Ecological Research

, Volume 32, Issue 4, pp 627–631 | Cite as

Relationship between seasonal progression of floral meristem development and FLOWERING LOCUS T expression in the deciduous tree Fagus crenata

  • Yuko Miyazaki
  • Akiko Satake
Note and Comment


Estimating the timing of flower bud formation in plants is essential to identify environmental factors that regulate floral transition. The presence of winter dormancy between the initiation of flowers and anthesis, characteristic of most trees in the temperate forests, hampers accurate estimation of the timing of floral transition. To overcome this difficulty, expression levels of flowering-time genes could be used as indicators of the timing of floral transition. Here, we evaluated the usefulness of molecular markers in estimating the timing of floral transition in Fagus crenata, a deciduous tree that shows intermittent and synchronized flowering at the population level. We selected FLOWERING LOCUS T (FT) as a candidate molecular marker and quantified the expression levels of its ortholog in F. crenata (FcFT). Subsequently, we analyzed the relationship between morphogenetic changes that occur between the vegetative state of the buds and the initiation of floral organs, and compared the FcFT expression levels in reproductive and vegetative buds, collected from spring to autumn. FcFT expression in leaves peaked at least two weeks before the morphological changes associated with flowering were visible in the buds in late July. FcFT expression levels were significantly higher in the reproductive buds than in the vegetative buds in July. These results suggest that the FcFT expression in July is a reliable indicator of the timing and occurrence of floral transition. This study highlights the utility of molecular tools in unraveling reproductive dynamics in plants, in combination with ecological and physiological approaches.


Development Flowering Gene expression Masting Shoot apical meristem 



We thank Hokkaido Research Center of Forestry and Forest Products Research Institute for permission to use their facilities, Y. Sano for advice in embedding samples, Y. Saburi and Y. Mori for their laboratory assistance, K. Kitamura for field assistance, and MJ Kobayashi for comments for manuscript. This study was funded by the Program to Disseminate Tenure Tracking System, MEXT, Japan (grant to YM) and JSPS KAKENHI (Grant Number 26251042 to AS).


  1. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013. doi: 10.1111/j.1365-313X.2010.04148.x CrossRefPubMedGoogle Scholar
  2. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639. doi: 10.1038/nrg3291 CrossRefPubMedGoogle Scholar
  3. Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664. doi: 10.1016/j.cell.2006.05.005 CrossRefPubMedGoogle Scholar
  4. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Nuller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622. doi: 10.1373/clinchem.2008.112797 CrossRefPubMedGoogle Scholar
  5. Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis thaliana. Cell 141:550, 550 e1–550 e2. doi:  10.1016/j.cell.2010.04.024
  6. Hokkaido Research Center FFPRI (2013) Meteorological data at the Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo, Japan. Available upon request at
  7. Hyun Y, Richter R, Coupland G (2017) Competence to flower: age-controlled sensitivity to environmental cues. Plant Physiol 173:36–46. doi: 10.1104/pp.16.01523 CrossRefPubMedGoogle Scholar
  8. 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. doi: 10.1126/science.286.5446.1962 CrossRefPubMedGoogle Scholar
  9. Kelly D (1994) The evolutionary ecology of mast seeding. Trends Ecol Evol 9:465–470. doi: 10.1016/0169-5347(94)90310-7 CrossRefPubMedGoogle Scholar
  10. Kelly D, Sork VL (2002) Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst 33:427–447. doi: 10.1146/annurev.ecolsys.33.020602.095433 CrossRefGoogle Scholar
  11. 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. doi: 10.1126/science.286.5446.1960 CrossRefPubMedGoogle Scholar
  12. Kobayashi MJ, Takeuchi Y, Kenta T, Kume T, Diway B, Shimizu KK (2013) Mass flowering of the tropical tree Shorea beccariana was preceded by expression changes in flowering and drought-responsive genes. Mol Ecol 22:4767–4782. doi: 10.1111/mec.12344 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kon H, Noda T, Terazawa K, Koyama H, Yasaka M (2005) Proximate factors causing mast seeding in Fagus crenata: the effects of resource level and weather cues. Can J Bot 83:1402–1409. doi: 10.1139/b05-120 CrossRefGoogle Scholar
  14. Krzymuski M, Andres F, Cagnola JI, Jang S, Yanovsky MJ, Coupland G, Casal JJ (2015) The dynamics of FLOWERING LOCUS T expression encodes long-day information. Plant J 83:952–961. doi: 10.1111/tpj.12938 CrossRefPubMedGoogle Scholar
  15. Kudoh H (2016) Molecular phenology in plants: in natura systems biology for the comprehensive understanding of seasonal responses under natural environments. New Phytol 210:399–412. doi: 10.1111/nph.13733 CrossRefPubMedGoogle Scholar
  16. Masaki T, Oka T, Osumi K, Suzuki W (2008) Geographical variation in climatic cues for mast seeding of Fagus crenata. Pop Ecol 50:357–366. doi: 10.1007/s10144-008-0104-6 CrossRefGoogle Scholar
  17. Miyazaki Y, Maruyama Y, Chiba Y, Kobayashi MJ, Joseph B, Shimizu KK, Mochida K, Hiura T, Kon H, Satake A (2014) Nitrogen as a key regulator of flowering in Fagus crenata: understanding the physiological mechanism of masting by gene expression analysis. Ecol Lett 17:1299–1309. doi: 10.1111/ele.12338 CrossRefPubMedGoogle Scholar
  18. Nishikawa F (2013) Regulation of floral induction in citrus. J Jpn Soc Hortic Sci 82:283–292. doi: 10.2503/jjshs1.82.283 CrossRefGoogle Scholar
  19. Ostfeld RS, Keesing F (2000) Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol Evol 15:232–237. doi: 10.1016/S0169-5347(00)01862-0 CrossRefPubMedGoogle Scholar
  20. Ostfeld RS, Jones CG, Wolff JO (1996) Of mice and mast: ecological connections in eastern deciduous forests. Bioscience 46:323–329. doi: 10.2307/1312946 CrossRefGoogle Scholar
  21. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:e45. doi: 10.1093/nar/29.9.e45 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Ruiz-García L, Madueno F, Wilkinson M, Haughn G, Salinas J, Martínez-Zapater JM (1997) Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell 9:1921–1934. doi: 10.1105/tpc.9.11.1921 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Satake A, Kawagoe T, Saburi Y, Chiba Y, Sakurai G, Kudoh H (2013) Forecasting flowering phenology under climate warming by modelling the regulatory dynamics of flowering-time genes. Nat Commun 4:2303–2311. doi: 10.1038/ncomms3303 CrossRefPubMedGoogle Scholar
  24. Simpson GG, Dean C (2002) Arabidopsis, the rosetta stone of flowering time? Science 296:285–289. doi: 10.1126/science.296.5566.285 CrossRefPubMedGoogle Scholar
  25. Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037. doi: 10.1007/s00018-011-0673-y CrossRefPubMedGoogle Scholar
  26. Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594. doi: 10.1146/annurev.arplant.59.032607.092755 CrossRefPubMedGoogle Scholar
  27. 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. doi: 10.1126/science.1114358 CrossRefPubMedGoogle Scholar
  28. Yasaka M, Takiya M, Watanabe I, Oono Y, Mizui N (2008) Variation in seed production among years and among individuals in 11 broadleaf tree species in northern Japan. J For Sci 13:83–88. doi: 10.1007/s10310-007-0052-6 Google Scholar

Copyright information

© The Ecological Society of Japan 2017

Authors and Affiliations

  1. 1.Graduate School of Environmental and Life ScienceOkayama UniversityOkayamaJapan
  2. 2.Department of Biology, Faculty of ScienceKyushu UniversityFukuokaJapan

Personalised recommendations