Control of Flowering in Strawberries

  • Elli A. Koskela
  • Timo HytönenEmail author
Part of the Compendium of Plant Genomes book series (CPG)


Strawberries (Fragaria sp.) are small perennial plants capable of both sexual reproduction through seeds and clonal reproduction via runners. Because vegetative and generative developmental programs are tightly connected, the control of flowering is presented here in the context of the yearly growth cycle. The rosette crown of strawberry consists of a stem with short internodes produced from the apical meristem. Each node harbors one trifoliate leaf and an axillary bud. The fate of axillary buds is dictated by environmental conditions; high temperatures and long days (LDs) promote axillary bud development into runners, whereas cool temperature and short days (SDs) favor the formation of branch crowns. SDs and cool temperature also promote flowering; under these conditions, the main shoot apical meristem is converted into a terminal inflorescence, and vegetative growth is continued from the uppermost axillary branch crown. The environmental factors that regulate vegetative and generative development in strawberries have been reasonably well characterized and are reviewed in the first two chapters. The genetic basis of the physiological responses in strawberries is much less clear. To provide a point of reference for the flowering pathways described in strawberries so far, a short review on the molecular mechanisms controlling flowering in the model plant Arabidopsis is given. The last two chapters will then describe the current knowledge on the molecular mechanisms controlling the physiological responses in strawberries.


  1. Abe M, Kobayashi Y, Yamamoto S et al (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056CrossRefPubMedGoogle Scholar
  2. Albani MC, Coupland G (2010) Comparative analysis of flowering in annual and perennial plants. Curr Top Dev Biol 91:323–348CrossRefPubMedGoogle Scholar
  3. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639CrossRefPubMedGoogle Scholar
  4. Battey NH, Le Miére P, Tehranifar A et al (1998) Genetic and environmental control of flowering in strawberry. In: Cockshull KE, Gray D, Seymour GB, Thomas B (eds) Genetic and environmental manipulation of horticultural crops. CABI Publishing, Wallingford, UK, pp 111–131Google Scholar
  5. Bielenberg DG, Wang YE, Li Z et al (2008) Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes 4:495–507CrossRefGoogle Scholar
  6. Böhlenius H, Huang T, Charbonnel-Campaa L et al (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043CrossRefPubMedGoogle Scholar
  7. Bouché F, Lobet G, Tocquin P et al (2016) FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucl Acids Res 44(D1):D1167–D1171CrossRefPubMedGoogle Scholar
  8. Bradford E, Hancock JF, Warner RM (2010) Interactions of temperature and photoperiod determine expression of repeat flowering in strawberry. J Amer Soc Hort Sci 135:102–107Google Scholar
  9. Brown T, Wareing PF (1965) The genetical control of the everbearing habit and three other characters in varieties of Fragaria vesca. Euphytica 14:97–112Google Scholar
  10. Camacaro PME, Camacaro GJ, Hadley P et al (2002) Pattern of growth and development of the strawberry cultivars Elsanta, Bolero, and Everest. J Amer Soc Hort Sci 127:901–907Google Scholar
  11. Castro P, Bushakra JM, Stewart P et al (2015) Genetic mapping of day-neutrality in cultivated strawberry. Mol Breed 35:79CrossRefGoogle Scholar
  12. Corbesier L, Vincent C, Jang S et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033CrossRefPubMedGoogle Scholar
  13. Dale A, Luby JJ, Hancock JF (2002) Breeding dayneutral strawberries for Northern North America. Acta Hort 567:133–136CrossRefGoogle Scholar
  14. Darrow GM (1966) The strawberry. Holt, Rinehart and Winston, NY, USAGoogle Scholar
  15. Darrow GM, Waldo GF (1934) Responses of strawberry varieties and species to duration of the daily light period. US Dept Agr Tech Bull 453Google Scholar
  16. Durner EF, Barden JA, Himelrick DG et al (1984) Photoperiod and temperature effects on flower and runner development in day-neutral, Junebearing and everbearing strawberries. J Am Soc Hort Sci 109:396–400Google Scholar
  17. Flachowsky H, Szankowski I, Waidmann S et al (2012) The MdTFL1 of apple (Malus × domestica Borkh.) reduces vegetative growth and generation time. Tree Physiol 32:1288–1301CrossRefPubMedGoogle Scholar
  18. Freiman A, Shlizerman L et al (2012) Development of a transgenic early flowering pear (Pyrus communis L.) genotype by RNAi silencing of PcTFL1-1 and PcTFL1-2. Planta 235:1239–1251CrossRefPubMedGoogle Scholar
  19. Gaston A, Perrotte J, Lercetau-Köhler E et al (2013) PFRU, a single dominant locus regulates the balance between sexual and asexual plant reproduction in cultivated strawberry. J Exp Bot 64:1837–1848CrossRefPubMedGoogle Scholar
  20. Guttridge CG (1985) Fragaria × ananassa. In: Halevy A (ed) CRC handbook of flowering, vol III. CRC Press Inc., Boca Raton, FL, pp 16–33Google Scholar
  21. Guttridge CG, Thompson PA (1964) The Effect of Gibberellins on Growth and Flowering of Fragaria and Duchesnea. J Exp Bot 15(3):631–646CrossRefGoogle Scholar
  22. Haberman A, Ackerman M, Crane O et al (2016) Different flowering response to various fruit loads in apple cultivars correlates with degree of transcript reaccumulation of a TFL1-encoding gene. Plant J 87(2):161–173CrossRefPubMedGoogle Scholar
  23. Hanano S, Goto K (2011) Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional regulation. Plant Cell 23:3172–3184CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hayama R, Yokoi S, Tamaki S et al (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722CrossRefPubMedGoogle Scholar
  25. Heide OM (1977) Photoperiod and temperature interactions in growth and flowering of strawberry. Physiol Plant 40:21–26CrossRefGoogle Scholar
  26. Heide OM, Sønsteby A (2007) Interactions of temperature and photoperiod in the control of flowering of latitudinal and altitudinal populations of wild strawberry (Fragaria vesca). Physiol Plant 130:280–289CrossRefGoogle Scholar
  27. Hempel FD, Weigel D, Mandel MA et al (1997) Floral determination and expression of floral regulatory genes in Arabidopsis. Development 124:3845–3853PubMedGoogle Scholar
  28. Ho WWH, Weigel D (2014) Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T. Plant Cell 26:552–564CrossRefPubMedPubMedCentralGoogle Scholar
  29. Honjo M, Nunome T, Kataoka S et al (2015) Simple sequence repeat markers linked to the everbearing flowering gene in long-day and day-neutral cultivars of the octoploid cultivated strawberry Fragariaxananassa. Euphytica 209:291–303CrossRefGoogle Scholar
  30. Hytönen T, Elomaa P (2011) Genetic and Environmental Regulation of Flowering and Runnering in Strawberry. In: Husaini AM & Mercado JA (Eds). Genomics, Transgenics, Molecular Breeding and Biotechnology of Strawberry. Global Science Books, UKGoogle Scholar
  31. Hytönen T, Elomaa P, Moritz T et al (2009) Gibberellin mediates daylength-controlled differentiation of vegetative meristems in strawberry (Fragaria × ananassa Duch). BMC Plant Biol 9:18CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hytönen T, Palonen P, Mouhu K et al (2004) Crown branching and cropping potential in strawberry (Fragaria × ananassa Duch.) can be enhanced by daylength treatments. J Hort Sci Biotech 79:466–471CrossRefGoogle Scholar
  33. Iwata H, Gaston A, Remay A et al (2012) The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J 69:116–125CrossRefPubMedGoogle Scholar
  34. Jonkers H (1965) On the flower formation, the dormancy and the early forcing of strawberries. Mededlingen Landbouwhogeschool Wageningen 65:1–71Google Scholar
  35. Kobayashi Y, Kaya H, Goto K et al (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962CrossRefPubMedGoogle Scholar
  36. Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66CrossRefPubMedGoogle Scholar
  37. Koskela EA, Mouhu K, Albani MC et al (2012) Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. Plant Physiol 159:1043–1054CrossRefPubMedPubMedCentralGoogle Scholar
  38. Koskela E, Sønsteby A, Flachowsky H et al (2016) TERMINAL FLOWER1 is a breeding target for a novel everbearing trait and tailored flowering responses in cultivated strawberry (Fragaria × ananassa Duch.). Plant. Biotech. Scholar
  39. Kotoda N, Iwanami H, Takahashi S, Abe K (2006) Antisense expression of MdTFL1, a TFL1-like gene, reduces the juvenile phase in apple. J Amer Soc Hort Sci 131(1):74–81Google Scholar
  40. Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147CrossRefPubMedGoogle Scholar
  41. Kumar SV, Lucyshyn D, Jaeger KE et al (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–246CrossRefPubMedPubMedCentralGoogle Scholar
  42. Le Miére P, Hadley P, Darby J et al (1998) The effect of thermal environment, planting date and crown size on growth, development and yield of Fragaria x ananassa Duch. cv. Elsanta. J Hort Sci Biotech 73(6):786–795CrossRefGoogle Scholar
  43. Lee JH, Ruy HS, Chung KS et al (2013) Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342:628–632CrossRefPubMedGoogle Scholar
  44. Leida C, Conesa A, Llácer G et al (2012) Histone modifications and expression of DAM6 gene in peach are modulated during bud dormancy release in a cultivar dependent manner. New Phytol 193:67–80CrossRefPubMedGoogle Scholar
  45. Li Z, Reighard GL, Abbott AG et al (2009) Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot 60:3521–3530CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lieten F (1997) Effects of chilling and night-break treatment on greenhouse production of ‘Elsanta’. Acta Hort 439:633–640CrossRefGoogle Scholar
  47. Lin MK, Belanger H, Lee YJ et al (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19:1488–1506CrossRefPubMedPubMedCentralGoogle Scholar
  48. Liu L, Liu C, Hou X et al (2012) FTIP1 Is an Essential Regulator Required for Florigen Transport. PLoS Biol 10(4):e1001313CrossRefPubMedPubMedCentralGoogle Scholar
  49. Manakasem Y, Goodwin PB (2001) Responses of dayneutral and Junebearing strawberries to temperature and daylength. J Hort Sci Biotech 76:629–635Google Scholar
  50. Mimida N, Kotoda N, Ueda T et al (2009) Four TFL1/CEN-like genes on distinct linkage groups show different expression patterns to regulate vegetative and reproductive development in apple (Malus × domestica Borkh.). Plant Cell Physiol 50(2):394–412CrossRefPubMedGoogle Scholar
  51. Mouhu K, Hytönen T, Folta K et al (2009) Identification of flowering genes in strawberry, a perennial SD plant. BMC Plant Biol 9:122CrossRefPubMedPubMedCentralGoogle Scholar
  52. Mouhu K, Kurokura T, Koskela EA et al (2013) The Fragaria vesca homolog of SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 represses flowering and promotes vegetative growth. Plant Cell 25:3296–3310CrossRefPubMedPubMedCentralGoogle Scholar
  53. Nakajima R, Otagaki S, Yamada K et al (2014) Molecular cloning and expression analyses of FaFT, FaTFL, and FaAP1 genes in cultivated strawberry: their correlation to flower bud formation. Biol Plant 58:641–648CrossRefGoogle Scholar
  54. Nakano Y, Higuchi Y, Sumimoto K et al (2013) Flowering retardation by high temperature in chrysanthemums: involvement of FLOWERING LOCUS T-LIKE 3 gene repression. J Exp Bot 64:909–920CrossRefPubMedPubMedCentralGoogle Scholar
  55. Nakano J, Higuchi Y, Yoshida Y et al (2015) Environmental responses of the FT/TFL1 gene family and their involvement in flower induction in Fragaria × ananassa. J Plant Physiol 177:60–66CrossRefPubMedGoogle Scholar
  56. Nishikawa F, Endo T, Shimada T et al (2007) Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.). J Exp Bot 58:3915–3927CrossRefPubMedGoogle Scholar
  57. Nishiyama M, Kanahama K (2002) Effects of temperature and photoperiod on flower bud initiation of day-neutral and everbearing strawberries. Acta Hort 567:253–255CrossRefGoogle Scholar
  58. Niu Q, Li J, Cai D et al (2016) Dormancy-associated MADS-box genes and microRNAs jointly control dormancy transition in pear (Pyrus pyrifolia white pear group) flower bud. J Exp Bot 67:239–257CrossRefPubMedGoogle Scholar
  59. Perrotte J, Gaston A, Potier A et al (2016a) Narrowing down the single homoeologous FaPFRU locus controlling flowering in cultivated octoploid strawberry using a selective mapping strategy. Plant Biotechnol J 14:2176–2189CrossRefPubMedPubMedCentralGoogle Scholar
  60. Perrotte J, Guédon Y, Gaston A et al (2016b) Identification of successive flowering phases highlights a new genetic control of the flowering pattern in strawberry. J Exp Bot. Scholar
  61. Pnueli L, Gutfinger T, Hareven D et al (2001) Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell 13:2687–2701CrossRefPubMedPubMedCentralGoogle Scholar
  62. Posé D, Verhage L, Ott F et al (2013) Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503:414–417CrossRefPubMedGoogle Scholar
  63. Putterill J, Robson F, Lee K et al (1995) The CONSTANS gene of arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80(6):847–857CrossRefPubMedGoogle Scholar
  64. Randoux M, Davière JM, Jeauffre J et al (2014) RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose. New Phytol 202:161–173CrossRefPubMedGoogle Scholar
  65. Rantanen M, Kurokura T, Mouhu K et al (2014) Light quality regulates flowering in FvFT1/FvTFL1 dependent manner in the woodland strawberry Fragaria vesca. Front Plant Sci 5:271CrossRefPubMedPubMedCentralGoogle Scholar
  66. Rantanen M, Kurokura T, Jiang P et al (2015) Strawberry homologue of TERMINAL FLOWER1 integrates photoperiod and temperature signals to inhibit flowering. Plant J 82:163–173CrossRefPubMedGoogle Scholar
  67. Saito T, Bai S, Ito A et al (2013) Expression and genomic structure of the dormancy-associated MADS box genes MADS13 in Japanese pears (Pyrus pyrifolia Nakai) that differ in their chilling requirement for dormancy release. Tree Physiol 33:654–667CrossRefPubMedGoogle Scholar
  68. Saito T, Bai S, Imai T et al (2015) Histone modification and signalling cascade of the dormancy-associated MADS-box gene, PpMADS13-1, in Japanese pear (Pyrus pyrifolia) during endodormancy. Plant Cell Env 38:1157–1166CrossRefGoogle Scholar
  69. Samach A, Onouchi H, Gold SE et al (2000) Distinct roles of CONSTANS target genes in reproductive development in Arabidopsis. Science 288:1613–1616CrossRefPubMedGoogle Scholar
  70. Sawa M, Nusinow DA, Kay SA et al (2007) FKF1 and GIGANTEA Complex Formation Is Required for Day-Length Measurement in Arabidopsis. Science 318(5848):261–265CrossRefPubMedPubMedCentralGoogle Scholar
  71. Serçe S, Hancock JF (2005) The temperature and photoperiod regulation of flowering and runnering in the strawberries, Fragaria chiloensis, F. virginiana, and F. x ananassa. Sci Hortic 103(2):167–177Google Scholar
  72. Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892CrossRefPubMedPubMedCentralGoogle Scholar
  73. Shulaev V, Sargent DJ, Crowhurst RN et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116CrossRefPubMedGoogle Scholar
  74. Sønsteby A, Heide OM (2006) Dormancy relations and flowering of the strawberry cultivars Korona and Elsanta as influenced by photoperiod and temperature. Scientia Hort 110:57–67CrossRefGoogle Scholar
  75. Sønsteby A, Heide OM (2007) Long-day control of flowering in everbearing strawberries. J Hort Sci Biotech 82:875–884CrossRefGoogle Scholar
  76. Sønsteby A, Heide OM (2008a) Long-day rather than autonomous control of flowering in the diploid everbearing strawberry Fragaria vesca ssp. semperflorens. J Hort Sci Biotech 83:360–366CrossRefGoogle Scholar
  77. Sønsteby A, Heide OM (2008b) Flowering physiology of populations of Fragaria virginiana. J Hort Sci Biotech 83:641–647CrossRefGoogle Scholar
  78. Sønsteby A, Heide OM (2011) Environmental regulation of dormancy and frost hardiness in Norwegian populations of wood strawberry (Fragaria vesca L.). Eur J Plant Sci Biotechn 5(1):42–48Google Scholar
  79. Sønsteby A, Nes A (1998) Short days and temperature effects on growth and flowering in strawberry (Fragaria x ananassa Duch.). J Hort Sci Biotech 73:730–736CrossRefGoogle Scholar
  80. Teper-Bamnolker P, Samach S (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17:2661–2675CrossRefPubMedPubMedCentralGoogle Scholar
  81. Thompson PA, Guttridge CG (1959) Effect of Gibberellic Acid on the Initiation of Flowers and Runners in the Strawberry. Nature 184(4688):BA72–BA73CrossRefGoogle Scholar
  82. Tiwari SB, Shen Y, Chang HC et al (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol 187(1):57–66CrossRefPubMedGoogle Scholar
  83. Tränkner C, Lehmann S, Hoenicka H et al (2010) Over-expression of an FT-homologous gene of apple induces early flowering in annual and perennial plants. Planta 232:1309–1324CrossRefPubMedGoogle Scholar
  84. Verheul MJ, Sønsteby A, Grimstad SO (2007) Influences of day and night temperatures on flowering of Fragaria x ananassa Duch., cvs. Korona and Elsanta, at different photoperiods. Sci Hort 112:200–206CrossRefGoogle Scholar
  85. Wigge PA, Kim MC, Jaeger KE et al (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059CrossRefPubMedGoogle Scholar
  86. Yan L, Loukoianov A, Blechl A et al (2004) The Wheat VRN2 Gene Is a Flowering Repressor Down-Regulated by Vernalization. Science 303(5664):1640–1644CrossRefPubMedPubMedCentralGoogle Scholar
  87. Yeung K, Seitz T, Li S et al (1999) Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 401(6749):173–177CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Agricultural SciencesUniversity of HelsinkiHelsinkiFinland
  2. 2.Rosaceae Genetics and GenomicsCentre for Research in Agricultural GenomicsCerdanyolaSpain

Personalised recommendations