Skip to main content
SpringerLink
Log in

Identification of quantitative trait loci (QTL) for fruit-quality traits and number of weeks of flowering in the cultivated strawberry

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Fruit quality and repeat flowering are two major foci of several strawberry breeding programs. The identification of quantitative trait loci (QTL) and molecular markers linked to these traits could improve breeding efficiency. In this work, an F1 population derived from the cross ‘Delmarvel’ × ‘Selva’ was used to develop a genetic linkage map for QTL analyses of fruit-quality traits and number of weeks of flowering. Some QTL for fruit-quality traits were identified on the same homoeologous groups found in previous studies, supporting trait association in multiple genetic backgrounds and utility in multiple breeding programs. None of the QTL for soluble solids colocated with a QTL for titratable acids, and, although the total soluble solid contents were significantly and positively correlated with titratable acids, the correlation coefficient value of 0.2452 and independence of QTL indicate that selection for high soluble solids can be practiced independently of selection for low acidity. One genomic region associated with the total number of weeks of flowering was identified quantitatively on LG IV-S-1. The most significant marker, FxaACAO2I8C-145S, explained 43.3 % of the phenotypic variation. The repeat-flowering trait, scored qualitatively, mapped to the same region as the QTL. Dominance of the repeat-flowering allele was demonstrated by the determination that the repeat-flowering parent was heterozygous. This genomic region appears to be the same region identified in multiple mapping populations and testing environments. Markers linked in multiple populations and testing environments to fruit-quality traits and repeat flowering should be tested widely for use in marker-assisted breeding.

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

  • Aaby K, Skrede G, Wrolstad RE (2005) Phenolic composition and antioxidant activities in flesh and achenes of strawberries (Fragaria ananassa). J Agric Food Chem 53:4032–4040

    Article  CAS  PubMed  Google Scholar 

  • Abbott JA (1999) Quality measurement of fruits and vegetables. Postharvest Biol Tachnol 15:207–225

    Article  Google Scholar 

  • Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier Sun Z, Jongsma MA, Schwab W, Bouwmeester HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16:3110–3131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Albani MC, Battey NH, Wilkinson MJ (2004) The development of ISSR-derived scar markers around the SEASONAL FLOWERING LOCUS (SFL) in Fragaria vesca. Theor Appl Genet 109:571–579

    Article  CAS  PubMed  Google Scholar 

  • Ashley MV, Styan SMN, Craft KJ, Jones KL, Feldheim KA, Fessler JL, Lewers KS, Ashman T-L (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 

  • Bassil NV, Davis TM, Zhang H, Ficklin S, Mittmann M, Webster T et al (2015) Development and preliminary evaluation of a 90 K Axiom SNP Array for the allo-octoploid cultivated strawberry Fragaria × ananassa. BMC Genom 16:155

    Article  Google Scholar 

  • Battino M, Beekwilder J, Denoyes-Rothan B, Laimer M, McDougall GJ, Mezzetti B (2009) Bioactive compounds in berries relevant to human health. Nutr Rev 67(S1):145–150

    Article  Google Scholar 

  • Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by tag DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20(6):1004

    CAS  PubMed  Google Scholar 

  • Capocasa F, Diamanti J, Tulipani S, Battino M, Mezzetti B (2008) Breeding strawberry (Fragaria × ananassa Duch) to increase fruit nutritional quality. BioFactors 34:67–72

    Article  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

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clark JH (1937) Inheritance of the so-called everbearing tendency in the strawberry. Proc Am Soc Hortic Sci 35:67–70

    Google Scholar 

  • Clifford MN (2000) Anthocyanins-nature, occurrence and dietary burden. J Sci Food Agric 80:1063–1072

    Article  CAS  Google Scholar 

  • Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196

    Article  CAS  Google Scholar 

  • Coman MS, Popescu AN (1997) Inheritance of some strawberry quantitative traits. In: van der Sheer HAT, Lieten F, Dijkstra J (eds) Proceedings of third international strawberry symposium, pp 81–88

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

    Google Scholar 

  • Demmig-Adams B, Adams WW (2002) Antioxidants in photosynthesis and human nutrition. Science 298:2149–2153

    Article  CAS  PubMed  Google Scholar 

  • Deng C, Davis TM (2001) Molecular identification of the yellow fruit color (c) locus in diploid strawberry: a candidate gene approach. Theor Appl Genet 103:316–322

    Article  CAS  Google Scholar 

  • Espin JC, Tomas-Barberan FA (2001) Phenolic compounds and related enzymes as determinants of fruits and vegetables quality. J Sci Food Agric 81:853–876

    Article  Google Scholar 

  • Galletta GJ, Maas JL (1990) Strawberry genetics. HortScience 25:871–879

    Google Scholar 

  • Gaston A, Perrotte J, Lerceteau-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 

  • Hancock JE (1999) Fruiting and postharvest physiology. Strawberries. CABI Publishing, Wallingford

    Google Scholar 

  • Hannum SM (2004) Potential impact of strawberries on human health: a review of the science. Crit Rev Food Sci Nutr 44:1–17

    Article  CAS  PubMed  Google Scholar 

  • Hirakawa H, Shirasawa K, Kosugi S, Tashiro K, Nakayama S, Yamada M, Kohara M, Watanabe A, Kishida Y, Fujishiro T, Tsuruoka H, Minami C, Sasamoto S, Kato M, Nanri K, Komaki A, Yanagi T, Guoxin Q, Maeda F, Ishikawa M, Kuhara S, Sato S, Tabata S, Isobe SN (2014) Dissection of the octoploid strawberry genome by deep sequencing of the genomes of Fragaria species. DNA Res 21:169–181

    Article  CAS  PubMed  Google Scholar 

  • Honjo M, Nunome T, Kataoka S, Yano T, Hamano M, Yamazaki H, Yamamoto T, Morishita M, Yui S (2016) 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. doi:10.1007/s10681-015-1626-6

    Google Scholar 

  • Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kader AA (1991) Quality and its maintence in relation to the postharvest physiology of strawberry. In: Dale A, Luby JJ (eds) The strawberry into the 21st century. Timber Press, Portland, pp 145–152

    Google Scholar 

  • Kähkönen MP, Hopia AI, Heinonen M (2001) Berry phenolics and their antioxidant activity. J Agric Food Chem 49:4076–4082

    Article  CAS  PubMed  Google Scholar 

  • Kalt W, Prange RK, Lidster PD (1993) Postharvest color development of strawberries: influence of maturity, temperature and light. Can J Plant Sci 73:541–548

    Article  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lerceteau-Köhler E, Moing A, Guerin G, Renaud C, Petit A, Rothan C, Denoyes B (2012) Genetic dissection of fruit quality traits in the octoploid cultivated strawberry highlights the role of homoeo-QTL in their control. Theor Appl Genet 124:1059–1077

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewers KS, Wang SY, Vinyard BT (2010) Evaluation of blackberry cultivars and breeding selections for fruit quality traits and flowering and fruiting dates. Crop Sci 50:2475–2491

    Article  Google Scholar 

  • Liu B (1998) Statistical genomics: linkage, mapping and QTL analysis. CRC Press, Boca Raton

    Google Scholar 

  • Lopes-da-Silva F, de Pascual-Teresa S, Rivas-Gonzalo JC, Santuos-Buelga C (2002) Identification of anthocyanin pigments in strawberry (cv. Camarosa) by LC using DAD and ESI-MS detection. Eur Food Res Technol 214:248–253

    Article  CAS  Google Scholar 

  • Lundergan CA, Moore JN (1975) Inheritance of ascorbic acid content and color intensity in fruits of strawberry (Fragaria × ananassa Duch). J Am Soc Hortic Sci 100:633–635

    CAS  Google Scholar 

  • Määttä-Riihinen KR, Kamal-Eldin A, Törrönen AR (2004) Identification and quantification of phenolic compounds in berries of Fragaria and Rubus species (family Rosaceae). J Agric Food Chem 52:6178–6187

    Article  CAS  PubMed  Google Scholar 

  • Ohtsuka Y, Kibe H, Hakoda N, Shimura I, Ogiwara I (2004) Heritability of sugar contents in strawberry fruit in the F-1 populations using a common pollen parent. J Jpn Soc Hortic Sci 73:31–35

    Article  CAS  Google Scholar 

  • Ourecky DK, Slate GL (1967) Behavior of the everbearing characteristics in strawberries. Proc Am Soc Hortic Sci 91:236–248

    Google Scholar 

  • Paterson AH, Damon S, Hewitt JD, Zamir D, Rabinowitch HD, Lincoln SE, Lander ES, Tanksley SD (1991) Mendelian factors underlying quantitative traits in tomato—comparison across species, generations, and environments. Genetics 127:181–197

    CAS  PubMed  PubMed Central  Google Scholar 

  • Powers L (1954) Inheritance of period of blooming in progenies of strawberries. Proc Am Soc Hortic Sci 64:293–298

    Google Scholar 

  • Rousseau-Gueutin M, Lerceteau-Köhler E, Barrot L, Sargent DJ, Monfort A, Simpson D, Arus P, Guerin 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 

  • 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, Clarke J, Simpson DW, Tobutt KR, Arus P, Monfort A, Vilanova S, Denoyes-Rothan B, Rousseau M, Folta KM, Bassil NV, Battey NH (2006) An enhanced microsatellite map of diploid Fragaria. Theor Appl Genet 112:1349–1359

    Article  CAS  PubMed  Google Scholar 

  • Sargent DJ, Rys A, Nier S, Simpson DW, Tobutt KR (2007) The development and mapping of functional markers in Fragaria and their transferability and potential for mapping in other genera. Theor Appl Genet 114:373–384

    Article  CAS  PubMed  Google Scholar 

  • Sargent DJ, Cipriani G, Vilanova S, Gil-Ariza D, Arus P, Simpson DW, Tobutt KR, Monfort A (2008) The development of a bin mapping population and the selective mapping of 103 markers in the diploid Fragaria reference map. Genome 51:120–127

    Article  CAS  PubMed  Google Scholar 

  • Sargent D, Fernandez-Fernandez F, Ruiz-Rojas JJ, Sutherland BG, Passey A, Whitehouse AB, Simpson DW (2009) A genetic linkage map of the cultivated strawberry (Fragaria × ananassa) and its comparison to the diploid Fragaria reference map. Mol Breed 24:293–303

    Article  CAS  Google Scholar 

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

  • Schauer N, Semel Y, Balbo I, Steinfath M, Repsilber D, Selbig J, Pleban T, Zamir D, Fernie AR (2008) Mode of inheritance of primary metabolic traits in tomato. Plant Cell 20:509–523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments: a poor man’s approach to genotyping for research and high-throughput diagnostics. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Scott DH (1936) Size, firmness, and time of ripening of fruit of seedlings of Fragaria virginiana Duch. crossed with cultivated strawberry varieties. Proc Am Soc Hortic Sci 74:388–393

    Google Scholar 

  • Seeram NP (2008) Berry fruits for cancer prevention: current status and future prospects. J Agric Food Chem 56:630–635

    Article  CAS  PubMed  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Article  Google Scholar 

  • Shaw DV (1988) Genotypic variation and genotypic correlations for sugars and organic acids of strawberries. J Am Soc Hortic Sci 113:770–774

    CAS  Google Scholar 

  • Shaw DV (2003) Heterogeneity of segregation ratios from selfed progenies demonstrate polygenic inheritance for day neutrality in strawberry (Fragaria × ananassa Duch.). J Am Sci 128:504–507

    Google Scholar 

  • Shaw DV, Famula TR (2005) Complex segregation analysis of dayneutrality in domestic strawberry (Fragaria × ananassa Duch.). Euphytica 145:331–338

    Article  Google Scholar 

  • Shaw DV, Bringhurst RS, Voth V (1987) Genetic variation for quality traits in an advanced-cycle breeding population of strawberries. J Am Soc Hortic Sci 112:699–702

    Google Scholar 

  • Sone K, Mochizuki T, Okimura M, Noguchi Y, Kitadani E (2003) Inheritance of ascorbic acid content in strawberry fruits. J Jpn Soc Hortic Sci 72:141–147

    Article  CAS  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 

  • Spigler RB, Lewers KS, Johnson AL, Ashman T-L (2010) Comparative mapping reveals autosomal origin of sex chromosome in octoploid Fragaria virginiana. J Hered 101:S107–S117

    Article  CAS  PubMed  Google Scholar 

  • Stam P (1993) Construction of integrated linkage maps by means of a new computer package: JoinMap. Plant J 3:739–744

    Article  CAS  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 

  • Tulipani S, Mezzetti B, Battino M (2009) Impact of strawberries on human health: insight into marginally discussed bioactive compounds for the Mediterranean diet. Public Health Nutr 12:1656–1662

    Article  PubMed  Google Scholar 

  • van Ooijen JW (2004) MapQTL 5, software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, Wageningen

    Google Scholar 

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

    Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTL. J Hered 93:77–78

    Article  CAS  PubMed  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 

  • Wrolstad RE, Putnam TP, Varseveld GW (1970) Color quality of frozen strawberries: effect of anthocyanin, pH, total acidity and ascorbic acid variability. J Food Sci 35:448–452

    Article  CAS  Google Scholar 

  • Zorrilla-Fontanesi Y, Cabeza A, Dominguez P et al (2011a) Quantitative trait loci and underlying candidate genes controlling agronomical and fruit quality traits in octoploid strawberry (Fragaria × ananassa). Theor App Genet 123:755–778

    Article  Google Scholar 

  • Zorrilla-Fontanesi Y, Cabeza A, Torres AM, Botella MA, Valpuesta V, Monfort A, Sanchez-Sevilla JF, Amaya I (2011b) 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 

  • Zorrilla-Fontanesi Y, Rambla JL, Cabeza A, Medina JJ, Sánchez-Sevilla JF, Valpuesta V, Botella MA, Granell A, Amaya I (2012) Genetic analysis of strawberry fruit aroma and identification of O-Methyltransferase FaOMT as the locus controlling natural variation in mesifurane content. Plant Physiol 159:851–870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This project was funded by USDA-ARS Project 8042-21220-254-00. The authors wish to thank Drs. Stan Hokanson and Sarah Nourse who generated the population before moving on to other research opportunities, Dr. Show Wang who collected the anthocyanin, phenolics and ORAC data before retiring and passing on, and the many former USDA-ARS technicians and undergraduate students who worked on this population at some point while associated with the project. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture or any of the other agencies involved in this research.

Author information

Authors and Affiliations

  1. Genetic Improvement of Fruits and Vegetables Laboratory, USDA-ARS, Building 010A BARC-West, 10300 Baltimore Ave., Beltsville, MD, 20705-2350, USA

    P. Castro & K. S. Lewers

Authors
  1. P. Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. S. Lewers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. S. Lewers.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castro, P., Lewers, K.S. Identification of quantitative trait loci (QTL) for fruit-quality traits and number of weeks of flowering in the cultivated strawberry. Mol Breeding 36, 138 (2016). https://doi.org/10.1007/s11032-016-0559-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-016-0559-7

Keywords

Search

Navigation