Theoretical and Applied Genetics

, Volume 123, Issue 5, pp 755–778 | Cite as

Quantitative trait loci and underlying candidate genes controlling agronomical and fruit quality traits in octoploid strawberry (Fragaria × ananassa)

  • Yasmín Zorrilla-Fontanesi
  • Amalia Cabeza
  • Pedro Domínguez
  • Juan Jesús Medina
  • Victoriano Valpuesta
  • Beatrice Denoyes-Rothan
  • José F. Sánchez-Sevilla
  • Iraida AmayaEmail author
Original Paper


Breeding for fruit quality traits in strawberry (Fragaria × ananassa, 2n = 8x = 56) is complex due to the polygenic nature of these traits and the octoploid constitution of this species. In order to improve the efficiency of genotype selection, the identification of quantitative trait loci (QTL) and associated molecular markers will constitute a valuable tool for breeding programs. However, the implementation of these markers in breeding programs depends upon the complexity and stability of QTLs across different environments. In this work, the genetic control of 17 agronomical and fruit quality traits was investigated in strawberry using a F1 population derived from an intraspecific cross between two contrasting selection lines, ‘232’ and ‘1392’. QTL analyses were performed over three successive years based on the separate parental linkage maps and a pseudo-testcross strategy. The integrated strawberry genetic map consists of 338 molecular markers covering 37 linkage groups, thus exceeding the 28 chromosomes. 33 QTLs were identified for 14 of the 17 studied traits and approximately 37% of them were stable over time. For each trait, 1–5 QTLs were identified with individual effects ranging between 9.2 and 30.5% of the phenotypic variation, indicating that all analysed traits are complex and quantitatively inherited. Many QTLs controlling correlated traits were co-located in homoeology group V, indicating linkage or pleiotropic effects of loci. Candidate genes for several QTLs controlling yield, anthocyanins, firmness and l-ascorbic acid are proposed based on both their co-localization and predicted function. We also report conserved QTLs among strawberry and other Rosaceae based on their syntenic location.


Quantitative Trait Locus Expansin Sweet Cherry Soluble Solid Content Linkage Group 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by grants RTA2008-00029-00-00 (INIA, partly funded by FEDER, European Union), AGR-03230 (CICE, Junta de Andalucía) and BIO2010-15630 (MEC). Y.Z-F. and I.A. were supported by a fellowship and a contract, respectively, from INIA. The authors would like to thank Luis Miranda for his excellent technical assistance in the field, Dr. E. Martínez-Ferri for statistical support, Dr. F. Csukasi for kindly providing the genomic sequence of FaTIR1, Dr. J.W. van Ooijen for helpful advice on mapping and QTL analysis and Dr. M.A. Botella for stimulating discussions and critical reading of the manuscript.

Supplementary material

122_2011_1624_MOESM1_ESM.doc (160 kb)
Supplementary tables (DOC 159 kb)
122_2011_1624_MOESM2_ESM.pdf (227 kb)
Fig. S1 (PDF 226 kb)
122_2011_1624_MOESM3_ESM.pdf (225 kb)
Fig. S2 (PDF 225 kb)


  1. Abbott AG, Rajapakse S, Sosinski B, Lu ZX, Sossey-Alaoui K, Gannavarapu M, Reighard G, Ballard RE, Baird WV, Scorza R, Callahan A (1998) Construction of saturated linkage maps of peach crosses segregating for characters controlling fruit quality, tree architecture and pest resistance. Acta Hortic 465:41–49Google Scholar
  2. Agius F, González-Lamonthe R, Caballero JL, Muñoz-Blanco J, Botella MA, Valpuesta V (2003) Engineering increased vitamin C levels in plants by over-expression of a d-galacturonic acid reductase. Nat Biotechnol 21:177–181PubMedCrossRefGoogle Scholar
  3. Aharoni A, Ric De Vos CH, Wein M, Sun Z, Greco R, Kroon A, Mol JNM, O’Connell AP (2001) The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J 28:319–332PubMedCrossRefGoogle Scholar
  4. Allan AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13:99–102PubMedCrossRefGoogle Scholar
  5. Andersson L, Haley CS, Ellegren H (1994) Genetic mapping of quantitative trait loci for growth and fatness in pigs. Science 263:1771–1774PubMedCrossRefGoogle Scholar
  6. Aubert G, Morin J, Jacquin F, Loridon K, Quillet M, Petit A, Rameau C, Lejeune-Hénaut I, Huguet T, Burstin J (2006) Functional mapping in pea, as an aid to the candidate gene approach and for investigating the synteny with the model species Medicago truncatula. Theor Appl Genet 112:1024–1041PubMedCrossRefGoogle Scholar
  7. Barden CL, Bramlage WJ (1994) Accumulation of antioxidants in apple peal as related to preharvest factors and superficial scald susceptibility of the fruit. J Am Soc Hortic Sci 119:264–269Google Scholar
  8. Blanco-Portales R, Medina-Escobar N, López-Ráez JA, González-Reyes JA, Villalba JM, Moyano E, Caballero JL, Muñoz Blanco J (2002) Cloning, expression and immunolocalization pattern of a cinnamyl alcohol dehydrogenase gene from strawberry (Fragaria × ananassa cv. Chandler). J Exp Bot 53:1723–1734PubMedCrossRefGoogle Scholar
  9. Bombarely A, Merchante C, Csukasi F, Cruz-Rus E, Caballero JL, Medina-Escobar N, Blanco-Portales R, Botella MA, Muñoz-Blanco J, Sánchez-Sevilla JF, Valpuesta V (2010) Generation and analysis of ESTs from strawberry (Fragaria × ananassa) fruits and evaluation of their utility in genetic and molecular studies. BMC Genomics 11:503PubMedCrossRefGoogle Scholar
  10. Brummell DA, Harpstera MH, Civello PM, Palys JM, Bennett AB, Dunsmuira P (1999) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11:2203–2216PubMedCrossRefGoogle Scholar
  11. Bustamante CA, Civello PM, Martínez GA (2009) Cloning of the promoter region of b-xylosidase (FaXyl1) gene and effect of plant growth regulators on the expression of FaXyl1 in strawberry fruit. Plant Sci 177:49–56CrossRefGoogle Scholar
  12. Cai Q, Guy CL, Moore GA (1994) Extension of the linkage map in Citrus using random amplified polymorphic DNA (RAPD) markers and RFLP mapping of cold-acclimation-responsive loci. Theor Appl Genet 89:606–614CrossRefGoogle Scholar
  13. Cameron J, Soost R (1977) Acidity and total soluble solids in Citrus hybrids and advanced crosses involving acidless orange and acidless pummelo. J Am Soc Hortic Sci 120:510–514Google Scholar
  14. Castillejo C, de la Fuente JI, Iannetta P, Botella MA, Valpuesta V (2004) Pectin esterase gene family in strawberry fruit: study of FaPE1, a ripening-specific isoform. J Exp Bot 55:909–918PubMedCrossRefGoogle Scholar
  15. Chagné D, Carlisle C, Blond C, Volz R, Whitworth C, Oraguzie N, Crowhurst R, Allan A, Espley R, Hellen R, Gardiner S (2007) Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8:212PubMedCrossRefGoogle Scholar
  16. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971PubMedGoogle Scholar
  17. Civello PM, Powell AL, Sabehat A, Bennett AB (1999) An expansin gene expressed in ripening strawberry fruit. Plant Physiol 121:1273–1280PubMedCrossRefGoogle Scholar
  18. Cong B, Barrero L, Tanksley S (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 40:800–804PubMedCrossRefGoogle Scholar
  19. Cosgrove DJ (2000a) Loosening of plant cell walls by expansins. Nature 407:321–326PubMedCrossRefGoogle Scholar
  20. Cosgrove DJ (2000b) New genes and new biological roles for expansins. Curr Opin Plant Biol 3:73–78PubMedCrossRefGoogle Scholar
  21. Costa F, Van de Weg WE, Stella S, Dondini L, Pratesi D, Musacchi S, Sansavini S (2008) Map position and functional allelic diversity of Md-Exp7, a new putative expansin gene associated with fruit softening in apple (Malus × domestica Borkh.) and pear (Pyrus communis). Tree Genet Genomes 4:575–586CrossRefGoogle Scholar
  22. Costa F, Peace CP, Stella S, Serra S, Musacchi S, Bazzani M, Sansavini S, Van de Weg WE (2010) QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (Malus × domestica Borkh.). J Exp Bot 61:3029–3039PubMedCrossRefGoogle Scholar
  23. Cruz-Rus E, Amaya I, Sanchez-Sevilla JF, Botella MA, Valpuesta V (2011) Regulation of l-ascorbic acid content in strawberry fruits. J Exp BotGoogle Scholar
  24. Darrow G (1966) The strawberry. Holt, Rinehart and Winston, New YorkGoogle Scholar
  25. Davey MW, Montagu MV, Inzé D, Sanmartin M, Kanellis A, Smirnoff N, Benzie IJ, Strain JJ, Favell D, Fletcher J (2000) Plant l-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J Sci Food Agric 80:825–860CrossRefGoogle Scholar
  26. Davey MW, Kenis K, Keulemans J (2006) Genetic control of fruit vitamin C contents. Plant Physiol 142:335–343CrossRefGoogle Scholar
  27. Davey MW, Auwerkerken A, Keulemans J (2007) Relationship of apple vitamin C and antioxidant contents to harvest date and postharvest pathogen infection. J Sci Food Agric 87:802–813CrossRefGoogle Scholar
  28. 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
  29. Di Matteo A, Sacco A, Anacleria M, Pezzotti M, Delledonne M, Ferrarini A, Frusciante L, Barone A (2010) The ascorbic acid content of tomato fruits is associated with the expression of genes involved in pectin degradation. BMC Plant Biol 10:163PubMedCrossRefGoogle Scholar
  30. Dirlewanger E, Moing A, Rothan C, Svanella L, Pronier V, Guye A, Plomion C, Monet R (1999) Mapping QTLs controlling fruit quality in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 98Google Scholar
  31. do Nascimento JR, Higuchi BK, Gómez M, Oshiro R, Lajolo FM (2005) l-Ascorbate biosynthesis in strawberries: l-galactono-1, 4-lactone dehydrogenase expression during fruit development and ripening. Postharvest Biol Technol 38:34–42CrossRefGoogle Scholar
  32. Doerge RW, Craig BA (2000) Model selection for quantitative trait locus analysis in polyploids. Proc Natl Acad Sci USA 97:7951–7956PubMedCrossRefGoogle Scholar
  33. Dotto MC, Martínez GA, Civello PM (2006) Expression of expansin genes in strawberry varieties with contrasting fruit firmness. Plant Phys Biochem 44:301–307CrossRefGoogle Scholar
  34. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  35. Eduardo I, Pacheco I, Chietera G, Bassi D, Pozzi C, Vecchietti A, Rossini L (2010) QTL analysis of fruit quality traits in two peach intraspecific populations and importance of maturity date pleiotropic effect. Tree Genet Genomes. doi: 10.1007/s11295-010-0334-6
  36. Etienne C, Moing A, Dirlewanger E, Raymond P, Monet R, Rothan C (2002a) Isolation and characterization of six peach cDNAs encoding key proteins in organic acid metabolism and solute accumulation: involvement in regulating peach fruit acidity. Physiol Plant 114:259–270PubMedCrossRefGoogle Scholar
  37. Etienne C, Rothan C, Moing A, Plomion C, Bodenes C, Svanella-Dumas L, Cosson P, Pronier V, Monet R, Dirlewanger E (2002b) Candidate genes and QTLs for sugar and organic acid content in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 105:145–159PubMedCrossRefGoogle Scholar
  38. Fait A, Hanhineva K, Beleggia R, Dai N, Rogachev I, Nikiforova VJ, Fernie AR, Aharoni A (2008) Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiol 148:730–750PubMedCrossRefGoogle Scholar
  39. Folta KM, Davis TM (2006) Strawberry genes and genomics. Crit Rev Plant Sci 25:399–415CrossRefGoogle Scholar
  40. Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88PubMedCrossRefGoogle Scholar
  41. Gentinetta E, Ceppi D, Lepori C, Perico G, Motto M (1986) A major gene for delayed senescence in maize. Pattern of photosynthates accumulation and inheritance. Plant Breed 97:193–203CrossRefGoogle Scholar
  42. Gil-Ariza DJ, Amaya I, Botella MA, Muñoz Blanco J, Caballero JL, López-Aranda JM, Valpuesta V, Sánchez-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
  43. Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137PubMedGoogle Scholar
  44. Hancock JF (1999) Strawberries. CABI Publishing, New YorkGoogle Scholar
  45. Hancock RD, Viola R (2005) Improving the nutritional value of crops through enhancement of l-ascorbic acid (vitamin C) content: rationale and biotechnological opportunities. J Agric Food Chem 53:5248–5257PubMedCrossRefGoogle Scholar
  46. Harapanhalli RS, Howel RW, Rao DV (1993) Testicular and plasma ascorbic acid levels in mice following dietary intake: a high-performance liquid chromatographic analysis. J Chromatogr 614:233–243PubMedCrossRefGoogle Scholar
  47. Harrison EP, McQueen-Mason SJ, Manning K (2001) Expression of six expansin genes in relation to extension activity in developing strawberry fruit. J Exp Bot 52:1437–1446PubMedCrossRefGoogle Scholar
  48. Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162PubMedCrossRefGoogle Scholar
  49. Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41:494–497PubMedCrossRefGoogle Scholar
  50. Illa E, Eduardo I, Audergon JM, Barale F, Dirlewanger E, Li X, Moing A, Lambert P, Le Dantec L, Gao Z, Poëssel J-L, Pozzi C, Rossini L, Vecchietti A, Arús P, Howad W (2011) Saturating the Prunus (stone fruits) genome with candidate genes for fruit quality. Mol Breed. doi: 10.1007/s11032-010-9518-x
  51. Illa E, Sargent DJ, Lopez Girona E et al (2011) Comparative analysis of rosaceous genomes and the reconstruction of a putative ancestral genome for the family. BMC Evol Biol 11. doi: 10.1186/1471-2148-1111-1189
  52. Jansen RC (1993) Interval mapping of multiple quantitative trait loci. Genetics 135:205–211PubMedGoogle Scholar
  53. Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455PubMedGoogle Scholar
  54. Jarrell DC, Roose ML, Traugh SN, Kupper RS (1992) A genetic map of Citrus based on the segregation of isozymes and RFLPs in an intergeneric cross. Theor Appl Genet 84:49–56CrossRefGoogle Scholar
  55. Jiménez-Bermúdez S, Redondo-Nevado J, Munoz-Blanco J, Caballero J, Lopez-Aranda J, Valpuesta V, Pliego-Alfaro F, Quesada M, Mercado J (2002) Manipulation of strawberry fruit softening by antisense expression of a pectate lyase gene. Plant Physiol 128:751–759PubMedCrossRefGoogle Scholar
  56. Keniry A, Hopkins C, 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
  57. Kenis K, Keulemans J (2007) Study of tree architecture of apple (Malus × domestica Borkh.) by QTL analysis of growth traits. Mol Breed 19:193–208CrossRefGoogle Scholar
  58. Kenis K, Keulemans J, Davey MW (2008) Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genomes 4:647–661CrossRefGoogle Scholar
  59. King GJ, Lynn JR, Dover CJ, Evans KM, Seymour GB (2001) Resolution of quantitative trait loci for mechanical measures accounting for genetic variation in fruit texture of apple (Malus pumila Mill.). Theor Appl Genet 2001:1227–1235CrossRefGoogle Scholar
  60. Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199PubMedGoogle Scholar
  61. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181PubMedCrossRefGoogle Scholar
  62. Landry BS, Hubert N, Etoh T, Harada JJ, Lincoln SE (1991) A genetic map for Brassica napus based on restriction fragment length polymorphisms detected with expressed DNA sequences. Genome 34:543–552CrossRefGoogle Scholar
  63. Lecerteau-Köhler E, Moing A, Guérin G, Renaud C, Courlit S, Camy K, Praud V, 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). Acta Hortic 663:331–335Google Scholar
  64. Lecerteau-Köhler E, Moing A, Guerin F, Renaud C, Maucourt M, Rolin D, Roudeillac P, Denoyes-Rothan B (2006) QTL analysis for sugars and organic acids in strawberry fruits. Acta Hortic 708:573–577Google Scholar
  65. Lerceteau-Köhler 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 107:619–628PubMedCrossRefGoogle Scholar
  66. Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C (2003) Mapping quantitative physiological traits in apple (Malus × domestica Borkh.). Plant Mol Biol 52:511–526PubMedCrossRefGoogle Scholar
  67. López-Aranda JM (2008) Origin of the crop: a pioneer. In: Junta de Andalucía (ed) The cultivation of strawberry in Huelva, pp 101–170Google Scholar
  68. Lorence A, Chevone BI, Mendes P, Nessler CL (2004) Myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol 134:1200–1205PubMedCrossRefGoogle Scholar
  69. Lyttle T (1991) Segregation distorters. Annu Rev Genet 25:511–557PubMedCrossRefGoogle Scholar
  70. Maccaferri M, Sanguineti M, Corneti S, Araus Ortega J, Ben Salem M, Bort J, DeAmbrogio E, Garcia del Moral L, Demontis A, El-Ahmed A, Maalouf F, Machlab H, Martos V, Moragues M, Motawaj J, Nachit M, Nserallah N, Ouabbou H, Royo C, Slama A, Tuberosa R (2008) Quantitative trait loci for grain yield and adaptation of durum wheat (Triticum durum Desf.) across a wide range of water availability. Genetics 178:489–511PubMedCrossRefGoogle Scholar
  71. Maliepaard C, Jansen J, van Ooijen J (1997) Linkage analysis in a full-sib family of an outbreeding species: overview and consequences for applications. Genet Res 70:237–250CrossRefGoogle Scholar
  72. Maliepaard C, Alston F, Arkel G, Brown L, Chevreau E, Dunemann F, Evans KM, Gardiner S, Guilford P, van Heusden A, Janse J, Laurens F, Lynn J, Manganaris A, Nijs A, Periam N, Rikkerink E, Roche P, Ryder C, Sansavini S, Schmidt H, Tartarini S, Verhaegh JJ, Vrielink-van Ginkel M, King G (1998) Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet 97:60–73CrossRefGoogle Scholar
  73. Martin C, Ellis N, Rook F (2010) Do transcription factors play special roles in adaptive variation? Future Perspect Plant Biol 154:506–511Google Scholar
  74. McCallum S, Woodhead M, Hackett C, Kassim A, Paterson A, Graham J (2010) Genetic and environmental effects influencing fruit colour and QTL analysis in raspberry. Theor Appl Genet 121:611–627PubMedCrossRefGoogle Scholar
  75. McGuire RG (1992) Reporting of objective color measurements. HortScience 27:1254–1255Google Scholar
  76. Medina-Minguez JJ (2008) Origin of the crop: a pioneer. In: Junta de Andalucía (ed) The strawberry crop at Huelva Sevilla, Spain, pp 17–46Google Scholar
  77. Ogundiwin EA, Peace CP, Nicolet CM, Rashbrook VK, Gradziel TM, Bliss FA, Parfitt D, Crisosto CH (2008) Leucoanthocyanidin dioxygenase gene (PpLDOX): a potential functional marker for cold storage browning in peach. Tree Genet Genomes 4:543–554CrossRefGoogle Scholar
  78. Ogundiwin EA, Peace CP, Gradziel TM, Parfitt DE, Bliss FA, Crisosto CH (2009) A fruit quality gene map of Prunus. BMC Genomics 10:587PubMedCrossRefGoogle Scholar
  79. Orita M, Suzuki Y, Sekiya T, Hayashi K (1989) Rapid and sensitive detection of point mutations and DNA polymorphisms using the polymerase chain reaction. Genomics 5:874–879PubMedCrossRefGoogle Scholar
  80. Paterson A, Lander E, Hewitt J, Peterson S, Lincoln S, Tanksley S (1988) Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature 335:721–726PubMedCrossRefGoogle Scholar
  81. Peace CP, Crisosto CH, Gradziel TM (2005) Endopolygalacturonase: a candidate gene for Freestone and Melting flesh in peach. Mol Breed 16:21–31CrossRefGoogle Scholar
  82. Perkins-Veazie P (1995) Growth and ripening of strawberry fruit. Hort Rev 17:197–267Google Scholar
  83. Pierce RO, Knowles PF, Phillips DA (1984) Inheritance of delayed leaf senescence in soybean. Crop Sci 24:515–518CrossRefGoogle Scholar
  84. Prince JP, Pochard E, Tanksley SD (1993) Construction of a molecular linkage map of pepper and a comparison of synteny with tomato. Genome 36:404–417PubMedCrossRefGoogle Scholar
  85. Quilot B, Wu BH, Kervella J, Genard M, Foulongne M, Moreau K (2004) QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theor Appl Genet 109:884–897PubMedCrossRefGoogle Scholar
  86. Redondo-Nevado J, Moyano E, Medina-Escobar N, Caballero JL, Muñoz-Blanco J (2001) A fruit-specific and developmentally regulated endopolygalacturonase gene from strawberry (Fragaria × ananassa cv.Chandler). J Exp Bot 52:1941–1945PubMedCrossRefGoogle Scholar
  87. 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 179:2045–2060PubMedCrossRefGoogle Scholar
  88. 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 51:515–530PubMedCrossRefGoogle Scholar
  89. Rousseaux MC, Jones CM, Adams D, Chetelat R, Bennett A, Powell A (2005) QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines. Theor Appl Genet 111:1396–1408PubMedCrossRefGoogle Scholar
  90. Sainz M, Grotewold E, Chandler V (1997) Evidence for direct activation of an anthocyanin promoter by the maize C1 protein and comparison of DNA binding by related Myb domain proteins. Plant Cell 9:611–625PubMedCrossRefGoogle Scholar
  91. Saliba-Colombani V, Causse M, Langlois D, Philouze J, Buret M (2001) Genetic analysis of organoleptic quality in fresh market tomato. 1. Mapping QTLs for physical and chemical traits. Theor Appl Genet 102:259–272CrossRefGoogle Scholar
  92. 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 109:1385–1391PubMedCrossRefGoogle Scholar
  93. 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 112:1349–1359PubMedCrossRefGoogle Scholar
  94. 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 114:373–384PubMedCrossRefGoogle Scholar
  95. 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 51:120–127PubMedCrossRefGoogle Scholar
  96. Sargent D, Fernandez-Fernandez F, Ruiz-Rojas JJ, Sutherland BG, Passey A, Withehouse 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 24:293–303CrossRefGoogle Scholar
  97. Sato Y, Morita R, Nishimura M, Yamaguchi H, Kusaba M (2007) Mendel’s green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway. Proc Natl Acad Sci 104:14169–14174PubMedCrossRefGoogle Scholar
  98. Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24:447–454PubMedCrossRefGoogle Scholar
  99. Schittenhelm S, Menge-Hartmann U, Oldenburg E (2004) Photosynthesis, carbohydrate metabolism, and yield of phytochrome-B-overexpressing potatoes under different light regimes. Crop Sci 44:131–143CrossRefGoogle Scholar
  100. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611Google Scholar
  101. Shaw DV (1997) Trait mean depression for second-generation inbred strawberry populations with and without parent selection. Theor Appl Genet 95:261–264CrossRefGoogle Scholar
  102. Shi J, Li R, Qiu D, Jiang C, Long Y, Morgan C, Bancroft I, Zhao J, Meng J (2009) Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182:851–861PubMedCrossRefGoogle Scholar
  103. Shulaev V, Sargent DJ, Crowhurst RN et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–118PubMedCrossRefGoogle Scholar
  104. Sooriyapathirana S, Khan A, Sebolt A, Wang D, Bushakra J, Lin-Wang K, Allan A, Gardiner S, Chagné D, Iezzoni A (2010) QTL analysis and candidate gene mapping for skin and flesh color in sweet cherry fruit (Prunus avium L.). Tree Genet Genomes 6:821–832CrossRefGoogle Scholar
  105. Spano G, Di Fonzo N, Perrotta C, Platani C, Ronga G (2003) Physiological characterization of ‘stay green’ mutants in durum wheat. J Exp Bot 54:1415–1420PubMedCrossRefGoogle Scholar
  106. Srinivas G, Satish K, Madhusudhana R, Nagaraja Reddy R, Murali Mohan S, Seetharama N (2009) Identification of quantitative trait loci for agronomically important traits and their association with genic-microsatellite markers in sorghum. Theor Appl Genet 118:1439–1454PubMedCrossRefGoogle Scholar
  107. Stam P (1993) Construction of integrated linkage maps by means of a new computer package: JoinMap. Plant J 3:739–744CrossRefGoogle Scholar
  108. Stevens R, Buret M, Duffe P, Garchery C, Baldet P, Rothan C, Causse M (2007) Candidate genes and quantitative trait loci affecting fruit ascorbic acid content in three tomato populations. Plant Physiol 143:1943–1953PubMedCrossRefGoogle Scholar
  109. Stevens R, Page D, Gouble B, Garchery C, Zamir D, Causse M (2008) Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ 31:1086–1096PubMedCrossRefGoogle Scholar
  110. Tanksley S (1993) Mapping polygenes. Annu Rev Genet 27:205–233PubMedCrossRefGoogle Scholar
  111. Trainotti L, Ferrarese L, Dalla Vecchia F, Rascio N, Casadoro G (1999a) Two different endo-β-1, 4-glucanases contribute to the softening of the strawberry fruits. J Plant Physiol 154:355–362Google Scholar
  112. Trainotti L, Spolaore S, Pavanello A, Baldan B, Casadoro G (1999b) A novel E-type endo-β-1, 4-glucanase with a putative cellulose-binding domain is highly expressed in ripening strawberry fruits. Plant Mol Biol 40:323–332PubMedCrossRefGoogle Scholar
  113. Valpuesta V, Botella MA (2004) Biosynthesis of l-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci 9:573–577PubMedCrossRefGoogle Scholar
  114. van Ooijen JW (2004) MapQTL® 5, software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, WageningenGoogle Scholar
  115. van Ooijen JW (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, WageningenGoogle Scholar
  116. Veltman RH, Kho RM, van Schaik ACR, Sanders MG, Oosterhaven J (2000) Ascorbic acid and tissue browning in pears (Pyrus communis L. cvs Rocha and Conference) under controlled atmosphere conditions. Postharvest Biol Technol 19:129–137CrossRefGoogle Scholar
  117. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  118. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M et al (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  119. Walulu RS, Rosenow DT, Wester DB, Nguyen HT (1994) Inheritance of the stay-green trait in sorghum. Crop Sci 34:970–972CrossRefGoogle Scholar
  120. 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 127:94–101Google Scholar
  121. Woodward JR (1972) Physical and chemical changes in developing strawberry fruits. J Sci Food Agric 23:465–473PubMedCrossRefGoogle Scholar
  122. Xu Y, Zhang L, Xie H, Zhang YQ, Oliveira MM, Ma RC (2008) Expression analysis and genetic mapping of three SEPALLATA-like genes from peach (Prunus persica (L.) Batsch). Tree Genet Genomes 4:693–703CrossRefGoogle Scholar
  123. Yin T, Huang M, Wang M, Zhu L-H, Zeng Z-B, Wu R (2001) Preliminary interespecific genetic maps of the Populus genome constructed from RAPD markers. Genome 44:602–609PubMedGoogle Scholar
  124. Yoshida M (1970) Genetical studies on the fruit quality of peach varieties. I. Acidity. Bull Hortic Res Stn Jpn Ser A 9:1–15Google Scholar
  125. Yoshida K, Toyama-Kato Y, Kameda K, Kondo T (2003) Sepal colour variation of Hydrangea macrophylla and vacuolar pH measured with a proton-selective microelectrode. Plant Cell Physiol 44:262–268PubMedCrossRefGoogle Scholar
  126. Zhang G, Sebolt AM, Sooriyapathirana SS, Wang D, Bink MC, Olmstead JW, Iezzoni AF (2010) Fruit size QTL analysis of an F1 population derived from a cross between a domesticated sweet cherry cultivar and a wild forest sweet cherry. Tree Genet Genomes 6:25–36CrossRefGoogle Scholar
  127. Zorrilla-Fontanesi Y, Cabeza A, Torres AM, Botella MA, Valpuesta V, Monfort A, Sánchez-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 27:137–156CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Yasmín Zorrilla-Fontanesi
    • 1
  • Amalia Cabeza
    • 1
  • Pedro Domínguez
    • 2
  • Juan Jesús Medina
    • 2
  • Victoriano Valpuesta
    • 3
  • Beatrice Denoyes-Rothan
    • 4
  • José F. Sánchez-Sevilla
    • 1
  • Iraida Amaya
    • 1
    Email author
  1. 1.IFAPA-Centro de ChurrianaMálagaSpain
  2. 2.IFAPA-Centro Las TorresSevillaSpain
  3. 3.Departamento de Biología Molecular y BioquímicaInstituto de Hortofruticultura Subtropical y Mediterránea, Universidad de Málaga-Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC)MálagaSpain
  4. 4.Institut National de la Recherche Agronomique, UREF, BP81, INRA, UR 419Villenave d’Ornon CedexFrance

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