Theoretical and Applied Genetics

, Volume 112, Issue 7, pp 1349–1359 | Cite as

An enhanced microsatellite map of diploid Fragaria

  • D. J. SargentEmail author
  • J. Clarke
  • D. W. Simpson
  • K. R. Tobutt
  • P. Arús
  • A. Monfort
  • S. Vilanova
  • B. Denoyes-Rothan
  • M. Rousseau
  • K. M. Folta
  • N. V. Bassil
  • N. H. Battey
Original Paper


A total of 45 microsatellites (SSRs) were developed for mapping in Fragaria. They included 31 newly isolated codominant genomic SSRs from F. nubicola and a further 14 SSRs, derived from an expressed sequence tagged library (EST-SSRs) of the cultivated strawberry, F. × ananassa. These, and an additional 64 previously characterised but unmapped SSRs and EST-SSRs, were scored in the diploid Fragaria interspecific F2 mapping population (FV×FN) derived from a cross between F. vesca 815 and F. nubicola 601. The cosegregation data of these 109 SSRs, and of 73 previously mapped molecular markers, were used to elaborate an enhanced linkage map. The map is composed of 182 molecular markers (175 microsatellites, six gene specific markers and one sequence-characterised amplified region) and spans 424 cM over seven linkage groups. The average marker spacing is 2.3 cM/marker and the map now contains just eight gaps longer than 10 cM. The transferability of the new SSR markers to the cultivated strawberry was demonstrated using eight cultivars. Because of the transferable nature of these markers, the map produced will provide a useful reference framework for the development of linkage maps of the cultivated strawberry and for the development of other key resources for Fragaria such as a physical map. In addition, the map now provides a framework upon which to place transferable markers, such as genes of known function, for comparative mapping purposes within Rosaceae.


Fragaria Genetic mapping Microsatellites EST Functional genomics 



This research was supported at EMR by funds from Defra, the University of Reading Research Endowment Trust Fund, the East Malling Trust for Horticultural Research and the Worshipful Company of Fruiterers. Funding at IRTA was provided by grant no. AGL2003-04691 from CICYT (Spain), and a fellowship to S. Vilanova from MEC of Spain (EX2003-1083). Funding at INRA was provided by Région Aquitaine and the European Community (FEDER funds). The authors also to acknowledge the North American Strawberry Growers’ Association for funding allocated toward the sequencing of ESTs used in this study at the University of Florida.


  1. Altschul S, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  2. Aranzana J, Pineda A, Cosson P, Dirlewanger E, Ascasibar J, Cipriani G, Ryder D, Testolin R, Abbott A, King J, Iezzoni A, Arús P (2003) A set of simple sequence repeat markers covering the Prunus genome. Theor Appl Genet 106:819–825PubMedGoogle Scholar
  3. Areshchenkova T, Ganal MW (1999) Long tomato microsatellites are predominantly associated with centromeric regions. Genome 42:536–544CrossRefPubMedGoogle Scholar
  4. Ascenzi R, Gantt JS (1997) A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants. Plant Mol Biol 34:629–641CrossRefPubMedGoogle Scholar
  5. 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 octoploid Fragaria virginiana Mill (Rosaceae). Theor Appl Genet 107:1201–1207CrossRefPubMedGoogle Scholar
  6. Barrett B, Griffiths A, Schreiber M, Ellison N, Mercer C, Bouton J, Ong B, Forster J, Sawbridge T, Spangenberg G, Bryan G, Woodfield D (2004) A microsatellite map of white clover. Theor Appl Genet 109:596–608CrossRefPubMedGoogle Scholar
  7. Blair MW, Pedraza F, Buendia HF, Gaitán Solìs E, Beebe SE, Gepts P, Tohme J (2003) Development of a genome-wide anchored microsatellite map for common bean (Phaseolus vulgaris L). Theor Appl Genet 107:1362–1374CrossRefPubMedGoogle Scholar
  8. Chassin Y, Kapri-Pardes E, Sinvany G, Arad T, Adam Z (2002) Expression and characterization of the thylakoid lumen protease DegP1 from Arabidopsis. Plant Physiol 130:857–864CrossRefPubMedGoogle Scholar
  9. Cipriani G, Testolin R (2004) Isolation and characterisation of microsatellite loci in Fragaria. Mol Ecol Notes 4:366–368CrossRefGoogle Scholar
  10. Cregan PB, Mudge J, Fickus EW, Marek LF, Danesh D, Denny R, Shoemaker RC, Matthews BF, Jarvik T, Young ND (1999) Targeted isolation of simple sequence repeat markers through the use of bacterial artificial chromosomes. Theor Appl Genet 98:919–928CrossRefGoogle Scholar
  11. Davis TM, Yu H (1997) A linkage map of the diploid strawberry, Fragaria vesca. J Hered 88:215–221Google Scholar
  12. Decroocq V, Favé MG, Hagen L, Bordenave L, Decroocq S (2003) Development and transferability of apricot and grape EST microsatellite markers across taxa. Theor Appl Genet 106:912–922PubMedGoogle Scholar
  13. Deeks MJ, Hussey PJ, Davies B (2002) Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci 7:492–498PubMedCrossRefGoogle Scholar
  14. Deng C, Davis TM (2001) Molecular identification of the yellow fruit color (c) locus in diploid strawberry: a candidate gene approach. Theor Appl Genet 103:316–322CrossRefGoogle Scholar
  15. Elsik CG, Williams CG (2001) Families of clustered microsatellites in a conifer genome. Mol Genet Genomics 265:535–542CrossRefPubMedGoogle Scholar
  16. Eujayl I, Sorrells ME, Baum M, Wolters P, Powell W (2002) Isolation of EST-derived microsatellite markers for genotyping the A and B genomes of wheat. Theor Appl Genet 104:399–407CrossRefPubMedGoogle Scholar
  17. Folta KM, Staton M, Stewart PJ, Jung S, Bies DH, Jesudurai C, Main D (2005) Expressed sequence tags (ESTs) and simple sequence repeat (SSR) markers from octoploid strawberry (Fragaria × ananassa). BMC Plant Biol 5:12CrossRefPubMedGoogle Scholar
  18. Fraser LG, Harvey CF, Crowhurst RN, De Silva HN (2004) EST-derived microsatellites from Actinidia species and their potential for mapping. Theor Appl Genet 108:1010–1016CrossRefPubMedGoogle Scholar
  19. Gish W, States DJ (1993) Identification of protein coding regions by database similarity search. Nat Genet 3:266–272CrossRefPubMedGoogle Scholar
  20. Hadonou AM, Sargent DJ, Wilson F, James CM, Simpson DW (2004) Development of microsatellite markers in Fragaria, their use in genetic diversity analysis and their potential for genetic linkage mapping. Genome 47:429–438CrossRefPubMedGoogle Scholar
  21. Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111CrossRefPubMedGoogle Scholar
  22. Jung S, Jesudurai C, Staton M, Du ZD, Ficklin S, Cho IH, Abbott A, Tomkins J, Main D (2004) GDR (Genome Database for Rosaceae): integrated web resources for Rosaceae genomics and genetics research. BMC Bioinformatics 5:130CrossRefPubMedGoogle Scholar
  23. Jung S, Abbott A, Jesudurai C, Tomkins J, Main D (2005) Frequency, type, distribution and annotation of simple sequence repeats in Rosaceae ESTs. Funct Int Genome 5:136–143CrossRefGoogle Scholar
  24. Kieliszewski MJ, Lamport DT (1994) Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J 5:157–172CrossRefPubMedGoogle Scholar
  25. Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412PubMedGoogle Scholar
  26. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincon SE, Newburg L (1987) MapMaker: an interactive computer package for constructing primary genetic maps of experimental and natural populations. Genomics 1:174–181CrossRefPubMedGoogle Scholar
  27. Lewers KS, Styan SMN, Hokanson SC, Bassil NV (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 Hortic Sci 130:102–115Google Scholar
  28. Li JZ, Sjakste TG, Röder MS, Ganal MW (2003) Development and genetic mapping of 127 new microsatellite markers in barley. Theor Appl Genet 107:1021–1027CrossRefPubMedGoogle Scholar
  29. Monfort A, Vilanova S, Davis TM, Arús P (2005) A new set of polymorphic simple sequence repeat (SSR) markers from a wild strawberry (Fragaria vesca) are transferable to other diploid Fragaria species and to Fragaria × ananassa. Mol Ecol Notes; doi:10.1111/j.1471–8286.2005.01191.xGoogle Scholar
  30. Paran I, Michelmore RW (1993) Development of reliable PCR-based markers linked to downy mildew resistance genes in lettuce. Theor Appl Genet 85:985–993CrossRefGoogle Scholar
  31. Ramsay L, Macaulay M, degli Ivanissevich S, MacLean K, Cardle L, Fuller J, Edwards KJ, Tuvesson S, Morgante M, Massari M, Maestri E, Marmiroli N, Sjakste T, Ganal M, Powell W, Waugh W (2000) A simple sequence repeat-based linkage map of barley. Genetics 156:1997–2005PubMedGoogle Scholar
  32. Reiter WD, Vanzin GF (2001) Molecular genetics of nucleotide sugar interconversion pathways in plants. Plant Mol Biol 47:95–113CrossRefPubMedGoogle Scholar
  33. Rozen S, Skaletsky HJ (1998) PRIMER 3. Code available at
  34. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  35. Sanwen H, Baoxi Z, Milbourne D, Cardle L, Guimei Y, Jiazhen G (2000) Development of pepper SSR markers from sequence databases. Euphytica 117:163–167CrossRefGoogle Scholar
  36. Sargent DJ, Hadonou AM, Simpson DW (2003) Development and characterisation of polymorphic microsatellite markers from Fragaria viridis, a wild diploid strawberry. Mol Ecol Notes 3:550–552CrossRefGoogle Scholar
  37. Sargent DJ, Davis TM, Tobutt KR, Wilkinson MJ, Battey NH, Simpson DW (2004a) A genetic linkage map of microsatellite, gene specific and morphological markers in diploid Fragaria. Theor Appl Genet 109:1385–1391CrossRefGoogle Scholar
  38. Sargent DJ, Geibel M, Hawkins JA, Wilkinson MJ, Battey NH, Simpson DW (2004b) Quantitative and qualitative differences in morphological traits revealed between diploid Fragaria species. Ann Bot 94:787–796CrossRefGoogle Scholar
  39. Senanayake YDA, Bringhurst RS (1967) Origin of Fragaria polyploids I cytological analysis. Am J Bot 54:221–228CrossRefGoogle Scholar
  40. Taji T, Seki M, Yamaguchi-Shinozaki K, Kamada H, Giraudat J, Shinozaki K (1999) Mapping of 25 drought-inducible genes, RD and ERD, in Arabidopsis thaliana. Plant Cell Physiol 40:119–123PubMedGoogle Scholar
  41. Tang S, Yu JK, Slabaugh MB, Shintani DK, Knapp SJ (2002) Simple sequence repeat map of the sunflower genome. Theor Appl Genet 105:1124–1136CrossRefPubMedGoogle Scholar
  42. Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0: Software for the calculation of genetic linkage maps. Plant Research International, WageningenGoogle Scholar
  43. Voorrips RE (2002) MapChart: Software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefPubMedGoogle Scholar
  44. Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP—a new technique for DNA-fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  45. Wang Y, Georgi LL, Zhebentyayeva TN, Reighard GL, Scorza R, Abbott AG (2002) High-throughput targeted SSR marker development in peach (Prunus persica). Genome 45:319–328CrossRefPubMedGoogle Scholar
  46. Welsh J, McClelland M (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res 18:7213–7218PubMedCrossRefGoogle Scholar
  47. Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic-markers. Nucleic Acids Res 18:6531–6535PubMedCrossRefGoogle Scholar
  48. Yamamoto Y, Sato E, Shimizu T, Nakamich N, Sato S, Kato T, Tabata S, Nagatani A, Yamashino T, Mizuno T (2003) Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering time, and early photomorphogenesis. Plant Cell Physiol 44:1119–1130CrossRefPubMedGoogle Scholar
  49. Yan N, Doelling JH, Falbel TG, Durski AM, Vierstra RD (2000) The ubiquitin-specific protease family from Arabidopsis. AtUBP1 and 2 are required for the resistance to the amino acid analog canavanine. Plant Physiol 124:1828–1843CrossRefPubMedGoogle Scholar
  50. Zhou J, Rumeau D, Showalter AM (1992) Isolation and characterization of two wound-regulated tomato extensin genes. Plant Mol Biol 20:5–17CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • D. J. Sargent
    • 1
    • 6
    Email author
  • J. Clarke
    • 1
  • D. W. Simpson
    • 1
  • K. R. Tobutt
    • 1
  • P. Arús
    • 2
  • A. Monfort
    • 2
  • S. Vilanova
    • 2
  • B. Denoyes-Rothan
    • 3
  • M. Rousseau
    • 3
  • K. M. Folta
    • 4
  • N. V. Bassil
    • 5
  • N. H. Battey
    • 6
  1. 1.East Malling Research (EMR)KentUK
  2. 2.Departament de Genética VegetalInstitut de Recerca i Tecnologia Agroalimentáries (IRTA)Cabrils (Barcelona)Spain
  3. 3.INRA-Unité de Recherche sur les Espèces Fruitières et la VigneVillenave d’Ornon CedexFrance
  4. 4.Plant Molecular and Cellular Biology Program and Horticultural Sciences DepartmentThe University of FloridaGainesvilleUSA
  5. 5.USDA-ARS NCGRCorvallisUSA
  6. 6.School of Plant SciencesThe University of ReadingReadingUK

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