Skip to main content
SpringerLink
Log in

Simple sequence repeat markers linked to the everbearing flowering gene in long-day and day-neutral cultivars of the octoploid cultivated strawberry Fragaria × ananassa

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

To identify markers closely linked to the everbearing gene in the octoploid cultivated strawberry Fragaria × ananassa, we conducted linkage analysis based on simple sequence repeat (SSR) polymorphisms. We analyzed F1 populations from three crosses: ‘Sagahonoka’ × ‘Summer-berry’ (94 individuals), ‘Sagahonoka’ × ‘Ever-berry’ (137 individuals), and ‘Hecker’ × ‘Sagahonoka’ (177 individuals). ‘Sagahonoka’ is a June-bearing cultivar; ‘Summer-berry’ and ‘Ever-berry’ are everbearing cultivars classified as older everbearers with a long-day flowering response; ‘Hecker’ is a day-neutral cultivar having F. virginiana ssp. glauca in its ancestry. In these populations, the closest marker, FxaACA02I08C, was mapped at 1.1 cM (‘Summer-berry’ and ‘Hecker’) or 1.5 cM (‘Ever-berry’) from the everbearing gene. We detected correspondence between SSR allele segregation and the flowering habit: one allele was linked to the everbearing trait and the other one to the June-bearing trait. The concordance between the phenotype and marker genotype was more than 98 % in all three populations. These results indicate that the everbearing trait is regulated by a single dominant gene. We also conclude that the locus regulating the everbearing or June-bearing flowering habit is the same in long-day and day-neutral types. The identified markers will be useful for the selection of progeny of various everbearing cultivars.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    Google Scholar 

  • Ashley MV, Wilk JA, Styan SMN, Craft KJ, Jones KL, Feldheim KA, Lewers KS, Ashman TL (2003) High variability and disomic segregation of microsatellites in the octoploid Fragaria virginiana Mill (Rosaceae). Theor Appl Genet 107:1201–1207

    Article  CAS  PubMed  Google Scholar 

  • Bentvelsen GCM, Bouw E, Veldhuyzen van Zanten JE (1997) Breeding strawberries (Fragaria × ananassa Duch) from seed. Acta Hort 439:149–153

    Article  Google Scholar 

  • Bringhurst RS (1992) Origin and characteristics of the University of California day-neutral strawberry cultivars. Hort Sci 27:601

    Google Scholar 

  • Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20:1004–1010

    CAS  PubMed  Google Scholar 

  • Castro P, Bushakra JM, Stewart P, Weebadde CK, Wang D, Hancock JF, Finn CE, Luby JJ, Lewers KS (2015) Genetic mapping of day-neutrality in cultivated strawberry. Mol Breed 35:79–94

    Article  Google Scholar 

  • Darrow GM (1966) The strawberry: history, breeding and physiology. Holt, Rinehart and Winston, New York

    Google Scholar 

  • Durner EF, Barden JA, Himelrick DG, Poling EB (1984) Photoperiod and temperature effects on flower and runner development in day-neutral, June-bearing, and everbearing strawberries. J Am Soc Hort Sci 109:396–400

    Google Scholar 

  • Gaston A, Perrotte J, Lerceteau- Köhler E, Rousseau-Gueutin M, Petit A, Hernould M, Rothan C, Denoyes B (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 

  • Hancock JF (1999) Strawberries. CABI Publishing, Wallingford

    Google Scholar 

  • Heide OM, Stavang JA, Sønsteby A (2013) Physiology and genetics of flowering in cultivated and wild strawberries—a review. J Hort Sci Biotech 88:1–18

    CAS  Google Scholar 

  • Hirakawa H, Shirasawa K, Kosugi S et al (2014) Dissection of the octoploid strawberry genome by deep sequencing of the genomes of Fragaria species. DNA Res 21:169–181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Honjo M, Kataoka S, Yui S, Morishita M, Yano T, Hamano M, Yamazaki H (2011) Varietal differences and selection indicators for flowering pattern in everbearing strawberry. J Jpn Soc Hort Sci 80:38–44

    Article  Google Scholar 

  • Honjo M, Yui S, Kunihisa M (2013) Observation of the disomic inheritance of four allelic pairs in the octoploid cultivated strawberry. HortScience 48:948–954

    Google Scholar 

  • Isobe SN, Hirakawa H, Sato S et al (2013) Construction of an integrated high density simple sequence repeat linkage map in cultivated strawberry (Fragaria × ananassa) and its applicability. DNA Res 20:79–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwata H, Gaston A, Remay A, Thouroude T, Jeauffre J, Kawamura K, Oyant LH-S, 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 

  • James CM, Wilson F, Hadonou AM, Tobutt KR (2003) Isolation and characterization of polyploid microsatellites in diploid strawberry (Fragaria vesca L.) for mapping, diversity studies and clone identification. Mol Ecol Notes 3:171–173

    Article  CAS  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 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 

  • Kunihisa M, Fukino N, Matsumoto S (2003) Development of cleavage amplified polymorphic sequence (CAPS) markers for identification of strawberry cultivars. Euphytica 134:209–215

    Article  CAS  Google Scholar 

  • Kunihisa M, Fukino N, Matsumoto S (2005) CAPS markers improved by cluster-specific amplification for identification of octoploid strawberry (Fragaria × ananassa Duch) cultivars, and their disomic inheritance. Theor Appl Genet 110:1410–1418

    Article  CAS  PubMed  Google Scholar 

  • Lewers KL, Styan SMN, Hokanson SC (2005) Strawberry GenBank-derived and genomic simple sequence repeat (SSR) markers and their utility with strawberry, blackberry, and red and black raspberry. J Am Soc Hort Sci 130:102–115

    CAS  Google Scholar 

  • Maruo T, Ito Y, Ishikawa M, Kamisoyama D, Ohmameuda M, Ogura Y (2007) About the practical use of the seed propagation type strawberry (F. × ananassa Duch) cultivation system (using June-bearing cultivars). Hort Res 61:73–78 (In Japanese with English summary)

    Google Scholar 

  • Monma S, Okitsu S, Takada K (1990) Inheritance of everbearing in cultivated strawberry. Bull Natl Res Inst Veg Ornam Plants Tea Jpn Ser C1:21–29 (In Japanese with English summary)

    Google Scholar 

  • Morishita M, Honjo M, Hamano M, Yamazaki H, Yano T (2012a) Genetic analysis of the everbearing habit in strawberry cultivars under 24-hour daylength condition. Hort Res (Japan) 11:301–307 (In Japanese with English summary)

    Article  Google Scholar 

  • Morishita M, Honjo M, Hamano M, Yamazaki H, Yano T (2012b) Relationship between the nodal position of the first inflorescence in first-year runner plants and the everbearing strength in everbearing strawberry cultivars. Hort Res (Japan) 11:147–152 (In Japanese with English summary)

    Article  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 

  • Nicoll MF, Galletta GJ (1987) Variation in growth and flowering habits of Junebearing and everbearing strawberries. J Am Soc Hort Sci 112:872–880

    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 

  • Nishiyama M, Kanahama K, Ebihara Y (2007) Varietal differences in critical photoperiod for inflorescence production among day-neutral strawberry cultivars. Acta Hort 761:207–213

    Article  Google Scholar 

  • Nishiyama M, Ebihara Y, Kanahama K (2009) Differences in critical photoperiod for flower bud initiation among everbearing strawberry cultivars. Hort Res (Japan) 8:35–39 (In Japanese with English summary)

    Article  Google Scholar 

  • Rousseau-Gueutin M, Lerceteau-Köhler E, Barrot L, Sargent DJ, Monfort A, Simpson D, Arus P, Guérin G, Denoyes-Rothan B (2008) Comparative genetic mapping between octoploid and diploid Fragaria species reveals a high level of colinearity between their genomes and the essentially disomic behavior of the cultivated octoploid strawberry. Genetics 179:2045–2060

    Article  PubMed  PubMed Central  Google Scholar 

  • Rowland LJ, Nguyen B (1993) Use of PEG for purification of DNA from leaf tissue of woody plants. Biotechniques 14:735–736

    Google Scholar 

  • Sargent DJ, Hadonou AM, Simpson DW (2003) Development and characterization of polymorphic microsatellite markers from Fragaria viridis, a wild diploid strawberry. Mol Ecol Notes 3:550–552

    Article  CAS  Google Scholar 

  • Sargent DJ, Davis TM, Tobutt KR, Wilkinson MJ, Battey NH, Simpson DW (2004) A genetic linkage map of microsatellite, gene-specific and morphological markers in diploid Fragaria. Theor Appl Genet 109:1385–1391

    Article  CAS  PubMed  Google Scholar 

  • Sargent DJ, Passey T, Surbanovski N, Lopez Girona E, Kuchta P, Davik J, Harrison R, Passey A, Whitehouse AB, Simpson DW (2012) A microsatellite linkage map for the cultivated strawberry (Fragaria × ananassa) suggests extensive regions of homozygosity in the genome that may have resulted from breeding and selection. Theor Appl Genet 124:1229–1240

    Article  CAS  PubMed  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Serçe S, Hancock JF (2005) Inheritance of day-neutrality in octoploid species of Fragaria. J Am Soc Hort Sci 130:580–584

    Google Scholar 

  • Sønsteby A, Heide OM (2007a) Quantitative long-day flowering response in the perpetual-flowering F1 strawberry cultivar Elan. J Hort Sci Biotech 82:266–274

    Google Scholar 

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

    Google Scholar 

  • Spigler RB, Lewers KS, Main DS, Ashman TL (2008) Genetic mapping of sex determination in a wild strawberry, Fragaria virginiana, reveals earliest form of sex chromosome. Heredity 101:507–517

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto T, Tamaki K, Matsumoto J, Yamamoto Y, Shiwaku K, Watanabe K (2005) Detection of RAPD markers linked to the everbearing gene in Japanese cultivated strawberry. Plant Breed 124:498–501

    Article  CAS  Google Scholar 

  • Taimatsu T (1993) Horticultural characteristics and cultivation of everbearing strawberries for different harvest periods. Spec Res Bull Nara Agric Exp Stn 1–206 (In Japanese with English summary)

  • Van Ooijen JW (2006) JoinMap®4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen

    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 

  • Zorrilla-Fontanesi Y, Cabeza A, Torres AM, Botella MA, Valpuesta V, Monfort A, Sanchez-Sevilla JF, Amaya I (2011) Development and bin mapping of strawberry genic-SSRs in diploid Fragaria and their transferability across the Rosoideae subfamily. Mol Breed 27:137–156

    Article  Google Scholar 

Download references

Acknowledgments

We thank Naoe Suzuki and Shigeki Moriya for technical assistance in the laboratory, and Rikiya Kimura, Masato Inoue, Yoshiyuki Fujisawa, Setsuko Oki, Yukari Sakurai, and Keiko Iwabuchi for assistance with plant cultivation. This work was supported by National Agriculture and Food Research Organization Research Project No. 211 ‘Establishment of Integrated Basis for Development and Application of Advanced Tools for DNA Marker-Assisted Selection in Horticultural Crops’.

Author information

Authors and Affiliations

  1. NARO Tohoku Agricultural Research Center, 92 Nabeyashiki, Shimokuriyagawa, Morioka, Iwate, 020-0123, Japan

    Masanori Honjo, Megumi Hamano, Hiromichi Yamazaki & Susumu Yui

  2. NARO Institute of Vegetable and Tea Science, 360 Ano-Kusawa, Tsu, Mie, 514-2392, Japan

    Tsukasa Nunome & Sono Kataoka

  3. NARO Western Region Agricultural Research Center, 1-3-1 Senyu-cho, Zentsuji, Kagawa, 765-8508, Japan

    Takayoshi Yano

  4. NARO Kyushu Okinawa Agricultural Research Center, 1823-1 Miimachi, Kurume, Fukuoka, 839-8503, Japan

    Masami Morishita

  5. NARO Institute of Fruit Tree Science, 2-1 Fujimoto, Tsukuba, Ibaraki, 305-8605, Japan

    Toshiya Yamamoto

Authors
  1. Masanori Honjo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tsukasa Nunome
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sono Kataoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takayoshi Yano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Megumi Hamano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hiromichi Yamazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Toshiya Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Masami Morishita
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Susumu Yui
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masanori Honjo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 38 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Honjo, M., Nunome, T., Kataoka, S. et al. Simple sequence repeat markers linked to the everbearing flowering gene in long-day and day-neutral cultivars of the octoploid cultivated strawberry Fragaria × ananassa . Euphytica 209, 291–303 (2016). https://doi.org/10.1007/s10681-015-1626-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10681-015-1626-6

Keywords

Search

Navigation