Advertisement

Molecular Breeding

, Volume 27, Issue 2, pp 137–156 | Cite as

Development and bin mapping of strawberry genic-SSRs in diploid Fragaria and their transferability across the Rosoideae subfamily

  • Yasmín Zorrilla-Fontanesi
  • Amalia Cabeza
  • Ana M. Torres
  • Miguel A. Botella
  • Victoriano Valpuesta
  • Amparo Monfort
  • José F. Sánchez-Sevilla
  • Iraida AmayaEmail author
Article

Abstract

Cultivated strawberry (Fragaria × ananassa) together with other economically important genera such as Rosa (roses) and Rubus (raspberry and blackberry) belongs to the subfamily Rosoideae. There is increasing interest in the development of transferable markers to allow genome comparisons within the Rosaceae family. In this report, 122 new genic microsatellite (SSR) markers have been developed from cultivated strawberry and its diploid ancestor Fragaria vesca. More than 77% of the sequences from which the markers were developed show significant homology to known or predicted proteins and more than 92% were polymorphic among strawberry cultivars, representing valuable markers in transcribed regions of the genome. Sixty-three SSRs were polymorphic in the diploid Fragaria reference population and were bin-mapped together with another five previously reported but unmapped markers. In total, 72 loci were distributed across the seven linkage groups. In addition, the transferability of 174 Fragaria SSRs to the related Rosa and Rubus genera was investigated, ranging from 28.7% for genic-SSRs in rose to 16.1% for genomic-SSRs in raspberry. Among these markers, 33 and 16 were both localized in the diploid Fragaria reference map and cross-amplified in rose and raspberry, respectively. These results indicate that transferability of SSRs across the Rosoideae subfamily is limited. However, we have identified a set of Fragaria markers, polymorphic in the diploid reference population, which cross-amplified in both Rosa and Rubus, which represents a valuable tool for comparative mapping and genetic diversity analyses within the Rosoideae subfamily.

Keywords

Comparative mapping Synteny Strawberry Rose Raspberry Rosoideae 

Notes

Acknowledgments

This work was supported by grants RTA2008-00029-00-00 (INIA, partly funded by FEDER, European Union), AGR-03230 (CICE, Junta de Andalucía) and BIO2007-67509-C02-01 (MEC). The IFAPA Fragaria germplasm collection is funded by grant RFP2008-00009-00-00 (INIA). At CRAG, this work was supported with funds of the Spanish Ministry of Science and Innovation, project RTA2007-00063-00-00 (INIA). Y.Z-F. was supported by a fellowship and I.A. by a contract from INIA. We are gratefull to E. Cruz-Rus for obtaining the genomic sequence of GaLUR.

Ethical standards

The experiments of this study comply with the current laws of Spain.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11032_2010_9417_MOESM1_ESM.doc (44 kb)
Supplementary material 1 (DOC 43 kb)

References

  1. Akiyama Y, Yamamoto Y, Ohmido N, Oshima M, Fukui K (2001) Estimation of the nuclear DNA content of strawberries (Fragaria ssp.) compared with Arabidopsis thaliana by using dual-stem flow cytometry. Cytologia 66:431–436Google Scholar
  2. 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 109:571–579CrossRefPubMedGoogle Scholar
  3. Arnold C, Rossetto M, McNally J, Henry RJ (2002) The application of SSRs characterized for grape (Vitis vinifera) to conservation studies in Vitaceae. Am J Bot 89:22–28CrossRefGoogle Scholar
  4. 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 107:1201–1207CrossRefPubMedGoogle Scholar
  5. Bassil NV, Gunn M, Folta K, Lewers K (2006a) Microsatellite markers for Fragaria from ‘Strawberry Festival’ expressed sequence tags. Mol Ecol Notes 6:473–476CrossRefGoogle Scholar
  6. Bassil NV, Njuguna W, Slovin JP (2006b) EST-SSR markers from Fragaria vesca L. cv. yellow wonder. Mol Ecol Notes 6:806–809CrossRefGoogle Scholar
  7. Benbouza H, Jacquemin J, Baudoin JP, Mergeai G (2006) Optimization of a reliable, fast, cheap and sensitive silver staining method to detect SSR markers in polyacrylamide gels. Biotechnol Agron Soc Environ 10:77–81Google Scholar
  8. Cekic C, Battey NH, Wilkinson MJ (2001) The potential of ISSR-PCR primer-pair combinations for genetic linkage analysis using the seasonal flowering locus in Fragaria as a model. Theor Appl Genet 103:540–546CrossRefGoogle Scholar
  9. Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406CrossRefPubMedGoogle Scholar
  10. Cheng FS, Brown SK, Weeden NF (1997) A DNA extraction protocol from various tissues in woody species. Hortscience 32:921–922Google Scholar
  11. Cipriani G, Testolin R (2004) Isolation and characterization of microsatellite loci in Fragaria. Mol Ecol Notes 4:366–368CrossRefGoogle Scholar
  12. Cobb BD, Clarkson JM (1994) A simple procedure for optimising the polymerase chain reaction (PCR) using modified Taguchi methods. Nucleic Acids Res 22:3801–3805CrossRefPubMedGoogle Scholar
  13. Davis TM, Yu H (1997) A linkage map of the diploid strawberry, Fragaria vesca. J Hered 88:215–221Google Scholar
  14. Davis TM, DiMeglio LM, Yang RH, Styan SMN, Lewers KS (2006) Assessment of SSR marker transfer from the cultivated strawberry to diploid strawberry species: Functionality, linkage group assignment, and use in diversity analysis. J Am Soc Hort Sci 131:506–512Google Scholar
  15. Davis T, Denoyes-Rothan B, Lecerteau-Köhler E (2007) Strawberry. In: Kole C (ed) Genome mapping and molecular breeding in plants: fruits and nuts. Springer, Berlin, pp 189–206Google Scholar
  16. Decroocq V, Fave 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
  17. 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
  18. Devos KM, Gale MD (2000) Genome relationships: the grass model in current research. Plant Cell 12:637–646CrossRefPubMedGoogle Scholar
  19. Dirlewanger E, Graziano E, Joobeur T, Garriga-Caldere F, Cosson P, Howad W, Arus P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA 101:9891–9896CrossRefPubMedGoogle Scholar
  20. Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002) A comparative genetic linkage map of eggplant (Solanum melongena) and its implications for genome evolution in the solanaceae. Genetics 161:1697–1711PubMedGoogle Scholar
  21. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  22. Dugo ML, Satovic Z, Millan T, Cubero JI, Rubiales D, Cabrera A, Torres AM (2005) Genetic mapping of QTLs controlling horticultural traits in diploid roses. Theor Appl Genet 111:511–520CrossRefPubMedGoogle Scholar
  23. Ferguson ME, Burow MD, Schulze SR, Bramel PJ, Paterson AH, Kresovich S, Mitchell S (2004) Microsatellite identification and characterization in peanut (A. hypogaea L.). Theor Appl Genet 108:1064–1070CrossRefPubMedGoogle Scholar
  24. Fernandez-Silva I, Eduardo I, Blanca J, Esteras C, Pico B, Nuez F, Arus P, Garcia-Mas J, Monforte AJ (2008) Bin mapping of genomic and EST-derived SSRs in melon (Cucumis melo L.). Theor Appl Genet 118:139–150CrossRefPubMedGoogle Scholar
  25. Folta KM, Davis TM (2006) Strawberry genes and genomics. Crit Rev Plant Sci 25:399–415CrossRefGoogle Scholar
  26. Frary A, Xu YM, Liu JP, Mitchell S, Tedeschi E, Tanksley S (2005) Development of a set of PCR-based anchor markers encompassing the tomato genome and evaluation of their usefulness for genetics and breeding experiments. Theor Appl Genet 111:291–312CrossRefPubMedGoogle Scholar
  27. Gasic K, Han YP, Kertbundit S, Shulaev V, Iezzoni AF, Stover EW, Bell RL, Wisniewski ME, Korban SS (2009) Characteristics and transferability of new apple EST-derived SSRs to other Rosaceae species. Mol Breed 23:397–411CrossRefGoogle Scholar
  28. Gil-Ariza DJ, Amaya I, Botella MA, Blanco JM, Caballero JL, Lopez-Aranda JM, Valpuesta V, Sanchez-Sevilla JF (2006) EST-derived polymorphic microsatellites from cultivated strawberry (Fragaria × ananassa) are useful for diversity studies and varietal identification among Fragaria species. Mol Ecol Notes 6:1195–1197CrossRefGoogle Scholar
  29. Gil-Ariza D, Amaya I, Lopez-Aranda JM, Botella MA, Valpuesta V, Sanchez-Sevilla JF (2009) Impact of plant breeding on the genetic diversity of cultivated strawberry as revealed by expressed sequence tag-derived simple sequence repeat markers. J Am Soc Hort Sci 134:337–347Google Scholar
  30. Gisbert A, Martínez-Calvo J, Llácer G, Badenes M, Romero C (2009) Development of two loquat [Eriobotrya japonica (Thunb.) Lindl.] linkage maps based on AFLPs and SSR markers from different Rosaceae species. Mol Breed 23:523–538CrossRefGoogle Scholar
  31. Govan CL, Simpson DW, Johnson AW, Tobutt KR, Sargent DJ (2008) A reliable multiplexed microsatellite set for genotyping Fragaria and its use in a survey of 60 F. × ananassa cultivars. Mol Breed 22:649–661CrossRefGoogle Scholar
  32. Gupta PK, Rustgi S, Sharma S, Singh R, Kumar N, Balyan HS (2003) Transferable EST-SSR markers for the study of polymorphism and genetic diversity in bread wheat. Mol Genet Genomics 270:315–323CrossRefPubMedGoogle Scholar
  33. Hadonou M, Sargent D, Walden R, Simpson D (2004) Characterisation of Fragaria vesca single sequence repeats (SSR) markers. Proceedings of the Euro Berry Symposium–Cost 836 Final Worskhop, pp 99–102Google Scholar
  34. Haymes KM, Henken B, Davis TM, Van de Weg WE (1997) Identification of RAPD markers linked to a Phytophthora fragariae resistance gene (Rpf1) in the cultivated strawberry. Theor Appl Genet 94:1097–1101CrossRefGoogle Scholar
  35. Hokanson SC, Maas J (2001) Strawberry biotechnology. Plant Breed Rev 21:139–180Google Scholar
  36. Howad W, Yamamoto T, Dirlewanger E, Testolin R, Cosson P, Cipriani G, Monforte AJ, Georgi L, Abbott AG, Arus P (2005) Mapping with a few plants: using selective mapping for microsatellite saturation of the Prunus reference map. Genetics 171:1305–1309CrossRefPubMedGoogle Scholar
  37. Jennings DL (1988) Raspberries and blackberries: their breeding, diseases and growth. Academic, LondonGoogle Scholar
  38. Kalo P, Seres A, Taylor SA, Jakab J, Kevei Z, Kereszt A, Endre G, Ellis THN, Kiss GB (2004) Comparative mapping between Medicago sativa and Pisum sativum. Mol Genet Genomics 272:235–246CrossRefPubMedGoogle Scholar
  39. Keniry A, Hopkins CJ, Jewell E, Morrison B, Spangenberg GC, Edwards D, Batley J (2006) Identification and characterization of simple sequence repeat (SSR) markers from Fragaria × ananassa expressed sequences. Mol Ecol Notes 6:319–322CrossRefGoogle Scholar
  40. Kuleung C, Baenziger PS, Dweikat I (2004) Transferability of SSR markers among wheat, rye, and triticale. Theor Appl Genet 108:1147–1150CrossRefPubMedGoogle Scholar
  41. Lerceteau-Kohler E, Guerin G, Laigret F, Denoyes-Rothan B (2003) Characterization of mixed disomic and polysomic inheritance in the octoploid strawberry (Fragaria × ananassa) using AFLP mapping. Theor Appl Genet 107:619–628CrossRefPubMedGoogle Scholar
  42. Lerceteau-Kohler E, Moing F, Gurin G, Renaud C, Courlit S, Camy D, Praud K, Parisy V, Bellec F, Maucourt M, Rolin D, Roudeillac P, Denoyes-Rothan B (2004) QTL analysis for fruit quality traits in octoploid strawberry (Fragaria × ananassa). Proceedings of the XIth Eucarpia Symposium on Fruit Breeding and Genetics, Vols 1 and 2:331–335Google Scholar
  43. 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 Hort Sci 130:102–115Google Scholar
  44. Lukens L, Zou F, Lydiate D, Parkin I, Osborn T (2003) Comparison of a Brassica oleracea genetic map with the genome of Arabidopsis thaliana. Genetics 164:359–372PubMedGoogle Scholar
  45. Monfort A, Vilanova S, Davis TM, Arus P (2006) 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 6:197–200CrossRefGoogle Scholar
  46. Pierantoni L, Cho KH, Shin IS, Chiodini R, Tartarini S, Dondini L, Kang SJ, Sansavini S (2004) Characterisation and transferability of apple SSRs to two European pear F-1 populations. Theor Appl Genet 109:1519–1524CrossRefPubMedGoogle Scholar
  47. Potter D, Eriksson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Plant System Evol 266:5–43CrossRefGoogle Scholar
  48. Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–857CrossRefPubMedGoogle Scholar
  49. Rousseau-Gueutin M, Lerceteau-Kohler 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 179:2045–2060CrossRefPubMedGoogle Scholar
  50. Rousseau-Gueutin M, Gaston A, Ainouche A, Ainouche ML, Olbricht K, Staudt G, Richard L, Denoyes-Rothan B (2009) Tracking the evolutionary history of polyploidy in Fragaria L. (strawberry): new insights from phylogenetic analyses of low-copy nuclear genes. Mol Phylogenet Evol 51:515–530CrossRefPubMedGoogle Scholar
  51. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Meth Mol Biol 132:365–386Google Scholar
  52. 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 109:1385–1391CrossRefPubMedGoogle Scholar
  53. 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 112:1349–1359CrossRefPubMedGoogle Scholar
  54. 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 114:373–384CrossRefPubMedGoogle Scholar
  55. 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 51:120–127CrossRefPubMedGoogle Scholar
  56. Sargent DJ, Fernandez-Fernandez F, Ruiz-Roja JJ, Sutherland BG, Passey A, Whitehouse AB, Simpson DW (2009a) A genetic linkage map of cultivated strawberry (Fragaria × ananassa) and its comparison to the diploid Fragaria reference map. Mol Breed 24:293–303CrossRefGoogle Scholar
  57. Sargent DJ, Marchese A, Simpson DW, Howad W, Fernandez-Fernandez F, Monfort A, Arus P, Evans KM, Tobutt KR (2009b) Development of “universal” gene-specific markers from Malus spp. cDNA sequences, their mapping and use in synteny studies within Rosaceae. Tree Genet Genome 5:133–145CrossRefGoogle Scholar
  58. Shulaev V, Korban SS, Sosinski B, Abbott AG, Aldwinckle HS, Folta KM, Iezzoni A, Main D, Arus P, Dandekar AM, Lewers K, Brown SK, Davis TM, Gardiner SE, Potter D, Veilleux RE (2008) Multiple models for Rosaceae genomics. Plant Physiol 147:985–1003CrossRefPubMedGoogle Scholar
  59. Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh.) genome. Tree Genet Genome 2:202–224CrossRefGoogle Scholar
  60. Tang JF, Gao LF, Cao YS, Jia JZ (2006) Homologous analysis of SSR-ESTs and transferability of wheat SSR-EST markers across barley, rice and maize. Euphytica 151:87–93CrossRefGoogle Scholar
  61. Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422PubMedGoogle Scholar
  62. Torres AM, Weeden NF, Martin A (1993) Linkage among isozyme, RFLP and RADP markers in Vicia faba. Theor Appl Genet 85:937–945CrossRefGoogle Scholar
  63. Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23:48–55CrossRefPubMedGoogle Scholar
  64. Vilanova S, Sargent DJ, Arus P, Monfort A (2008) Synteny conservation between two distantly-related Rosaceae genomes: Prunus (the stone fruits) and Fragaria (the strawberry). BMC Plant Biol 8:67CrossRefPubMedGoogle Scholar
  65. Vision TJ, Brown DG, Shmoys DB, Durrett RT, Tanksley SD (2000) Selective mapping: a strategy for optimizing the construction of high-density linkage maps. Genetics 155:407–420PubMedGoogle Scholar
  66. Bombarely A, Merchante C-, Csukasi F, Cruz-Rus E, Caballero JL, Medina-Escobar N, Botella MA, Muñoz-Blanco J, Valpuesta V, Sanchez-Sevilla JF (submitted) Generation and analysis of ESTs from strawberry (Fragaria × ananassa) fruits and evaluation of their utility in genetic and molecular studies. BMC GenomicsGoogle Scholar
  67. Yamamoto T, Kirnura T, Saito T, Kotobuki K, Matsuta N, Liebhard R, Gessler C, van de Weg WE, Hayashi T (2004) Genetic linkage maps of Japanese and European pears aligned to the apple consensus map. Proceedings of the XIth Eucarpia Symposium on Fruit Breeding and Genetics, Vols 1 and 2: 51–56Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Yasmín Zorrilla-Fontanesi
    • 1
  • Amalia Cabeza
    • 1
  • Ana M. Torres
    • 2
  • Miguel A. Botella
    • 3
  • Victoriano Valpuesta
    • 3
  • Amparo Monfort
    • 4
  • José F. Sánchez-Sevilla
    • 1
  • Iraida Amaya
    • 1
    Email author
  1. 1.IFAPA-Centro de ChurrianaMálagaSpain
  2. 2.IFAPA-Centro Alameda del ObispoCórdobaSpain
  3. 3.Departamento de Biología Molecular y BioquímicaUniversidad de MálagaMálagaSpain
  4. 4.IRTA-Centre de Recerca en Agrigenòmica CSIC-IRTA-UABCabrils (Barcelona)Spain

Personalised recommendations