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Genome-Assisted Breeding in the Octoploid Strawberry

  • Sujeet Verma
  • Luis F. Osorio
  • Seonghee Lee
  • Nahla V. Bassil
  • Vance M. Whitaker
Chapter
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

The application of genomic information to the breeding of allo-octoploid (2n = 8x = 56) cultivated strawberry (Fragaria × ananassa) has increased rapidly in the last five years. These advances have been fueled by technological improvements in high-throughput genotyping and genome sequencing, as well as concerted efforts to develop DNA tests for routine use in breeding. Genome-wide and subgenome-specific markers have advanced availability of DNA tests for major loci, as well as the development and validation of genomic selection methodology for complex traits in strawberry. Eight DNA tests for fruit quality and disease resistance loci are fully or partially in the public sphere. Genome-wide predictions have delivered genetic gain efficiencies for parent selection larger than 50% of conventional methods but without the need for phenotypic information. Meanwhile, the construction of haploblocks and haplotypes allows increased understanding of genome structure as it relates to breeding applications. With octoploid sequence assemblies merely months away and the development of gene editing technologies, precision manipulation of genes may shape the future of strawberry genetic improvement.

References

  1. 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
  2. Alexander L (2016) Rapid, effective DNA isolation from Osmanthus via modified alkaline lysis. J Biomol Tech 27:53–60PubMedPubMedCentralGoogle Scholar
  3. Anciro A, Mangandi J, Verma S, Whitaker V, Lee S (2016) Identification of quantitative trait loci and molecular markers for resistance to Colletotrichum crown rot in strawberry. Phytopathology 106(S2):6.  https://doi.org/10.1094/PHYTO-106-4-S2.6CrossRefGoogle Scholar
  4. Antanaviciute L, Šurbanovski N, Harrison N, McLeary KJ, Simpson DW, Wilson F, Sargent DJ, Harrison RJ (2015) Mapping QTL associated with Verticillium dahliae resistance in the cultivated strawberry (Fragaria × ananassa). Hortic Res 2:15009CrossRefPubMedPubMedCentralGoogle Scholar
  5. Auinger H-J, Schönleben N, Lehermeier C, Schmidt M, Korzun V, Geiger HH, Piepho H-P, Gordillo A, Wilde P, Bauer E, Schön C-C (2016) Model training across multiple breeding cycles significantly improves genomic prediction accuracy in rye (Secale cereale L.). Theor Appl Genet 129:2043–2053CrossRefPubMedPubMedCentralGoogle Scholar
  6. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265CrossRefPubMedGoogle Scholar
  7. Bassil NV, Davis TM, Zhang H, Ficklin S, Mittmann M, Webster T, Mahoney L, Wood D, Alperin ES, Rosyara UR, Koehorst-vanc Putten H, Monfort A, Sargent DJ, Amaya I, Denoyes B, Bianco L, van Dijk T, Pirani A, Iezzoni A, Main D, Peace C, Yang Y, Whitaker V, Verma S, Bellon L, Brew F, Herrera R, van de Weg E (2015) Development and preliminary evaluation of a 90K Axiom® SNP array for the allo-octoploid cultivated strawberry Fragaria × ananassa. BMC Genom 16:1CrossRefGoogle Scholar
  8. Bernardo R, Yu J (2007) Prospects for genomewide selection for quantitative traits in maize. Crop Sci 47:1082–1089CrossRefGoogle Scholar
  9. Bink MCAM, Jansen J, Madduri M, Voorrips RE, Durel C-E, Kouassi AB, Laurens F, Mathis F, Gessler C, Gobbin D, Rezzonico F, Patocchi A, Kellerhals M, Boudichevskaia A, Dunemann F, Peil A, Nowicka A, Lata B, Stankiewicz-Kosyl M, Jeziorek K, Pitera E, Soska A, Tomala K, Evans KM, Fernández-Fernández F, Guerra W, Korbin M, Keller S, Lewandowski M, Plocharski W, Rutkowski K, Zurawicz E, Costa F, Sansavini S, Tartarini S, Komjanc M, Mott D, Antofie A, Lateur M, Rondia A, Gianfranceschi L, Weg WE (2014) Bayesian QTL analyses using pedigreed families of an outcrossing species, with application to fruit firmness in apple. Theor Appl Genet 127:1073–1090PubMedGoogle Scholar
  10. Calus MPL, Veerkamp RF (2011) Accuracy of multi-trait genomic selection using different methods. Genet Sel Evol 43:26CrossRefPubMedPubMedCentralGoogle Scholar
  11. Castro P, Lewers KS (2016) Identification of quantitative trait loci (QTL) for fruit-quality traits and number of weeks of flowering in the cultivated strawberry. Mol Breed 36:138CrossRefGoogle Scholar
  12. 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 35:79CrossRefGoogle Scholar
  13. Chambers AH, Pillet J, Plotto A, Bai J, Whitaker VM, Folta KM (2014) Identification of a strawberry flavor gene candidate using an integrated genetic-genomic-analytical chemistry approach. BMC Genom 15:217CrossRefGoogle Scholar
  14. Clark SA, Hickey JM, van der Werf JHJ (2011) Different models of genetic variation and their effect on genomic evaluation. Genet Sel Evol 43:18CrossRefPubMedPubMedCentralGoogle Scholar
  15. Daetwyler HD, Pong-Wong R, Villanueva B, Woolliams JA (2010) The impact of genetic architecture on genome-wide evaluation methods. Genetics 185:1021–1031CrossRefPubMedPubMedCentralGoogle Scholar
  16. Daetwyler HD, Calus MLP, Pong-Wong R, de los Campos G, Hickey JM (2013) Genomic prediction in animals and plants: simulation of data, validation, reporting, and benchmarking. Genetics 193:347–365CrossRefPubMedGoogle Scholar
  17. Darwish O, Shahan R, Liu Z, Slovin JP, Alkharouf NW (2015) Re-annotation of the woodland strawberry (Fragaria vesca) genome. BMC Genom 16:29CrossRefGoogle Scholar
  18. Davis TM, Yu H (1997) A linkage map of the diploid strawberry, Fragaria vesca. J Hered 88:215–221CrossRefGoogle Scholar
  19. Davis TM, DiMeglio LM, Yang R, 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
  20. de los Campos G, Hickey JM, Pong-Wong R, Daetwyler HD, Calus MPL (2013) Whole genome regression and prediction methods applied to plant and animal breeding. Genetics 193:327–345Google Scholar
  21. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443–461CrossRefPubMedGoogle Scholar
  22. Duangjit J, Causse M, Sauvage C (2016) Efficiency of genomic selection for tomato fruit quality. Mol Breeding 36:29CrossRefGoogle Scholar
  23. Estaghvirou SBO, Ogutu JO, Schulz-Streeck T, Knaak C, Ouzunuva M, Gordillo A, Phiepo H-P (2013) Evaluation of approaches for estimating the accuracy of genomic prediction in plant breeding. BMC Genom 14:860CrossRefGoogle Scholar
  24. Feldman M, Levy AA, Fahima T, Korol A (2012) Genomic asymmetry in allopolyploid plants: wheat as a model. J Exp Bot 63:5045–5059CrossRefPubMedGoogle Scholar
  25. Gabriel SB, Schaffner SF, Nguyen H, Morre JM, Roy J, Blumenstiel B, Higgins J, DeFelice M, Lochner A, Faggart M, Liu-Cordero SN, Rotimi C, Adeyemo A, Cooper R, Ward R, Lander ES, Daly MJ, Altshuler D (2002) The structure of haplotype blocks in the human genome. Science 296:2225–2229CrossRefPubMedGoogle Scholar
  26. Gaston A, Perrotte J, Lerceteau-Kohler 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 64:1837–1848CrossRefPubMedGoogle Scholar
  27. Gezan S, Osorio LF, Verma S, Whitaker VM (2017) An experimental validation of genomic selection in octoploid strawberry. Hortic Res 4:16070. http://dx.doi.org/10.1038/hortres.2016.70.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gianola D (2013) Priors in whole-genome regression: the Bayesian alphabet returns. Genetics 90:525–540CrossRefGoogle Scholar
  29. Gianola D, Fernando RL, Stella A (2006) Genomic-assisted prediction of genetic value with semiparametric procedures. Genetics 173:1761–1776CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gouy M, Rousselle Y, Bastianelli D, Lecomte P, Bonnal L, Roques D, Efile JC, Rocher S, Daugrois J, Toubi L, Nabeneza S, Hervouet C, Telismart H, Denis M, Thong-Chane A, Glaszmann JC, Hoarau JH, Nibouche S, Costet L (2013) Experimental assessment of the accuracy of genomic selection in sugarcane. Theor Appl Genet 126:2575–2586CrossRefPubMedGoogle Scholar
  31. Grattapaglia D, Vilela Resende M, Resende M, Sansaloni C, Petroli C, Missiaggia A, Takahashi E, Zamprogno K, Kilian A (2011) Genomic selection for growth traits in eucalyptus: accuracy within and across breeding populations. BMC Proc 5:O16CrossRefPubMedCentralGoogle Scholar
  32. Guo G, Zhao F, Wang Y, Zhang Y, Du L, Su G (2014) Comparison of single-trait and multiple-trait genomic prediction models. BMC Genet 15:30CrossRefPubMedPubMedCentralGoogle Scholar
  33. Habier D, Fernando RL, Dekker JCM (2007) The impact of genetic relationship information on genome-assisted breeding values. Genetics 177:2389–2397PubMedPubMedCentralGoogle Scholar
  34. Habier D, Fernando RL, Kizilkaya K, Garrick D (2011) Extension of the Bayesian alphabet for genomic selection. BMC Bioinf 12:186CrossRefGoogle Scholar
  35. Habier D, Fernando RL, Garrick DJ (2013) Genomic BLUP decoded: a look into the black box of genomic prediction. Genetics 194:597–607CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hancock JF (1999) Strawberries. CAB International, Wallingford, UKGoogle Scholar
  37. Hancock JF, Luby JJ, Dale A, Callow PW, Serce S, El-Shiek A (2002) Utilizing wild Fragaria virginiana in strawberry cultivar development: Inheritance of photoperiod sensitivity, fruit size, gender, female fertility and disease resistance. Euphytica 126:177–184CrossRefGoogle Scholar
  38. Harrison RE, Luby JJ, Furnier GR (1997) Chloroplast DNA restriction fragment variation among strawberry (Fragaria spp.) taxa. J Am Soc Hort Sci 122:63–68Google Scholar
  39. Hayashi T, Iwata H (2013) A Bayesian method and its variational approximation for prediction of genomic breeding values in multiple traits. BMC Bioinform 14:34CrossRefGoogle Scholar
  40. Hayes BJ, Goddard ME (2010) Genome-wide association and genomic selection in animal breeding. Genome 53:876–883CrossRefPubMedGoogle Scholar
  41. 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
  42. Haymes KM, Van de Weg WE, Arens P, Maas JL, Vosman B, Den Nijs APM (2000) Development of SCAR markers linked to a Phytophthora fragariae resistance gene and their assessment in European and North American strawberry genotypes. J Am Soc Hortic Sci 125:330–339Google Scholar
  43. Heffner EL, Sorrels ME, Jannink JL (2009) Genomic selection for crop improvement. Crop Sci 49:1–12CrossRefGoogle Scholar
  44. Heslot N, Yang H-P, Sorrells ME, Jannink JL (2012) Genomic selection in plant breeding: A comparison of models. Crop Sci 52:146–160CrossRefGoogle Scholar
  45. Hoerl AE, Kennard RW (1970) Ridge regression: Biased estimation for non-orthogonal problems. Technometrics 12:55–67CrossRefGoogle Scholar
  46. Hubbard M, Kelly J, Rajapakse S, Abbott A, Ballard R (1992) Restriction-fragment-length-polymorphisms in rose and their use for cultivar identification. HortScience 27:172–173Google Scholar
  47. Isik F, Bartholome J, Farjat A, Chancerel E, Raffin A, Sanchez L, Plomion C, Bouffier L (2016) Genomic selection in maritime pine. Plant Sci 242:108–119CrossRefPubMedGoogle Scholar
  48. Isobe SN, Hirakawa H, Sato S, Maeda F, Ishikawa M, Mori T, Yamamoto Y, Shirasawa K, Kimura M, Fukami M, Hashizume F, Tsuji T, Sasamoto S, Kato M, Nanri K, Tsuruoka H, Minami C, Takahashi C, Wada T, Ono A, Kawashima K, Nakazaki N, Kishida Y, Kohara M, Nakayama S, Yamada M, Fujishiro T, Watanabe A, Tabata S (2013) Construction of an integrated high density simple sequence repeat linkage map in cultivated strawberry (Fragaria × ananassa) and its applicability. DNA Res 20:79–92CrossRefPubMedGoogle Scholar
  49. Iwata H, Hayashi T, Terakami S, Takada N, Sawamura Y, Yamamoto T (2013) Potential assessment of genome-wide association study and genomic selection in Japanese pear Pyrus pyrifolia. Breed Sci 63:125–140CrossRefPubMedPubMedCentralGoogle Scholar
  50. James CM, Wilson F, Hadonou AM, Tobutt KR (2003) Isolation and characterization of polymorphic microsatellites in diploid strawberry (Fragaria vesca L.) for mapping, diversity studies and clone identification. Mol Ecol Notes 3:171–173CrossRefGoogle Scholar
  51. Kumar S, Chagné D, Bink MC, Volz RK, Whitworth C, Carlisle C (2012) Genomic selection for fruit quality traits in apple (Malus × domestica borkh.). PLoS ONE 7:e36674CrossRefPubMedPubMedCentralGoogle Scholar
  52. Kumar S, Molloy C, Muñoz P, Daetwyler H, Chagne D, Volz R (2015) Genome-enabled estimates of additive and nonadditive genetic variances and prediction of apple phenotypes across environments. G3 5:2711CrossRefPubMedGoogle Scholar
  53. Larsen M, Poll L (1992) Odour thresholds of some important aroma compounds in strawberries. Z Lebensm Unters Forsch 195:120–123CrossRefGoogle Scholar
  54. 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 107:619–628CrossRefPubMedGoogle Scholar
  55. Lerceteau-Köhler E, Guérin G, Denoyes-Rothan B (2005) Identification of SCAR markers linked to Rca2 anthracnose resistance gene and their assessment in strawberry germplasm. Theor Appl Genet 111:862–870CrossRefPubMedGoogle Scholar
  56. Lerceteau-Köhler E, Moing A, Guérin 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 124:1059–1077CrossRefPubMedPubMedCentralGoogle Scholar
  57. Li J, Meng X, Zong Y, Chen K, Zhang H, Liu J, Li J, Gao C (2016) Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat Plants 2:16139CrossRefPubMedGoogle Scholar
  58. Lillehammer M, Meuwissen THE, Sonesson A (2013) A low-marker density implementation of genomic selection in aquaculture using within-family genomic breeding values. Genet Sel Evol 45:39CrossRefPubMedPubMedCentralGoogle Scholar
  59. Lunkenbein S, Salentijn EMJ, Coiner HA, Boone MJ, Krens FA, Schwab W (2006) Up- and down-regulation of Fragaria × ananassa O-methyl-transferase: impacts on furanone and phenylpropanoid metabolism. J Exp Bot 57:2445–2453CrossRefPubMedGoogle Scholar
  60. Mahoney LL, Sargent DJ, Abebe-Akele F, Wood DJ, Ward JA, Bassil NV, Hancock JF, Folta KM, Davis TM (2016) A high-density linkage map of the ancestral diploid strawberry, Fragaria iinumae, constructed with single nucleotide polymorphism markers from the IStraw90 array and genotyping by sequencing. Plant Genome 9:0Google Scholar
  61. Mangandi J (2016) The genetic architecture of resistance to Phytophthora cactorum and Colletotrichum gloeosporioides in strawberry, PhD thesis, University of Florida, USAGoogle Scholar
  62. Mangandi J, Verma S, Osorio L, Peres N, van de Weg E, Whitaker VM (2017) Pedigree-based analysis in a multiparental population of octoploid strawberry reveals QTL alleles conferring resistance to Phytophthora cactorum. G3 7:1707–1719PubMedPubMedCentralGoogle Scholar
  63. Mathey MM (2013) Phenotyping diverse strawberry (Fragaria spp.) germplasm for aid in marker-assisted breeding, and marker-trait association for red stele (Phytophthora fragariae) resistance marker Rpf1. Master’s thesis. Oregon State University, USAGoogle Scholar
  64. Meuwissen THE, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829PubMedPubMedCentralGoogle Scholar
  65. Meuwissen T, Hayes B, Goddard M (2016) Genomic selection: a paradigm shift in animal breeding. Anim Front 6:6–14CrossRefGoogle Scholar
  66. Michell S, Ametz C, Gungor H (2016) Genomic selection across multiple breeding cycles in applied bread wheat breeding. Theor Appl Genet 129:1179–1189CrossRefGoogle Scholar
  67. Monfort A, Vilanova SD, Davis TM, Arús 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
  68. Morales RGF, Resende JTV, Faria MV, Andrade MC, Resende LV, Delatorre CA, da Silva PR (2011) Genetic similarity among strawberry cultivars assessed by RAPD and ISSR markers. Sci Agric 68:665–670CrossRefGoogle Scholar
  69. Noh Y-H, Lee S, Whitaker VM, Cearley KR, Cha J-S (2016) A high-throughput marker-assisted selection system combining rapid DNA extraction and high-resolution melting and simple sequence repeat analysis: strawberry as a model for fruit crops. J Berry Res, pp 1–9.  https://doi.org/10.3233/jbr-160145
  70. Pai A, Pritchard K, Gilad Y (2015) The genetic and mechanistic basis for variation in gene regulation. PLoS Genet 11:e1004857CrossRefPubMedPubMedCentralGoogle Scholar
  71. Park T, Casella G (2008) The Bayesian LASSO. J Am Stat Assoc 103:681–686CrossRefGoogle Scholar
  72. Patil N, Berno AJ, Hinds DA, Barrett WA, Doshi JM, Hacker CR, Kautzer CR, Lee DH, Marjoribanks C, McDonough DP, Nguyen BT (2001) Blocks of limited haplotype diversity revealed by high-resolution scanning of human chromosome 21. Science 294:1719–1723CrossRefPubMedGoogle Scholar
  73. Pérez A, Olías R, Sanz C (1996) Furanones in strawberries: evolution during ripening and postharvest shelf life. J Agric Food Chem 44:3620–3624CrossRefGoogle Scholar
  74. Perkins-Veazie P (1995) Growth and ripening of strawberry fruit. Hortic Rev (Am Soc Hortic Sci) 17:267–297Google Scholar
  75. Perrotte J, Gaston A, Potier A, Petit A, Rothan C, Denoyes B (2016) Narrowing down the single homoeologous FaPFRU locus controlling flowering in octoploid strawberry using a selective mapping strategy. Plant Biotechnol J 14:2176–2189CrossRefPubMedPubMedCentralGoogle Scholar
  76. Pillet J, Yu H, Chambers A, Whitaker VM, Folta K (2015) Identification of candidate flavonoid pathway genes using transcriptome correlation network analysis in ripe strawberry (Fragaria × ananassa) fruits. J Exp Bot.  https://doi.org/10.1093/jxb/erv205
  77. Powers L (1954) Inheritance of period of blooming in progenies of strawberries. Proc J Am Soc Hort Sci 64:293–298Google Scholar
  78. Pyysalo T, Honkanen E, Hirvi T (1979) Volatiles of wild strawberries, Fragaria vesca L., compared to those of cultivated berries, Fragaria × ananassa cv Senga Sengana. J Agric Food Chem 27:19–22CrossRefGoogle Scholar
  79. Raab TL, López-Ráez JA, Klein D, Caballero JL, Moyano E, Schwab W, Muñoz-Blanco J (2006) FaQR, required for the biosynthesis of the strawberry flavor compound 4-hydroxy-2,5-dimethyl-3(2H)-furanone, encodes an enone oxidoreductase. Plant Cell 18:1023–1037CrossRefPubMedPubMedCentralGoogle Scholar
  80. Resende MFR Jr, Muñoz P, Resende MDV, Garrick DJ, Fernando RL, Davis JM, Jokela EJ, Martin TA, Peter GF, Kirst M (2012) Accuracy of genomic selection methods in a standard dataset of loblolly pine (Pinus taeda L.). Genetics 190:1503–1510CrossRefPubMedPubMedCentralGoogle Scholar
  81. Roach JA, Verma S, Peres NA, Jamieson AR, van de Weg WE, Bink MCAM, Bassil NV, Lee S, Whitaker VM (2016a) FaRXf1: a locus conferring resistance to angular leaf spot caused by Xanthomonas fragariae in octoploid strawberry. Theor Appl Genet 129:1191–1201CrossRefPubMedGoogle Scholar
  82. Roach J, Verma S, Anciro A, Lee S, Isobe S, Jamieson A, Bassil N, Bink MCAM, van de Weg E, Whitaker VM (2016b) QTL discovery and marker development for strawberry angular leaf spot caused by Xanthomonas fragariae. In: Plant and animal genome XXIV Conference, San Diego, CA, USA: https://pag.confex.com/pag/xxiv/webprogram/Paper21811.html
  83. Salinas N (2015) Validation of molecular markers associated with perpetual flowering (PF) and soluble solids content (SSC) in strawberry (Fragaria × ananassa Duch. ex Rozier). Master’s thesis, Oregon State University, USAGoogle Scholar
  84. Sánchez-Sevilla JF, Cruz-Rus E, Valpuesta V, Botella MA, Amaya I (2014) Deciphering gamma-decalactone biosynthesis in strawberry fruit using a combination of genetic mapping, RNA-Seq and eQTL analyses. BMC Genom 15:1CrossRefGoogle Scholar
  85. Sánchez-Sevilla JF, Horvath A, Botella MA, Gaston A, Folta K, Kilian A, Denoyes B, Amaya I (2015) Diversity arrays technology (DArT) marker platforms for diversity analysis and linkage mapping in a complex crop, the octoploid cultivated strawberry (Fragaria × ananassa). PLoS ONE 10:e0144960CrossRefPubMedPubMedCentralGoogle Scholar
  86. Santos R, Moraes BFX, Missiaggia A, Aguiar AM, Lima BM, Dias DC, Rezende G DPS, Goncalves FMA, Resende M, Munoz PR, Kirst M (2016) Comparing sequence-capture and SNP-array genotyping methods for development of genomic selection prediction models in Eucalyptus. In: Plant and animal genome XXIV conference, San Diego, CA, USA. https://pag.confex.com/pag/xxiv/webprogram/Paper19733.html
  87. Sargent DJ, Hadonou AM, Simpson DW (2003) Development and characterization of polymorphic microsatellite markers from Fragaria viridis, a wild diploid strawberry. Mol Ecol Resour 3:550–552CrossRefGoogle Scholar
  88. 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
  89. Sargent DJ, Fernandéz-Fernandéz F, Ruiz-Roja JJ, Sutherland BG, Passey A, Whitehouse AB (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
  90. Sargent D, Kuchta P, Girona E, Zhang H, Davis T, Celton J-M, Marchese A, Korbin M, Folta KM, Shulaev V, Simpson W (2011) Simple sequence repeat marker development and mapping targeted to previously unmapped regions of the strawberry genome sequence. Plant Genome 4:165–177CrossRefGoogle Scholar
  91. 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 124:1229–1240CrossRefPubMedGoogle Scholar
  92. Sargent DJ, Yang Y, Šurbanovski N, Bianco L, Buti M, Velasco R, Giongo L, Davis TM (2016) HaploSNP affinities and linkage map positions illuminate subgenome composition in the octoploid, cultivated strawberry (Fragaria × ananassa). Plant Sci 242:140–150CrossRefPubMedGoogle Scholar
  93. Schieberle P, Hofmann T (1997) Evaluation of the character impact odorants in fresh strawberry juice by quantitative measurements and sensory studies on model mixtures. J Agric Food Chem 45:227–232CrossRefGoogle Scholar
  94. Schmitt J, Fournier-Level A (2016) Genetics of adaptation to changing climate in Arabidopsis thaliana. In: Abstracts of the 5th international conference on quantitative genetics, ICQG5. Madison, Wisconsin, USA. http://www.icqg5.org/schedule
  95. Schwieterman ML, Colquhoun TA, Jaworski EA, Bartoshuk LM, Gilbert JL, Tieman DM, Odabasi AZ, Moskowitz HR, Folta KM, Klee HJ, Sims CA, Whitaker VM, Clark DG (2014) Strawberry flavor: diverse chemical compositions, a seasonal influence, and effects on sensory perception. PLoS ONE 9:e88446CrossRefPubMedPubMedCentralGoogle Scholar
  96. Shimomura K, Hirashima K (2006) Development and characterization of simple sequence repeats (SSR) as markers to identify strawberry cultivars (Fragaria × ananassa Duch.). J Jpn Soc Hortic Sci 75:399–402CrossRefGoogle Scholar
  97. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, Burns P, Davis TM, Slovin JP, Bassil N, Hellens RP, Evans C, Harkins T, Kodira C, Desany B, Crasta OR, Jensen RV, Allan AC, Michael TP, Setubal JC, Celton J-M, Rees DJG, Williams KP, Holt SH, Rojas JJR, Chatterjee M, Liu B, Silva H, Meisel L, Adato A, Filichkin SA, Troggio M, Viola R, Ashman T-L, Wang H, Dharmawardhana P, Elser J, Raja R, Priest HD, Bryant DW, Fox SE, Givan SA, Wilhelm LJ, Naithani S, Christoffels A, Salama DY, Carter J, Girona EL, Zdepski A, Wang W, Kerstetter RA, Schwab W, Korban SS, Davik J, Monfort A, Denoyes-Rothan B, Arus P, Mittler R, Flinn B, Aharoni A, Bennetzen JL, Salzberg SL, Dickerman AW, Velasco R, Borodovsky M, Veilleux RE, Folta KM (2010) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116CrossRefPubMedPubMedCentralGoogle Scholar
  98. Simko I (2016) High-resolution DNA melting analysis in plant research. Trends Plant Sci 21:528–537CrossRefPubMedGoogle Scholar
  99. Slater A, Cogan NOI, Forster JW, Hayes BJ, Daetwyler HD (2016) Improving genetic gain with genomic selection in autotetraploid potato. Plant Genome 9:1–15CrossRefGoogle Scholar
  100. Sun C, VanRaden PM, Cole JB, O’Connell JR (2014) Improvement of prediction ability for genomic selection of dairy cattle by including dominance effects. PLoS ONE 9:e103934CrossRefPubMedPubMedCentralGoogle Scholar
  101. Tennessen JA, Govindarajulu R, Ashman T-L, Liston A (2014) Evolutionary origins and dynamics of octoploid strawberry subgenomes revealed by dense targeted capture linkage maps. Genome Biol Evol 6:3295–3313CrossRefPubMedPubMedCentralGoogle Scholar
  102. Van de Weg WE (1997) Gene-for-gene relationships between strawberry and the causal agent of red stele root rot, Phytophthora fragariae. CPRO-DLO, PhD thesis, Wageningen Agricultural University, The NetherlandsGoogle Scholar
  103. Van Dijk T, Pagliarani G, Pikunova A, Noordijk Y, Yilmaz-Temel H, Meulenbroek B, Visser RG, van de Weg E (2014) Genomic rearrangements and signatures of breeding in the allo-octoploid strawberry as revealed through an allele dose based SSR linkage map. BMC Plant Biol 14:55CrossRefPubMedPubMedCentralGoogle Scholar
  104. VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91:4414–4423CrossRefPubMedGoogle Scholar
  105. Verma S, Roach J, Mangandi J, Lee S, Salinas N, Bassil N, Bink M, van de Weg E, Peace C, Iezzoni A, Whitaker V (2016a) DNA-informed strawberry breeding in RosBREED. In: Plant and animal genome XXIV conference, San Diego, CA, USA. https://pag.confex.com/pag/xxiv/webprogram/Paper18784.html
  106. Verma S, Bassil N, van de Weg E, Harrison R, Monfort A, Hidalgo JM, Amaya I, Denoyes B, Mahoney LL, Davis TM, Fan Z, Knapp S, Whitaker VM (2016b) Development and evaluation of the Axiom® IStraw35 384HT array for the allo-octoploid cultivated strawberry Fragaria × ananassa. Acta Hort (accepted in the proceedings of the international strawberry symposium, Quebec City, CAN)Google Scholar
  107. Voorrips RE, Bink MC, Kruisselbrink JW, Koehorst-van Putten HJ, van de Weg WE (2016) PediHaplotyper: software for consistent assignment of marker haplotypes in pedigrees. Mol Breed 36:119CrossRefPubMedPubMedCentralGoogle Scholar
  108. Wang H, Qi M, Cutler AJ (1993) A simple method of preparing plant samples for PCR. Nucl Acids Res 21:4153–4154CrossRefPubMedGoogle Scholar
  109. Wein M, Lavid N, Lunkenbein S, Lewinsohn E, Schwab W, Kaldenhoff R (2002) Isolation, cloning and expression of a multifunctional O-methyltransferase capable of forming 2,5-dimethyl-4-methoxy-3(2H)-furanone, one of the key aroma compounds in strawberry fruits. Plant J 31:755–765CrossRefPubMedGoogle Scholar
  110. Wong CK, Bernardo R (2008) Genomewide selection in oil palm: increasing selection gain per unit time and cost with small populations. Theor Appl Genet 116:815–824CrossRefPubMedGoogle Scholar
  111. Würschum T, Reif JC, Kraft T, Janssen G, Zhao Y (2013) Genomic selection in sugar beet breeding populations. BMC Genet 14:85CrossRefPubMedPubMedCentralGoogle Scholar
  112. Xin Z, Velten JP, Oliver MJ, Burke JJ (2003) High-throughput DNA extraction method suitable for PCR. Biotechniques 34:820–824PubMedGoogle Scholar
  113. Zhong S, Dekkers J, Fernando RL, Jannick JL (2009) Factors affecting accuracy from genomic selection in populations derived from multiple inbred lines: a barley case study. Genetics 182:355–364CrossRefPubMedPubMedCentralGoogle Scholar
  114. Zorrilla-Fontanesi Y, Cabeza A, Domínguez P, Medina JJ, Valpuesta V, Denoyes-Rothan B, Sánchez-Sevilla JF, Amaya I (2012) Quantitative trait loci and underlying candidate genes controlling agronomical and fruit quality traits in octoploid strawberry (Fragaria × ananassa). Theor Appl Genet 123:755–778CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Sujeet Verma
    • 1
  • Luis F. Osorio
    • 1
  • Seonghee Lee
    • 1
  • Nahla V. Bassil
    • 2
  • Vance M. Whitaker
    • 1
  1. 1.Gulf Coast Research and Education CenterUniversity of Florida IFASWimaumaUSA
  2. 2.United States Department of Agriculture-Agricultural Research ServiceNational Clonal Germplasm RepositoryCorvallisUSA

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