of flowering time control in Arabidopsis by comparison of double and triple mutants. Plant Physiol 126:1085–1091CrossRefGoogle Scholar
  42. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarzsommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616CrossRefGoogle Scholar
  43. Shen B, Allen WB, Zheng PZ, Li CJ, Glassman K, Ranch J, Nubel D, Tarczynski MC (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 153:980CrossRefGoogle Scholar
  44. Simon R, Igeño MI, Coupland G (1996) Activation of floral meristem identity genes in Arabidopsis. Nature 384:59–62CrossRefGoogle Scholar
  45. Simpson GG, Dean C (2002) Arabidopsis, the rosetta stone of flowering time?. Science 296:285–289CrossRefGoogle Scholar
  46. Stephenson TJ, Mcintyre CL, Collet C, Xue GP (2011) TaNF-YB3 is involved in the regulation of photosynthesis genes in Triticum aestivum. Funct Integr Genomic 11:327CrossRefGoogle Scholar
  47. Suárezlópez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410: 1116CrossRefGoogle Scholar
  48. Wang CQ, Guthrie C, Sarmast MK, Dehesh K (2014) BBX19 interacts with CONSTANS to repress FLOWERING LOCUS T transcription, defining a flowering time checkpoint in Arabidopsis. Plant Cell 26:3589CrossRefGoogle Scholar
  49. Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738CrossRefGoogle Scholar
  50. Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438CrossRefGoogle Scholar
  51. Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H, Wan J (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758CrossRefGoogle Scholar
  52. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859CrossRefGoogle Scholar
  53. Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500CrossRefGoogle Scholar
  54. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis Thaliana by mir156 and its target SPL3. Dev 133:3539–3547CrossRefGoogle Scholar
  55. Yadav D, Shavrukov Y, Bazanova N, Chirkova L, Borisjuk N, Kovalchuk N, Ismagul A, Parent B, Langridge P, Hrmova M (2015) Constitutive overexpression of the TaNF-YB4 gene in transgenic wheat significantly improves grain yield. J Exp Bot 66:6635CrossRefGoogle Scholar
  56. Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner, Doris (2009) The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17:268–278CrossRefGoogle Scholar
  57. Yamaguchi N, Winter CM, Wu MF, Kanno Y, Yamaguchi A, Seo M, Wagner D (2014) Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 344: 638CrossRefGoogle Scholar
  58. Yu S, Galvão VC, Zhang YC, Horrer D, Zhang TQ, Hao YH, Feng YQ, Wang S, Schmid M, Wang JW (2012) Gibberellin regulates the Arabidopsis floral transition through mir156-targeted SQUAMOSA PROMOTER BINDING-LIKE transcription factors. Plant Cell 24:3320–3332CrossRefGoogle Scholar
  59. Zhang Z, Li X, Zhang C, Zou H, Wu Z (2016) Isolation, structural analysis, and expression characteristics of the maize nuclear factor Y gene families. Biochem Bioph Res Co., 478:752–758CrossRefGoogle Scholar
  60. Zhu S, Wang J, Cai M, Zhang H, Wu F, Xu Y, Li C, Cheng Z, Zhang X, Guo X (2017) The OsHAPL1-DTH8-Hd1 complex functions as the transcription regulator to repress heading date in rice. J Exp Bot 68:553–568Google Scholar

Copyright information

© Korean Society of Plant Biologists and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Xiupeng Mei
    • 1
  • Ping Li
    • 1
  • Lu Wang
    • 1
  • Chaoxian Liu
    • 1
  • Lian Zhou
    • 1
  • Yilin Cai
    • 1
    Email author
  1. 1.College of Agronomy and BiotechnologySouthwest UniversityChongqingPeople’s Republic of China

Personalised recommendations