Skip to main content
Log in

Expression Profile of FaFT1 and Its Ectopic Expression in Arabidopsis Demonstrate Its Function in the Reproductive Development of Fragaria × ananassa

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

FT homologs are crucial for the flowering process, playing a vital role as ‘florigens’ in plants. In this study, we isolated and characterized an FT homolog, FaFT1, from cultivated strawberry. Nucleotide sequence analysis revealed a 531-bp open reading frame in FaFT1, encoding a putative protein with typical DPDxP and GxHR motifs belonging to the PEBP family proteins. For vegetative tissues or organs, qRT-PCR revealed that FaFT1 was primarily expressed in leaves. Notably high expression levels were detected in flowers and fruits, including the pith and cortex of the receptacle. Analysis of potential putative cis-acting regulatory elements (CREs) in this gene promoter indicated that many of them are associated with plant hormonal responses and abiotic stress responses. Expression detection confirmed that GA3 treatment enhanced the expression of FaFT1. When ectopically expressed in Arabidopsis, FaFT1 could promote the flowering process under SD conditions. These results suggested the possible role of FaFT1 in the regulation of reproductive development in cultivated strawberry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (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 

  • Ahmadi H, Bringhurst RS, Voth V (1990) Modes of inheritance of photoperiodism in Fragaria. J Am Soc Hortic Sci 115:146–152

    Article  Google Scholar 

  • Banfield MJ, Brady RL (2000) The structure of Antirrhinum centroradialis protein (CEN) suggests a role as a kinase regulator. J Mol Biol 297:1159–1170

    Article  CAS  PubMed  Google Scholar 

  • Bouché F, Lobet G, Tocquin P, Périlleux C (2016) FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Res 44:D1167–D1171

    Article  PubMed  Google Scholar 

  • Chang L, Zhang Z, Yang H, Li H, Dai H (2007) Detection of strawberry RNA and DNA viruses by RT-PCR using total nucleic acid as a template. J Phytopathol 155:431–436

    Article  CAS  Google Scholar 

  • Chaurasia AK, Patil HB, Krishna B, Subramaniam VR, Sane PV, Sane AP (2017) Flowering time in banana (Musa spp.), a day neutral plant, is controlled by at least three FLOWERING LOCUS T homologues. Sci Rep 7:5935

    Article  PubMed  PubMed Central  Google Scholar 

  • Choma ME, Himelrick DG (1984) Responses of day-neutral, June-bearing and everbearing strawberry cultivars to gibberellic acid and phthalimide treatments. Sci Hortic 22:257–264

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    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 transcription repression. Plant Cell 23:3172–3184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci USA 102:7748–7753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu CY, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM, Wickett N, Gunter LE, Tuskan GA, Brunner AM, Page GP, Barakat A, Carlson JE, DePamphilis CW, Luthe DS, Yuceer C (2011) FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci USA 108:10756–10761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwata H, Gaston A, Remay A, Thouroude T, Jeauffre J, Kawamura K, Oyant LH, Araki T, Denoyes B, Foucher F (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 

  • Kang C, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z (2013) Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. Plant Cell 25(6):1960–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klintenäs M, Pin PA, Benlloch R, Ingvarsson PK, Nilsson O (2012) Analysis of conifer FLOWERING LOCUS T/TERMINAL FLOWER1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage. New Phytol 196:1260–1273

    Article  PubMed  Google Scholar 

  • Koembuoy K, Nakajima R, Otagaki S, Kurokura T, Takahashi H, Nakazono M, Shiratake K, Matsumoto S (2017) Functional analyses of cultivated strawberry FT and TFL1 homologs. Acta Hortic 1156:95–102

    Article  Google Scholar 

  • Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774

    Article  CAS  PubMed  Google Scholar 

  • Koskela EA, Mouhu K, Albani MC, Kurokura T, Rantanen M, Sargent DJ, Battey NH, Coupland G, Elomaa P, Hytönen T (2012) Mutation in TERMINAL FLOWER 1 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 EA, Anita S, Flachowsky H, Heide OM, Magda-Viola H, Elomaa P, Hytönen T (2016) TERMINAL FLOWER1 is a breeding target for a novel everbearing trait and tailored flowering responses in cultivated strawberry (Fragaria × ananassa Duch.). Plant Biotechnol J 14:1852–1861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koskela EA, Kurokura T, Toivainen T, Sønsteby A, Heide OM, Sargent DJ, Isobe S, Jaakola L, Hilmarsson H, Elomaa P, Hytönen T (2017) Altered regulation of TERMINAL FLOWER 1 causes the unique vernalisation response in an arctic woodland strawberry accession. New Phytol 216:841–853

    Article  CAS  PubMed  Google Scholar 

  • Krzymuski M, Andrés 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

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurokura T, Samad S, Koskela E, Mouhu K, Hytönen T (2017) Fragaria vesca CONSTANS controls photoperiodic flowering and vegetative development. J Exp Bot 68:4839–4850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei H, Guo X, Wang Y, Yao L, Wang S, Li T (2015) Identification and characterization of FaFT1: a homolog of Flowering Locus T from strawberry. Adv J Food Sci Technol 8(3):180–188

    Article  CAS  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakajima R, Otagaki S, Yamada K, Shiratake K, Matsumoto S (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, Yoshida Y, Hisamatsu T (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 

  • Pin PA, Nilsson O (2012) The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ 35:1742–1755

    Article  CAS  PubMed  Google Scholar 

  • Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJ, Nilsson O (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330:1397–1400

    Article  CAS  PubMed  Google Scholar 

  • Putterill J, Varkonyi-Gasic E (2016) FT and florigen long-distance flowering control in plants. Curr Opin Plant Biol 33:77–82

    Article  CAS  PubMed  Google Scholar 

  • Rantanen M, Kurokura T, Mouhu K, Pinho P, Tetri E, Halonen L, Palonen P, Elomaa P, Hytönen T (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, Mouhu K, Hytönen T (2015) Strawberry homologue of TERMINAL FLOWER1 integrates photoperiod and temperature signals to inhibit flowering. Plant J 82:163–173

    Article  CAS  PubMed  Google Scholar 

  • Song YH, Ito S, Imaizumi T (2013) Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends Plant Sci 18:575–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sreekantan L, Thomas MR (2006) VvFT and VvMADS8, the grapevine homologues of the floral integrators FT and SOC1, have unique expression patterns in grapevine and hasten flowering in Arabidopsis. Funct Plant Biol 33:1129–1139

    Article  CAS  PubMed  Google Scholar 

  • Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037

    Article  CAS  PubMed  Google Scholar 

  • Stewart PJ, Folta KM (2010) A review of photoperiodic flowering research in strawberry (Fragaria spp.). Crit Rev Plant Sci 29:1–13

    Article  Google Scholar 

  • Sun H, Jia Z, Cao D, Jiang B, Wu C, Hou W, Liu Y, Fei Z, Zhao D, Han T (2011) GmFT2a, a soybean homolog of FLOWERING LOCUS T, is involved in flowering transition and maintenance. PLoS ONE 6:e29238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tafazoli E, Vince-Prue D (1978) A comparison of the effects of long days and exogenous growth regulators on growth and flowering in strawberry, Fragaria × ananassa, Duch. J Hortic Sci 53:255–259

    Article  CAS  Google Scholar 

  • Thompson PA, Guttridge CG (1959) Effect of Gibberellic acid on the initiation of flowers and runners in the strawberry. Nature 184:BA72–BA73

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Yang R, Devisetty UK, Maloof JN, Zuo Y, Li J, Shen Y, Zhao J, Bao M, Ning G (2017) The divergence of flowering time modulated by FT/TFL1 is independent to their interaction and binding activities. Front Plant Sci 8:697

    Article  PubMed  PubMed Central  Google Scholar 

  • Weebadde CK, Wang D, Finn CE, Lewers KS, Luby JJ, Bushakra J, Sjulin TM, Hancock JF (2008) Using a linkage mapping approach to identify QTL for day-neutrality in the octoploid strawberry. Plant Breed 127:94–101

    Google Scholar 

  • Wickland DP, Hanzawa Y (2015) The FLOWERING LOCUS T/TERMINAL FLOWER1 gene family: functional evolution and molecular mechanisms. Mol Plant 8:983–997

    Article  CAS  PubMed  Google Scholar 

  • Zhai H, Lü S, Liang S, Wu H, Zhang X, Liu B, Kong F, Yuan X, Li J, Xia Z (2014) GmFT4, a homolog of FLOWERING LOCUS T, is positively regulated by E1 and functions as a flowering repressor in soybean. PLoS ONE 9:e89030

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (No. 31872073), the Liaoning Key R&D Program (2020JH2/10200032) and the Natural Science Foundation of Liaoning Province (No. 2014027015, 20180550431). Our sincere thanks go to Dr. Junhui Zhou of UMD for grammar checking. We also thank the editor and the reviewers for their valuable comments and suggestions.

Author information

Authors and Affiliations

Authors

Contributions

YL designed the research. WC, HL, DZ, YY, CL and AY performed the experiments. YL, WC, HL and ZZ wrote the manuscript.

Corresponding author

Correspondence to Yuexue Liu.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Handling Editor: Karine David.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

344_2021_10409_MOESM1_ESM.tif

Supplementary file1 Fruit without seed cross-section showing pith (center) and cortex (flanking) tissues; the red line indicates the boundary of two tissues (TIF 91 kb) (Color figure online)

344_2021_10409_MOESM2_ESM.jpg

Supplementary file2 Vector construction. FaFT1 was inserted into the plasmid pCAMBIA1304. 35S promoter: the cauliflower mosaic virus (CaMV) 35S promoter (JPG 43 kb)

344_2021_10409_MOESM3_ESM.tif

Supplementary file3 PCR detection of FaFT1 in Arabidopsis T3 generation lines. WT: nontransgenic Arabidopsis as a negative control, 1–9: PCR detection results for T3 generation plantlets (TIF 51 kb)

344_2021_10409_MOESM4_ESM.tif

Supplementary file4 Sequence alignment of five reported FaFTs. Black and blue colors indicate higher and lower amino acid residue conservation, respectively. Red and blue boxes indicate the same protein sequences with different accession numbers (TIF 102 kb) (Color figure online)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, W., Li, H., Zou, D. et al. Expression Profile of FaFT1 and Its Ectopic Expression in Arabidopsis Demonstrate Its Function in the Reproductive Development of Fragaria × ananassa. J Plant Growth Regul 41, 1687–1698 (2022). https://doi.org/10.1007/s00344-021-10409-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-021-10409-z

Keywords

Navigation