Genes for Bolting and Flowering

  • Hiroyasu Kitashiba
  • Shuji YokoiEmail author
Part of the Compendium of Plant Genomes book series (CPG)


Floral transition which initiates bolting and flowering is induced in flowering plants by environmental factors such as low temperature and photoperiod and by endogenous factors such as growing stage and Phytohormone. The molecular mechanism in the floral transition has attracted considerable interest, and, in particular, agronomic application by genetic and physiological control of bolting and flowering times has been the subject of many researchers and breeders seeking to develop cultivars efficiently. Study of the floral transition has been remarkably advanced in Arabidopsis thaliana as a model plant using a variety of genomic resources such as various ecotypes and information on genome sequences and mutant lines. Four major flowering pathways in Arabidopsis have been found, and gene networks in these pathways have been revealed in the past about 20 years. Based on studies in Arabidopsis, genetic studies on bolting and flowering times have been conducted in Brassica species such as Brassica rapa and Brassica oleracea. Following these studies, high-density genetic maps and genome sequences have been recently published in radish (Raphanus sativus L.), and several studies to identify genetic factors or loci associated with bolting and flowering times have also been attempted. Here, we review genetic studies on bolting and flowering in Arabidopsis and Brassica species and then introduce recent studies in radish together with results of our current attempts.


Bolting Flowering Floral transition Genetic mechanisms QTLs Radish Raphanus 


  1. Achard P, Baghour M, Chapple A, Hedden P, Straeten DVD, Genschik P, Moritz T, Harberd NP (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc Natl Acad Sci USA 104:6484–6489CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ajisaka H, Kuginuki Y, Yui S, Enomoto S, Hirai M (2001) Identification and mapping of a quantitative trait locus controlling extreme late bolting in Chinese cabbage (Brassica rapa L. ssp. pekinensis syn. campestris L.) using bulked segregant analysis. Euphytica 118:75–81CrossRefGoogle Scholar
  3. Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36:162–166CrossRefPubMedGoogle Scholar
  4. Bond DM, Dennis ES, Pogson BJ, Finnegan EJ (2009) Histone acetylation, VERNALIZATION INSENSITIVE 3, FLOWERING LOCUS C, and the vernalization response. Mol Plant 2:724–737CrossRefPubMedGoogle Scholar
  5. Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064CrossRefPubMedGoogle Scholar
  6. Curtis IS, Nam HG, Yun JY, Seo KH (2002) Expression of an antisense GIGANTEA (GI) gene fragment in transgenic radish causes delayed bolting and flowering. Transgenic Res 11:249–256CrossRefPubMedGoogle Scholar
  7. Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 132:1107–1114CrossRefPubMedPubMedCentralGoogle Scholar
  8. Gocal GFW, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP, Li SF, Parish RW, Dennis ES, Weigel D, King RW (2001) GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol 127:1682–1693CrossRefPubMedPubMedCentralGoogle Scholar
  9. Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol 6:13–19CrossRefPubMedGoogle Scholar
  10. Hepworth S, Valverde F, Ravenscroft D, Mouradov A, Coupland G (2002) Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J 21:4327–4337CrossRefPubMedPubMedCentralGoogle Scholar
  11. Huq E, Tepperman JM, Quail PH (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc Natl Acad Sci USA 97:9789–9794CrossRefPubMedPubMedCentralGoogle Scholar
  12. Huang H, Nusinow DA (2016) Into the evening: Complex interactions in the Arabidopsis circadian clock. Trends Genet 32:674–686CrossRefPubMedGoogle Scholar
  13. Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16(Suppl):S1–17CrossRefPubMedPubMedCentralGoogle Scholar
  14. Jeong YM, Kim N, Ahn BO, Oh M, Chung WH, Chung H, Jeong S, Lim KB, Hwang YJ, Kim GB, Baek S, Choi SB, Hyung DJ, Lee SW, Sohn SH, Kwon SJ, Jin M, Seol YJ, Chae WB, Choi KJ, Park BS, Yu HJ, Mun JH (2016) Elucidating the triplicated ancestral genome structure of radish based on chromosome-level comparison with the Brassica genomes. Theor Appl Genet 129:1357–1372CrossRefPubMedGoogle Scholar
  15. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344–347CrossRefPubMedGoogle Scholar
  16. Jung WY, Park HJ, Lee A, Lee SS, Kim YS, Cho HS (2016) Identification of flowering-related genes responsible for differences in bolting time between two radish inbred lines. Front Plant Sci 7:1844CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kitamoto N, Yui S, Nishikawa K, Takahata Y, Yokoi S (2014) A naturally occurring long insertion in the first intron in the Brassica rapa FLC2 gene causes delayed bolting. Euphytica 196:213–223CrossRefGoogle Scholar
  18. Kitashiba H, Li F, Hirakawa H, Kawanabe T, Zou Z, Hasegawa Y, Tonosaki K, Shirasawa S, Fukushima A, Yokoi S, Takahata Y, Kakizaki T, Ishida M, Okamoto S, Sakamoto K, Shirasawa K, Tabata S, Nishio T (2014) Draft sequences of the radish (Raphanus sativus L.) genome. DNA Res 21:481–490CrossRefPubMedPubMedCentralGoogle Scholar
  19. Lee I, Aukerman MJ, Gore SL, Lohman KN, Michaels SD, Weaver LM, John MC, Feldmann KA, Amasino RM (1994) Isolation of LUMINIDEPENDENS-A gene involved in the control of flowering time in Arabidopsis. Plant Cell 6:75–83CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lee J, Oh M, Park H, Lee I (2008) SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J 55:832–843CrossRefPubMedGoogle Scholar
  21. Li F, Hasegawa Y, Saito M, Shirasawa S, Fukushima A, Ito T, Fujii H, Kishitani S, Kitashiba H, Nishio T (2011) Extensive chromosome homoeology among Brassiceae species were revealed by comparative genetic mapping with high-density EST-based SNP markers in radish (Raphanus sativus L.). DNA Res 18:401–411CrossRefPubMedPubMedCentralGoogle Scholar
  22. Li F, Kitashiba H, Inaba K, Nishio T (2009) A Brassica rapa linkage map of EST-based SNP markers for identification of candidate genes controlling flowering time and leaf morphological traits. DNA Res 16:311–323CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lim MH, Kim J, Kim YS, Chung KS, Seo YH, Lee I, Kim J, Hong CB, Kim HJ, Park CM (2004) A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16:731–740. doi: 10.1105/tpc.019331 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lin C (2000) Plant blue-light receptors. Trends Plant Sci 5:337–342CrossRefPubMedGoogle Scholar
  25. Liu C, Chen H, Er HL, Soo HM, Kumar PP, Han JH, Liou YC, Yu H (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135:1481–1491CrossRefPubMedGoogle Scholar
  26. Lou P, Zhao J, Kim JS, Shen S, Del Carpio DP, Song X, Jin M, Vreugdenhil D, Wang X, Koornneef M, Bonnema G (2007) Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa. J Exp Bot 58:4005–4016CrossRefPubMedGoogle Scholar
  27. Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love L, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89:737–745CrossRefPubMedGoogle Scholar
  28. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956CrossRefPubMedPubMedCentralGoogle Scholar
  29. Michaels SD, Amasino RM (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13:935–941CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mockler T, Yang H, Yu X, Parikh D, Cheng Y-C, Dolan S, Lin C (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc Natl Acad Sci USA 100:2140–2145CrossRefPubMedPubMedCentralGoogle Scholar
  31. Moon J, Lee H, Kim M, Lee I (2005) Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol 46:292–299CrossRefPubMedGoogle Scholar
  32. Mouradov A, Cremer FDR, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14:S111–S130PubMedPubMedCentralGoogle Scholar
  33. Nie S, Li C, Xu L, Wang Y, Huang D, Muleke EM, Sun X, Xie Y, Liu L (2016) De novo transcriptome analysis in radish (Raphanus sativus L.) and identification of critical genes involved in bolting and flowering. BMC Gen 17: 389Google Scholar
  34. Nie S, Xu L, Wang Y, Huang D, Muleke EM, Sun X, Wang R, Xie Y, Gong Y, Liu L (2015) Identification of bolting-related microRNAs and their targets reveals complex miRNA-mediated flowering-time regulatory networks in radish (Raphanus sativus L.). Sci Rep 5: 14034Google Scholar
  35. Nishioka M, Tamura J, Hayashi M, Fujimori Y, Ohkawa Y, Kuginuki Y, Harada K (2005) Mapping of QTLs for bolting time in Brassica rapa (syn. campestris) under different environmental conditions. Breed Sci 55:127–133CrossRefGoogle Scholar
  36. Okazaki K, Sakamoto K, Kikuchi R, Saito A, Togashi E, Kuginuki Y, Matsumoto S, Hirai M (2007) Mapping and characterization of FLC homologs and QTL analysis of flowering time in Brassica oleracea. Theor Appl Genet 114:595–608CrossRefPubMedGoogle Scholar
  37. Provart NJ, Alonso J, Assmann SM, Bergmann D, Brady SM, Brkljacic J, Browse J, Chapple C, Colot V, Cutler S, Dangl J, Ehrhardt D, Friesner JD, Frommer WB, Grotewold E, Meyerowitz E, Nemhauser J, Nordborg M, Pikaard C, Shanklin J, Somerville C, Stitt M, Torii KU, Waese J, Wagner D, McCourt P (2016) 50 years of Arabidopsis research: highlights and future directions. New Phytol 209:921–944CrossRefPubMedGoogle Scholar
  38. Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–857CrossRefPubMedGoogle Scholar
  39. Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93CrossRefPubMedGoogle Scholar
  40. Redei GP (1975) Arabidopsis as a genetic tool. Ann Rev Gen 9:111–127CrossRefGoogle Scholar
  41. Sanda SL, Amasino RM (1996) Ecotype-specific expression of a flowering mutant phenotype in Arabidopsis thaliana. Plant Physiol 111:641–644CrossRefPubMedPubMedCentralGoogle Scholar
  42. Schomburg FM, Patton DA, Meinke DW, Amasino RM (2001) FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13:1427–1436CrossRefPubMedPubMedCentralGoogle Scholar
  43. Schranz ME, Quijada P, Sung S-B, Lukens L, Amasino R, Osborn TC (2002) Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162:1457–1468PubMedPubMedCentralGoogle Scholar
  44. Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA 97:3753–3758CrossRefPubMedPubMedCentralGoogle Scholar
  45. Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296:285–289CrossRefPubMedGoogle Scholar
  46. Simpson GG, Dijkwel PP, Quesada V, Henderson I, Dean C (2003) FY is an RNA 3′ end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113:777–787CrossRefPubMedGoogle Scholar
  47. Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2016) Photoperiodic flowering: time measurement mechanisms in leaves. Ann Rev Plant Biol 66:441–464CrossRefGoogle Scholar
  48. Soppe W, Bentsink L, Koornneef M (1999) The early-flowering mutant efs is involved in the autonomous promotion pathway of Arabidopsis thaliana. Development 126:4763–4770PubMedGoogle Scholar
  49. Wang J, Lydiate DJ, Parkin IA, Falentin C, Delourme R, Carion PW, King GJ (2011) Integration of linkage maps for the Amphidiploid Brassica napus and comparative mapping with Arabidopsis and Brassica rapa. BMC Gen 12:101CrossRefGoogle Scholar
  50. Xu L, Hu K, Zhang Z, Guan C, Chen S, Hua W, Li J, Wen J, Yi B, Shen J, Ma C, Tu J, Fu T (2016) Genome-wide association study reveals the genetic architecture of flowering time in rapeseed (Brassica napus L.). DNA Res 23:43–52PubMedGoogle Scholar
  51. Yanovsky MJ, Kay SA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419:308–312CrossRefPubMedGoogle Scholar
  52. Yi G, Park H, Kim JS, Chae WB, Park S, Huh JH (2014) Identification of three FLOWERING LOCUS C genes responsible for vernalization response in radish (Raphanus sativus L.). Hort Environ Biotechnol 55:548–556CrossRefGoogle Scholar
  53. Zhao J, Kulkarni V, Liu N, Del Carpio DP, Bucher J, Bonnema G (2010) BrFLC2 (FLOWERING LOCUS C) as a candidate gene for a vernalization response QTL in Brassica rapa. J Exp Bot 61:1817–1825CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zou X, Suppanz I, Raman H, Hou J, Wang J, Long Y, Jung C, Meng J (2012) Comparative analysis of FLC homologues in Brassicaceae provides insight into their role in the evolution of oilseed rape. PLoS One 7:e45751CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan
  2. 2.Graduate School of Life and Environmental SciencesOsaka Prefecture UniversityNaka-ku, SakaiJapan

Personalised recommendations