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Control of Flowering in Strawberries

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Part of the book series: Compendium of Plant Genomes ((CPG))

Abstract

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.

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References

  • 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 309:1052–1056

    Article  CAS  PubMed  Google Scholar 

  • Albani MC, Coupland G (2010) Comparative analysis of flowering in annual and perennial plants. Curr Top Dev Biol 91:323–348

    Article  CAS  PubMed  Google Scholar 

  • Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639

    Article  CAS  PubMed  Google Scholar 

  • 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 111–131

    Google Scholar 

  • 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 4:495–507

    Article  Google Scholar 

  • 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 312:1040–1043

    Article  CAS  PubMed  Google Scholar 

  • 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–D1171

    Article  CAS  PubMed  Google Scholar 

  • Bradford E, Hancock JF, Warner RM (2010) Interactions of temperature and photoperiod determine expression of repeat flowering in strawberry. J Amer Soc Hort Sci 135:102–107

    Google Scholar 

  • Brown T, Wareing PF (1965) The genetical control of the everbearing habit and three other characters in varieties of Fragaria vesca. Euphytica 14:97–112

    Google Scholar 

  • 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 127:901–907

    Google Scholar 

  • Castro P, Bushakra JM, Stewart P et al (2015) Genetic mapping of day-neutrality in cultivated strawberry. Mol Breed 35:79

    Article  CAS  Google Scholar 

  • Corbesier L, Vincent C, Jang S et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033

    Article  CAS  PubMed  Google Scholar 

  • Dale A, Luby JJ, Hancock JF (2002) Breeding dayneutral strawberries for Northern North America. Acta Hort 567:133–136

    Article  Google Scholar 

  • Darrow GM (1966) The strawberry. Holt, Rinehart and Winston, NY, USA

    Google Scholar 

  • Darrow GM, Waldo GF (1934) Responses of strawberry varieties and species to duration of the daily light period. US Dept Agr Tech Bull 453

    Google Scholar 

  • 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 109:396–400

    Google Scholar 

  • Flachowsky H, Szankowski I, Waidmann S et al (2012) The MdTFL1 of apple (Malus × domestica Borkh.) reduces vegetative growth and generation time. Tree Physiol 32:1288–1301

    Article  CAS  PubMed  Google Scholar 

  • 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 235:1239–1251

    Article  CAS  PubMed  Google Scholar 

  • 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 64:1837–1848

    Article  CAS  PubMed  Google Scholar 

  • Guttridge CG (1985) Fragaria × ananassa. In: Halevy A (ed) CRC handbook of flowering, vol III. CRC Press Inc., Boca Raton, FL, pp 16–33

    Google Scholar 

  • Guttridge CG, Thompson PA (1964) The Effect of Gibberellins on Growth and Flowering of Fragaria and Duchesnea. J Exp Bot 15(3):631–646

    Article  CAS  Google Scholar 

  • 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):161–173

    Article  CAS  PubMed  Google Scholar 

  • Hanano S, Goto K (2011) Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional regulation. Plant Cell 23:3172–3184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayama R, Yokoi S, Tamaki S et al (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722

    Article  CAS  PubMed  Google Scholar 

  • Heide OM (1977) Photoperiod and temperature interactions in growth and flowering of strawberry. Physiol Plant 40:21–26

    Article  Google Scholar 

  • 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 130:280–289

    Article  CAS  Google Scholar 

  • Hempel FD, Weigel D, Mandel MA et al (1997) Floral determination and expression of floral regulatory genes in Arabidopsis. Development 124:3845–3853

    PubMed  CAS  Google Scholar 

  • Ho WWH, Weigel D (2014) Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T. Plant Cell 26:552–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 209:291–303

    Article  Google Scholar 

  • 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, UK

    Google Scholar 

  • 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 9:18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 79:466–471

    Article  Google Scholar 

  • 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 69:116–125

    Article  CAS  PubMed  Google Scholar 

  • Jonkers H (1965) On the flower formation, the dormancy and the early forcing of strawberries. Mededlingen Landbouwhogeschool Wageningen 65:1–71

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66

    Article  CAS  PubMed  Google Scholar 

  • 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 159:1043–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1111/pbi.12545

    Article  Google Scholar 

  • 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):74–81

    CAS  Google Scholar 

  • Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147

    Article  CAS  PubMed  Google Scholar 

  • Kumar SV, Lucyshyn D, Jaeger KE et al (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):786–795

    Article  Google Scholar 

  • Lee JH, Ruy HS, Chung KS et al (2013) Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342:628–632

    Article  CAS  PubMed  Google Scholar 

  • 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 193:67–80

    Article  CAS  PubMed  Google Scholar 

  • 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 60:3521–3530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lieten F (1997) Effects of chilling and night-break treatment on greenhouse production of ‘Elsanta’. Acta Hort 439:633–640

    Article  Google Scholar 

  • 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 19:1488–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Liu C, Hou X et al (2012) FTIP1 Is an Essential Regulator Required for Florigen Transport. PLoS Biol 10(4):e1001313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manakasem Y, Goodwin PB (2001) Responses of dayneutral and Junebearing strawberries to temperature and daylength. J Hort Sci Biotech 76:629–635

    Google Scholar 

  • 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):394–412

    Article  CAS  PubMed  Google Scholar 

  • Mouhu K, Hytönen T, Folta K et al (2009) Identification of flowering genes in strawberry, a perennial SD plant. BMC Plant Biol 9:122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 25:3296–3310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 58:641–648

    Article  CAS  Google Scholar 

  • 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 64:909–920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 177:60–66

    Article  CAS  PubMed  Google Scholar 

  • 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 58:3915–3927

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama M, Kanahama K (2002) Effects of temperature and photoperiod on flower bud initiation of day-neutral and everbearing strawberries. Acta Hort 567:253–255

    Article  Google Scholar 

  • 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 67:239–257

    Article  CAS  PubMed  Google Scholar 

  • 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 14:2176–2189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1093/jxb/erw326

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 13:2687–2701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Posé D, Verhage L, Ott F et al (2013) Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503:414–417

    Article  CAS  PubMed  Google Scholar 

  • 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):847–857

    Article  CAS  PubMed  Google Scholar 

  • 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 202:161–173

    Article  CAS  PubMed  Google Scholar 

  • 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 5:271

    Article  PubMed  PubMed Central  Google Scholar 

  • Rantanen M, Kurokura T, Jiang P et al (2015) Strawberry homologue of TERMINAL FLOWER1 integrates photoperiod and temperature signals to inhibit flowering. Plant J 82:163–173

    Article  CAS  PubMed  Google Scholar 

  • 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 33:654–667

    Article  CAS  PubMed  Google Scholar 

  • 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 38:1157–1166

    Article  CAS  Google Scholar 

  • Samach A, Onouchi H, Gold SE et al (2000) Distinct roles of CONSTANS target genes in reproductive development in Arabidopsis. Science 288:1613–1616

    Article  CAS  PubMed  Google Scholar 

  • 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):261–265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):167–177

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shulaev V, Sargent DJ, Crowhurst RN et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116

    Article  CAS  PubMed  Google Scholar 

  • Sønsteby A, Heide OM (2006) Dormancy relations and flowering of the strawberry cultivars Korona and Elsanta as influenced by photoperiod and temperature. Scientia Hort 110:57–67

    Article  Google Scholar 

  • Sønsteby A, Heide OM (2007) Long-day control of flowering in everbearing strawberries. J Hort Sci Biotech 82:875–884

    Article  Google Scholar 

  • 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 83:360–366

    Article  Google Scholar 

  • Sønsteby A, Heide OM (2008b) Flowering physiology of populations of Fragaria virginiana. J Hort Sci Biotech 83:641–647

    Article  Google Scholar 

  • 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):42–48

    Google Scholar 

  • Sønsteby A, Nes A (1998) Short days and temperature effects on growth and flowering in strawberry (Fragaria x ananassa Duch.). J Hort Sci Biotech 73:730–736

    Article  Google Scholar 

  • Teper-Bamnolker P, Samach S (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17:2661–2675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson PA, Guttridge CG (1959) Effect of Gibberellic Acid on the Initiation of Flowers and Runners in the Strawberry. Nature 184(4688):BA72–BA73

    Article  Google Scholar 

  • 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):57–66

    Article  CAS  PubMed  Google Scholar 

  • 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 232:1309–1324

    Article  CAS  PubMed  Google Scholar 

  • 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 112:200–206

    Article  Google Scholar 

  • Wigge PA, Kim MC, Jaeger KE et al (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Blechl A et al (2004) The Wheat VRN2 Gene Is a Flowering Repressor Down-Regulated by Vernalization. Science 303(5664):1640–1644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeung K, Seitz T, Li S et al (1999) Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 401(6749):173–177

    Article  CAS  PubMed  Google Scholar 

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Koskela, E.A., Hytönen, T. (2018). Control of Flowering in Strawberries. In: Hytönen, T., Graham, J., Harrison, R. (eds) The Genomes of Rosaceous Berries and Their Wild Relatives. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-319-76020-9_4

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