Fruit Ripening and QTL for Fruit Quality in the Octoploid Strawberry

  • Delphine M. Pott
  • José G. Vallarino
  • Sonia Osorio
  • Iraida AmayaEmail author
Part of the Compendium of Plant Genomes book series (CPG)


Fruit development and ripening is a unique developmental process to flowering plants that ensures the propagation of seeds and plant survival. In addition, fruits are an essential part of human diet. In particular, strawberry is a rich source of nutraceuticals such as vitamin C, folate and phenolic compounds. Strawberry production and breeding is becoming an extremely competing area of economic development worldwide. Cost of production in many countries is increasing due to a number of challenges such as rising labour costs, pest control or water availability. One way to increase competiveness is increasing fruit quality of new strawberry cultivars. Amazing advances have been made in our knowledge of the different metabolic pathways that take place in the final stages of fruit development and that lead to a flavourful and ripe strawberry fruit. Similarly, different genes involved in gene regulation during ripening have been discovered and characterized. In parallel, the discovery of loci responsible for natural variation among strawberry germplasm is producing a growing amount of DNA markers that after validation could be used in accelerating the selection of new cultivars with improved fruit quality. This chapter summarizes main advances in the study of fruit ripening in the octoploid strawberry and QTL controlling fruit quality traits.


  1. Aaby K, Ekeberg D, Skrede G (2007) Characterization of phenolic compounds in strawberry (Fragaria × ananassa) fruits by different HPLC detectors and contribution of individual compounds to total antioxidant capacity. J Agric Food Chem 55(11):4395–4406PubMedCrossRefGoogle Scholar
  2. Aaby K, Skrede G, Wrolstad RE (2005) Phenolic composition and antioxidant activities in flesh and achenes of strawberries (Fragaria × ananassa). J Agric Food Chem 53(10):4032–4040PubMedCrossRefGoogle Scholar
  3. Agius F, Gonzalez-Lamothe R, Caballero JL, Munoz-Blanco J, Botella MA, Valpuesta V (2003) Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nat Biotechnol 21(2):177–181PubMedCrossRefPubMedCentralGoogle Scholar
  4. Aharoni A, Keizer LC, Bouwmeester HJ, Sun Z, Alvarez-Huerta M, Verhoeven HA, Blaas J, van Houwelingen AM, De Vos RC, van der Voet H, Jansen RC, Guis M, Mol J, Davis RW, Schena M, van Tunen AJ, O’Connell AP (2000) Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell 12:647–662PubMedPubMedCentralCrossRefGoogle Scholar
  5. Aharoni A, De Vos CHR, Wein M, Sun ZK, 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(3):319–332PubMedCrossRefGoogle Scholar
  6. Aharoni A, Keizer LCP, Van den Broeck HC, Blanco-Portales R, Munoz-Blanco J, Bois G, Smit P, De Vos RCH, O’Connell AP (2002) Novel insight into vascular, stress, and auxin-dependent and -independent gene expression programs in strawberry, a non-climacteric fruit. Plant Physiol 129(3):1019–1031PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aharoni A, O’Connell AP (2002) Gene expression analysis of strawberry achene and receptacle maturation using DNA microarrays. J Exp Bot 53(377):2073–2087PubMedCrossRefGoogle Scholar
  8. Almeida JRM, D’Amico E, Preuss A, Carbone F, de Vos CHR, Deiml B, Mourgues F, Perrotta G, Fischer TC, Bovy AG, Martens S, Rosati C (2007) Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria × ananassa). Arch Biochem Biophys 465(1):61–71PubMedPubMedCentralCrossRefGoogle Scholar
  9. Alvarez-Suarez JM, Dekanski D, Ristić S, Radonjić NV, Petronijević ND, Giampieri F, Astolfi P, González-Paramás AM, Santos-Buelga C, Tulipani S, Quiles JL, Mezzetti B, Battino M (2011) strawberry polyphenols attenuate ethanol-induced gastric lesions in rats by activation of antioxidant enzymes and attenuation of MDA increase. PLoS ONE 6:e25878PubMedPubMedCentralCrossRefGoogle Scholar
  10. Ariza MT, Martínez-Ferri E, Domínguez P, Medina JJ, Miranda L, Soria C (2015) Effects of harvest time on functional compounds and fruit antioxidant capacity in ten strawberry cultivars. J Berry Res 5:71–80CrossRefGoogle Scholar
  11. Ayub RA, Bosetto L, Galvão CW, Etto RM, Inaba J, Lopes PZ (2016) Abscisic acid involvement on expression of related gene and phytochemicals during ripening in strawberry fruit Fragaria × ananassa cv Camino Real. Sci Hort 203:178–184CrossRefGoogle Scholar
  12. Basson CE, Groenewald JH, Kossmann J, Cronjé C, Bauer R (2010) Sugar and acid-related quality attributes and enzyme activities in strawberry fruits: invertase is the main sucrose hydrolysing enzyme. Food Chem 121(4):1156–1162CrossRefGoogle Scholar
  13. Benítez-Burraco A, Blanco-Portales R, Redondo-Nevado J, Bellido ML, Moyano E, Caballero JL, Muñoz-Blanco J (2003) Cloning and characterization of two ripening-related strawberry (Fragaria × ananassa cv. Chandler) pectate lyase genes. J Exp Bot 54(383):633–645PubMedCrossRefPubMedCentralGoogle Scholar
  14. Blake PS, Taylor DR, Crisp CM, Mander LN, Owen DJ (2000) Identification of endogenous gibberellins in strawberry, including the novel gibberellins GA123, GA124 and GA125. Phytochemistry 55(8):887–890PubMedCrossRefPubMedCentralGoogle Scholar
  15. Bood KG, Zabetakis I (2002) The biosynthesis of strawberry flavor (II): biosynthetic and molecular biology studies. J Food Sci 67(1):2–8CrossRefGoogle Scholar
  16. Burdock GA, Fenaroli G (2009) Fenaroli’s handbook of flavor ingredientsGoogle Scholar
  17. Bustamante CA, Civello PM, Martinez GA (2009) Cloning of the promoter region of beta-xylosidase (FaXyl1) gene and effect of plant growth regulators on the expression of FaXyl1 in strawberry fruit. Plant Sci 177(1):49–56CrossRefGoogle Scholar
  18. Casañal A, Zander U, Muñoz C, Dupeux F, Luque I, Botella MA, Schwab W, Valpuesta V, Marquez JA (2013) The strawberry pathogenesis-related 10 (PR-10) Fra a proteins control flavonoid biosynthesis by binding to metabolic intermediates. J Biol Chem 288(49):35322–35332PubMedPubMedCentralCrossRefGoogle Scholar
  19. 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(398):909–918PubMedCrossRefPubMedCentralGoogle Scholar
  20. 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 Breeding 36:138CrossRefGoogle Scholar
  21. 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 15:217 CrossRefGoogle Scholar
  22. Civello PM, Powell ALT, Sabehat A, Bennett AB (1999) An expansin gene expressed in ripening strawberry fruit. Plant Physiol 121(4):1273–1279PubMedPubMedCentralCrossRefGoogle Scholar
  23. Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond B Biol Sci 363:557–572PubMedCrossRefPubMedCentralGoogle Scholar
  24. Costa F, 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
  25. Cruz-Rus E, Amaya I, Sanchez-Sevilla JF, Botella MA, Valpuesta V (2011) Regulation of L-ascorbic acid content in strawberry fruits. J Exp Bot 62(12):4191–4201PubMedPubMedCentralCrossRefGoogle Scholar
  26. Cruz-Rus E, Sesmero R, Angel-Pérez JA et al (2017) Validation of a PCR test to predict the presence of flavor volatiles mesifurane and γ-decalactone in fruits of cultivated strawberry (Fragaria × ananassa). Mol Breeding 37(10):131CrossRefGoogle Scholar
  27. Csukasi F, Donaire L, Casañal A, Martínez-Priego L, Botella MA, Medina-Escobar N, Llave C, Valpuesta V (2012) Two strawberry miR159 family members display developmental-specific expression patterns in the fruit receptacle and cooperatively regulate Fa-GAMYB. New Phytol 195(1):47–57PubMedCrossRefPubMedCentralGoogle Scholar
  28. Csukasi F, Osorio S, Gutierrez JR, Kitamura J, Giavalisco P, Nakajima M, Fernie AR, Rathjen JP, Botella MA, Valpuesta V, Medina-Escobar N (2011) Gibberellin biosynthesis and signalling during development of the strawberry receptacle. New Phytol 191(2):376–390PubMedCrossRefPubMedCentralGoogle Scholar
  29. Cumplido-Laso G, Medina-Puche L, Moyano E, Hoffmann T, Sinz Q, Ring L, Studart-Wittkowski C, Caballero JL, Schwab W, Munoz-Blanco J, Blanco-Portales R (2012) The fruit ripening-related gene FaAAT2 encodes an acyl transferase involved in strawberry aroma biogenesis. J Exp Bot 63(11):4275–4290PubMedCrossRefPubMedCentralGoogle Scholar
  30. Chai YM, Jia HF, Li CL, Dong QH, Shen YY (2011) FaPYR1 is involved in strawberry fruit ripening. J Exp Bot 62(14):5079–5089PubMedCrossRefPubMedCentralGoogle Scholar
  31. Darrow GM (1966) The strawberry: history, breeding and physiology. Holt, Rinehart, and Winston, New YorkGoogle Scholar
  32. Davey MW, Montagu MV, Inzé D, Sanmartin M, Kanellis A, Smirnoff N, Benzie IJJ, Strain JJ, Favell D, Fletcher J (2000) Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J Sci Food Agric 80(7):825–860CrossRefGoogle Scholar
  33. Davies C, Boss PK, Robinson SP (1997) Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol 115(3):1155–1161PubMedPubMedCentralCrossRefGoogle Scholar
  34. de la Fuente JI, Amaya I, Castillejo C, Sanchez-Sevilla JF, Quesada MA, Botella MA, Valpuest V (2006) The strawberry gene FaGAST affects plant growth through inhibition of cell elongation. J Exp Bot 57(10):2401–2411PubMedCrossRefPubMedCentralGoogle Scholar
  35. Douillard C, Guichard E (1989) Comparison by multidimensional analysis of concentrations of volatile compounds in fourteen frozen strawberry varieties [aroma, furaneol, mesifurane]. Sci Aliments 9:53–76Google Scholar
  36. 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(2):730–750PubMedPubMedCentralCrossRefGoogle Scholar
  37. Franz-Oberdorf K, Eberlein B, Edelmann K, Hucherig S, Besbes F, Darsow U, Ring J, Schwab W (2016) Fra a 1.02 is the most potent isoform of the Bet v 1-like allergen in strawberry fruit. J Agric Food Chem 64(18):3688–3696PubMedCrossRefPubMedCentralGoogle Scholar
  38. Giampieri F, Tulipani S, Alvarez-Suarez JM, Quiles JL, Mezzetti B, Battino M (2012) The strawberry: composition, nutritional quality, and impact on human health. Nutrition 28:9–19PubMedCrossRefPubMedCentralGoogle Scholar
  39. Gillaspy G, Bendavid H, Gruissem W (1993) Fruits—a developmental perspective. Plant Cell 5(10):1439–1451PubMedPubMedCentralCrossRefGoogle Scholar
  40. Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16(suppl 1):S170–S180PubMedPubMedCentralCrossRefGoogle Scholar
  41. Given NK, Venis MA, Grierson D (1988) Hormonal-regulation of ripening in the strawberry, a non-climacteric fruit. Planta 174(3):402–406PubMedCrossRefPubMedCentralGoogle Scholar
  42. Griesser M, Hoffmann T, Bellido ML, Rosati C, Fink B, Kurtzer R, Aharoni A, Munoz-Blanco J, Schwab W (2008) Redirection of flavonoid biosynthesis through the down-regulation of an anthocyanidin glucosyltransferase in ripening strawberry fruit. Plant Physiol 146(4):1528–1539PubMedPubMedCentralCrossRefGoogle Scholar
  43. Halbwirth H, Puhl I, Haas U, Jezik K, Treutter D, Stich K (2006) Two-phase flavonoid formation in developing strawberry (Fragaria × ananassa) fruit. J Agric Food Chem 54(4):1479–1485PubMedPubMedCentralCrossRefGoogle Scholar
  44. Han Y, Dang R, Li J, Jiang J, Zhang N, Jia M, Wei L, Li Z, Li B, Jia W (2015) SUCROSE NONFERMENTING1-RELATED PROTEIN KINASE2.6, an ortholog of OPEN STOMATA1, is a negative regulator of strawberry fruit development and ripening. Plant Physiol 167(3):915–930PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hancock JF (1999) Strawberries. Crop production science in horticulture series. CABI, Wallingford, UKGoogle Scholar
  46. Hanhineva K, Kärenlampi SO, Aharoni A (2011) Recent advances in strawberry metabolomics. In: Husaini AM, Mercado JA (eds) Genomics, Transgenics, Molecular Breeding and Biotechnology of Strawberry. Glob Sci B, UK, 65–75.Google Scholar
  47. Hanson AD, Gregory JF (2011) Folate biosynthesis, turnover, and transport in plants. Annu Rev Plant Biol 62(1):105–125PubMedCrossRefPubMedCentralGoogle Scholar
  48. Harpster MH, Brummell DA, Dunsmuir P (1998) Expression analysis of a ripening-specific, auxin-repressed endo-1,4-beta-glucanase gene in strawberry. Plant Physiol 118(4):1307–1316PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hawkins C, Caruana J, Schiksnis E, Liu Z (2016) Genome-scale DNA variant analysis and functional validation of a SNP underlying yellow fruit color in wild strawberry. Sci Rep 6:29017PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hjernø K, Alm R, Canbäck B, Matthiesen R, Trajkovski K, Björk L, Roepstorff P, Emanuelsson C (2006) Down-regulation of the strawberry Bet v 1-homologous allergen in concert with the flavonoid biosynthesis pathway in colorless strawberry mutant. Proteomics 6(5):1574–1587PubMedCrossRefGoogle Scholar
  51. Huber DJ (1984) Strawberry fruit softening: the potential roles of polyuronides and hemicelluloses. J Food Sci 49(5):1310–1315CrossRefGoogle Scholar
  52. Iannetta PPM, Laarhoven L-J, Medina-Escobar N, James EK, McManus MT, Davies HV, Harren FJM (2006) Ethylene and carbon dioxide production by developing strawberries show a correlative pattern that is indicative of ripening climacteric fruit. Physiol Plant 127(2):247–259CrossRefGoogle Scholar
  53. Jain AK, Nessler CL (2000) Metabolic engineering of an alternative pathway for ascorbic acid biosynthesis in plants. Mol Breed 6(1):73–78CrossRefGoogle Scholar
  54. Jetti RR, Yang E, Kurnianta A, Finn C, Qian MC (2007) Quantification of selected aroma-active compounds in strawberries by headspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis. J Food Sci 72(7):S487–S496PubMedPubMedCentralCrossRefGoogle Scholar
  55. Ji K, Chen P, Sun L, Wang Y, Dai S, Li Q, Li P, Sun Y, Wu Y, Duan C, Leng P (2012) Non-climacteric ripening in strawberry fruit is linked to ABA, FaNCED2 and FaCYP707A1. Funct Plant Biol 39(4):351–357CrossRefGoogle Scholar
  56. Jia H-F, Chai Y-M, Li C-L, Lu D, Luo J-J, Qin L, Shen Y-Y (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157(1):188–199PubMedPubMedCentralCrossRefGoogle Scholar
  57. Jia H, Wang Y, Sun M, Li B, Han Y, Zhao Y, Li X, Ding N, Li C, Ji W, Jia W (2013) Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol 198(2):453–465PubMedCrossRefPubMedCentralGoogle Scholar
  58. Jia H, Jiu S, Zhang C, Wang C, Tariq P, Liu Z, Wang B, Cui L, Fang J (2016) Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress-ripening transcription factor. Plant Biotechnol J 14:2045–2065PubMedPubMedCentralCrossRefGoogle Scholar
  59. Jin W, Wang H, Li M, Wang J, Yang Y, Zhang X, Yan G, Zhang H, Liu J, Zhang K (2016) The R2R3 MYB transcription factor PavMYB10. 1 involves in anthocyanin biosynthesis and determines fruit skin colour in sweet cherry (Prunus avium L.). Plant Biotechnol J 14:2120–2133PubMedPubMedCentralCrossRefGoogle Scholar
  60. Karlsson AL, Alm R, Ekstrand B, Fjelkner-Modig S, Schiott A, Bengtsson U, Bjork L, Hjerno K, Roepstorff P, Emanuelsson CS (2004) Bet v 1 homologues in strawberry identified as IgE-binding proteins and presumptive allergens. Allergy 59(12):1277–1284PubMedCrossRefGoogle Scholar
  61. Klee HJ (2010) Improving the flavor of fresh fruits: genomics, biochemistry, and biotechnology. New Phytol 187(1):44–56PubMedCrossRefGoogle Scholar
  62. Larsen M, Poll L, Olsen C (1992) Evaluation of the aroma composition of some strawberry (Fragaria × ananassa Duch) cultivars by use of odour threshold values. Zeitschrift für Lebensmittel untersuchung und Forschung 195:536–539CrossRefGoogle Scholar
  63. 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
  64. Lerceteau-Köhler E, Moing A, Guerin G, Renaud C, Petit A, Rothan C, Denoyes B (2012) Genetic dissection of fruit quality traits in the octoploid cultivated strawberry highlights the role of homoeo-QTL in their control. Theor Appl Genet 124:1059–1077PubMedPubMedCentralCrossRefGoogle Scholar
  65. Li D, Li L, Luo Z, Mou W, Mao L, Ying T (2015) Comparative transcriptome analysis reveals the influence of abscisic acid on the metabolism of pigments, ascorbic acid and folic acid during strawberry fruit ripening. PLoS ONE 10(6):e0130037PubMedPubMedCentralCrossRefGoogle Scholar
  66. Liu D, Chen J, Lu W (2011) Expression and regulation of the early auxin-responsive Aux/IAA genes during strawberry fruit development. Mol Biol Rep 38:1187–1193PubMedCrossRefGoogle Scholar
  67. Lunkenbein S, Coiner H, de Vos CHR, Schaart JG, Boone MJ, Krens FA, Schwab W, Salentijn EMJ (2006a) Molecular characterization of a stable antisense chalcone synthase phenotype in strawberry (Fragaria × ananassa). J Agric Food Chem 54(6):2145–2153PubMedCrossRefGoogle Scholar
  68. Lunkenbein S, Salentijn EMJ, Coiner HA, Boone M, Krens FA, Schwab W (2006b) Up- and down-regulation of Fragaria × ananassa O-methyltransferase: impacts on furanone and phenylpropanoid metabolism. J Exp Bot 57:2445–2453PubMedCrossRefGoogle Scholar
  69. Manning K (1994) Changes in gene expression during strawberry fruit ripening and their regulation by auxin. Planta 194(1):62–68CrossRefGoogle Scholar
  70. Manning K (1998) Isolation of a set of ripening-related genes from strawberry: their identification and possible relationship to fruit quality traits. Planta 205(4):622–631PubMedCrossRefGoogle Scholar
  71. Martinez GA, Chaves AR, Anon MC (1996) Effect of exogenous application of gibberellic acid on color change and phenylalanine ammonia-lyase, chlorophyllase, and peroxidase activities during ripening of strawberry fruit (Fragaria × ananassa Duch). J Plant Growth Regul 15(3):139–146CrossRefGoogle Scholar
  72. Martínez GA, Chaves AR, Civello PM (2004) β-xylosidase activity and expression of a β-xylosidase gene during strawberry fruit ripening. Plant Physiol Biochem 42(2):89–96PubMedCrossRefGoogle Scholar
  73. Mazzoni L, Perez-Lopez P, Giampieri F, Alvarez-Suarez JM, Gasparrini M, Forbes-Hernandez TY, Quiles JL, Mezzetti B, Battino M (2016) The genetic aspects of berries: from field to health. J Sci Food Agric 96(2):365–371PubMedCrossRefGoogle Scholar
  74. Medina-Puche L, Blanco-Portales R, Molina-Hidalgo FJ, Cumplido-Laso G, García-Caparrós N, Moyano-Cañete E, Caballero-Repullo JL, Muñoz-Blanco J, Rodríguez-Franco A (2016) Extensive transcriptomic studies on the roles played by abscisic acid and auxins in the development and ripening of strawberry fruits. Funct Integr Genomics 1–22Google Scholar
  75. Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L, Rodriguez-Franco A, Caballero JL, Schwab W, Munoz-Blanco J, Blanco-Portales R (2014) MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria × ananassa fruits. J Exp Bot 65(2):401–417PubMedCrossRefGoogle Scholar
  76. Medina-Puche L, Molina-Hidalgo FJ, Boersma M, Schuurink RC, Lopez-Vidriero I, Solano R, Franco-Zorrilla JM, Caballero JL, Blanco-Portales R, Munoz-Blanco J (2015) An R2R3-MYB Transcription factor regulates eugenol production in ripe strawberry fruit receptacles. Plant Physiol 168(2):598–614PubMedPubMedCentralCrossRefGoogle Scholar
  77. Ménager I, Jost M, Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (Cv. Cigaline) during maturation. J Agric Food Chem 52:1248–1254PubMedCrossRefGoogle Scholar
  78. Merchante C, Vallarino JG, Osorio S, Aragüez I, Villarreal N, Ariza MT, Martínez GA, Medina-Escobar N, Civello MP, Fernie AR, Botella MA, Valpuesta V (2013) Ethylene is involved in strawberry fruit ripening in an organ-specific manner. J Exp Bot 64(14):4421–4439PubMedPubMedCentralCrossRefGoogle Scholar
  79. Moing A, Renaud C, Gaudillere M, Raymond P, Roudeillac P, Denoyes-Rothan B (2001) Biochemical changes during fruit development of four strawberry cultivars. J Am Soc Hort Sci 126(4):394–403Google Scholar
  80. Molina-Hidalgo FJ, Franco AR, Villatoro C, Medina-Puche L, Mercado JA, Hidalgo MA, Monfort A, Caballero JL, Munoz-Blanco J, Blanco-Portales R (2013) The strawberry (Fragaria × ananassa) fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase1) gene encodes an enzyme involved in the degradation of cell-wall middle lamellae. J Exp Bot 64(6):1471–1483PubMedCrossRefPubMedCentralGoogle Scholar
  81. Mounet F, Moing A, Kowalczyk M, Rohrmann J, Petit J, Garcia V, Maucourt M, Yano K, Deborde C, Aoki K, Bergès H, Granell A, Fernie AR, Bellini C, Rothan C, Lemaire-Chamley M (2012) Down-regulation of a single auxin efflux transport protein in tomato induces precocious fruit development. J Exp Bot 63(13):4901–4917PubMedPubMedCentralCrossRefGoogle Scholar
  82. Moyano-Cañete E, Bellido ML, García-Caparrós N, Medina-Puche L, Amil-Ruíz F, González-Reyes JA, Caballero JL, Muñoz-Blanco J, Blanco-Portales R (2013) FaGAST2, a strawberry ripening-related gene, acts together with FaGAST1 to determine cell size of the fruit receptacle. Plant Cell Physiol 54:218–236PubMedCrossRefPubMedCentralGoogle Scholar
  83. Muñoz C, Hoffmann T, Escobar NM, Ludemann F, Botella MA, Valpuesta V, Schwab W (2010) The strawberry fruit Fra a allergen functions in flavonoid biosynthesis. Mol Plant 3(1):113–124PubMedCrossRefPubMedCentralGoogle Scholar
  84. Nogata Y, Yoza K-i, Kusumoto K-i, Ohta H (1996) Changes in molecular weight and carbohydrate composition of cell wall polyuronide and hemicellulose during ripening in strawberry fruit. In: Visser J, Voragen AGJ (eds) Progress in biotechnology, vol 14. Elsevier, pp 591–596Google Scholar
  85. Olbricht K, Grafe C, Weiss K, Ulrich D (2008) Inheritance of aroma compounds in a model population of Fragaria × ananassa Duch. Plant Breeding 127(1):87–93Google Scholar
  86. Olbricht K, Ulrich D, Weiss K, Grafe C (2011) Variation in the amounts of selected volatiles in a model population of Fragaria × ananassa Duch. As influenced by harvest year. J Agric Food Chem 59:944–952PubMedCrossRefPubMedCentralGoogle Scholar
  87. Ornelas-Paz JJ, Yahia EM, Ramirez-Bustamante N, Perez-Martinez JD, Escalante-Minakata Mdel P, Ibarra-Junquera V, Acosta-Muniz C, Guerrero-Prieto V, Ochoa-Reyes E (2013) Physical attributes and chemical composition of organic strawberry fruit (Fragaria × ananassa Duch, Cv. Albion) at six stages of ripening. Food Chem 138(1):372–381CrossRefGoogle Scholar
  88. Paniagua C, Blanco-Portales R, Barcelo-Munoz M, Garcia-Gago JA, Waldron KW, Quesada MA, Munoz-Blanco J, Mercado JA (2016) Antisense down-regulation of the strawberry beta-galactosidase gene FaβGal4 increases cell wall galactose levels and reduces fruit softening. J Exp Bot 67(3):619–631Google Scholar
  89. Pérez AG, Olías R, Sanz C, Olías JM (1996) Furanones in strawberries: evolution during ripening and postharvest shelf life. J Agric Food Chem 44(11):3620–3624CrossRefGoogle Scholar
  90. Perkins-Veazie P (1995) Growth and ripening of strawberry fruit. Hortic Rev 17(8):267–297Google Scholar
  91. Perkins-Veazie PM, Huber DJ, Brecht JK (1996) In vitro growth and ripening of strawberry fruit in the presence of ACC, STS or propylene. Ann Appl Biol 128(1):105–116CrossRefGoogle Scholar
  92. Pillet J, Yu HW, Chambers AH, Whitaker VM, Folta KM (2015) Identification of candidate flavonoid pathway genes using transcriptome correlation network analysis in ripe strawberry (Fragaria × ananassa) fruits. J Exp Bot 66(15):4455–4467PubMedPubMedCentralCrossRefGoogle Scholar
  93. Pombo MA, Martinez GA, Civello PM (2011) Cloning of FaPAL6 gene from strawberry fruit and characterization of its expression and enzymatic activity in two cultivars with different anthocyanin accumulation. Plant Sci 181(2):111–118PubMedCrossRefPubMedCentralGoogle Scholar
  94. Raab T, López-Ráez J, Klein D, Caballero J, Moyano E, Schwab W, Munoz-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 18:1023–1037PubMedPubMedCentralCrossRefGoogle Scholar
  95. Redgwell RJ, MacRae EA, Hallet I, Fischer M, Perry J, Harker R (1997) In vivo and in vitro swelling of cell walls during fruit ripening. Planta 203:162–173CrossRefGoogle Scholar
  96. Ring L, Yeh S-Y, Hücherig S, Hoffmann T, Blanco-Portales R, Fouché M, Villatoro C, Denoyes B, Monfort A, Caballero JL, Muñoz-Blanco J, Gershenson J, Schwab W (2013) Metabolic interaction between anthocyanin and lignin biosynthesis is associated with peroxidase FaPRX27 in strawberry fruit. Plant Physiol 163:43–60PubMedPubMedCentralCrossRefGoogle Scholar
  97. Rosli HG, Civello PM, Martinez GA (2009) alpha-l-Arabinofuranosidase from strawberry fruit: cloning of three cDNAs, characterization of their expression and analysis of enzymatic activity in cultivars with contrasting firmness. Plant Physiol Biochem 47(4):272–281PubMedCrossRefPubMedCentralGoogle Scholar
  98. Rosli HG, Civello PM, Martínez GA (2004) Changes in cell wall composition of three Fragaria × ananassa cultivars with different softening rate during ripening. Plant Physiol Biochem 42(10):823–831PubMedCrossRefPubMedCentralGoogle Scholar
  99. 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 179:2045–2060PubMedPubMedCentralCrossRefGoogle Scholar
  100. 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 Genomics 15(1):1–15CrossRefGoogle Scholar
  101. 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:e0144960PubMedPubMedCentralCrossRefGoogle Scholar
  102. Santiago J, Dupeux F, Round A, Antoni R, Park SY, Jamin M, Cutler SR, Rodriguez PF, Márquez JA (2009) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462:665–668PubMedCrossRefPubMedCentralGoogle Scholar
  103. Sargent DJ, Fernandéz-Fernandéz F, Ruiz-Roja JJ, Sutherland BG, Passey A, Whitehouse AB, Simpson DW (2009) A genetic linkage map of the cultivated strawberry (Fragaria × ananassa) and its comparison to the diploid Fragaria reference map. Mol Breeding 24:293–303CrossRefGoogle Scholar
  104. Sargent DJ, Yang Y, Šurbanovski N, Bianco L, Buti M, Velasco R, Giongo L, Davis T (2016) HaploSNP affinities and linkage map positions illuminate subgenome composition in the octoploid, cultivated strawberry (Fragaria × ananassa). Plant Sci 242:140–150PubMedCrossRefPubMedCentralGoogle Scholar
  105. Schaart JG, Dubos C, Romero De La Fuente I, van Houwelingen AM, de Vos RC, Jonker HH, Xu W, Routaboul JM, Lepiniec L, Bovy AG (2013) Identification and characterization of MYB-bHLH-WD40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria × ananassa) fruits. New Phytol 197(2):454–467PubMedCrossRefPubMedCentralGoogle Scholar
  106. Schols HA, Geraeds CCJM, Searle-van Leeuwen MF, Kormelink FJM, Voragen AGJ (1990) Rhamnogalacturonase: a novel enzyme that degrades the hairy regions of pectins. Carbohydr Res 206(1):105–115CrossRefGoogle Scholar
  107. Schwab W, Davidovich-Rikanati R, Lewinsohn E (2008) Biosynthesis of plant-derived flavor compounds. Plant J 54(4):712–732PubMedPubMedCentralCrossRefGoogle Scholar
  108. Schwab W, Schaart JG, Rosati C (2009) Functional molecular biology research in Fragaria. In: Folta KM, Gardiner SE (eds) Genetics and genomics of rosaceae. plant genetics and genomics: crops and models, vol 6. Springer, pp 457–486CrossRefGoogle Scholar
  109. 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
  110. 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(2):e88446PubMedPubMedCentralCrossRefGoogle Scholar
  111. Seymour GB, Østergaard L, Chapman NH, Knapp S, Martin C (2013) Fruit development and ripening. Annu Rev Plant Biol 64:219–241PubMedCrossRefGoogle Scholar
  112. Shackel KA, Greve C, Labavitch JM, Ahmadi H (1991) Cell turgor changes associated with ripening in tomato pericarp tissue. Plant Physiol 97(2):814–816PubMedPubMedCentralCrossRefGoogle Scholar
  113. Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443(7113):823–826PubMedCrossRefGoogle Scholar
  114. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, et al. (2011) The genome of woodland strawberry (Fragaria vesca), vol 43. Nature Publishing Group, pp 109–116Google Scholar
  115. Song C, Hong X, Zhao S, Liu J, Schulenburg K, Huang F-C, Franz-Oberdorf K, Schwab W (2016) Glucosylation of 4-hydroxy-2,5-dimethyl-3(2H)-furanone, the key strawberry flavor compound in strawberry fruit. Plant Physiol 171:139–151PubMedPubMedCentralCrossRefGoogle Scholar
  116. Song J, Du L, Li L, Kalt W, Palmer LC, Fillmore S, Zhang Y, Zhang Z, Li X (2015) Quantitative changes in proteins responsible for flavonoid and anthocyanin biosynthesis in strawberry fruit at different ripening stages: a targeted quantitative proteomic investigation employing multiple reaction monitoring. J Proteomics 122:1–10PubMedCrossRefGoogle Scholar
  117. Sun JH, Luo JJ, Tian L, Li CL, Xing Y, Shen YY (2013) New evidence for the role of ethylene in strawberry fruit ripening. J Plant Growth Regul 32(3):461–470CrossRefGoogle Scholar
  118. Symons GM, Chua Y-J, Ross JJ, Quittenden LJ, Davies NW, Reid JB (2012) Hormonal changes during non-climacteric ripening in strawberry. J Exp Bot 63:4741–4750PubMedPubMedCentralCrossRefGoogle Scholar
  119. Telias A, Lin-Wang K, Stevenson DE, Cooney JM, Hellens RP, Allan AC, Hoover EE, Bradeen JM (2011) Apple skin patterning is associated with differential expression of MYB10. BMC Plant Biol 11(1):1–15CrossRefGoogle Scholar
  120. 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 6:3295–3313PubMedPubMedCentralCrossRefGoogle Scholar
  121. Tohge T, Alseekh S, Fernie AR (2014) On the regulation and function of secondary metabolism during fruit development and ripening. J Exp Bot 64(16):4599–4611 CrossRefGoogle Scholar
  122. Trainotti L, Pavanello A, Casadoro G (2005) Different ethylene receptors show an increased expression during the ripening of strawberries: does such an increment imply a role for ethylene in the ripening of these non-climacteric fruits? J Exp Bot 56(418):2037–2046PubMedCrossRefPubMedCentralGoogle Scholar
  123. Trainotti L, Spinello R, Piovan A, Spolaore S, Casadoro G (2001) beta-galactosidases with a lectin-like domain are expressed in strawberry. J Exp Bot 52(361):1635–1645PubMedPubMedCentralGoogle Scholar
  124. Trainotti L, Zanin D, Casadoro G (2003) A cell wall-oriented genomic approach reveals a new and unexpected complexity of the softening in peaches. J Exp Bot 54(389):1821–1832PubMedCrossRefPubMedCentralGoogle Scholar
  125. Tulipani S, Mezzetti B, Battino M (2009) Impact of strawberries on human health: insight into marginally discussed bioactive compounds for the Mediterranean diet. Public Health Nutr 12(9A):1656–1662PubMedCrossRefPubMedCentralGoogle Scholar
  126. Tulipani S, Mezzetti B, Capocasa F, Bompadre S, Beekwilder J, de Vos CHR, Capanoglu E, Bovy A, Battino M (2008) Antioxidants, phenolic compounds, and nutritional quality of different strawberry genotypes. J Agric Food Chem 56(3):696–704PubMedCrossRefGoogle Scholar
  127. Ulrich D, Hoberg E, Rapp A, Kecke S (1997) Analysis of strawberry flavour–discrimination of aroma types by quantification of volatile compounds. Zeitschrift für Lebensmitteluntersuchung und-Forschung A 205:218–223CrossRefGoogle Scholar
  128. Ulrich D, Komes D, Olbricht K, Hoberg E (2007) Diversity of aroma patterns in wild and cultivated Fragaria accessions. Genet Resour Crop Evol 54:1185–1196CrossRefGoogle Scholar
  129. Ulrich D, Olbricht K (2013) Diversity of volatile patterns in sixteen Fragaria vesca L. accessions in comparison to cultivars of Fragaria × ananassa. J Appl Bot Food Qual 86:37–46Google Scholar
  130. Ulrich D, Olbricht K (2016) A search for the ideal flavor of strawberry - Comparison of consumer acceptance and metabolite patterns in Fragaria × ananassa Duch. J Appl Bot Food Qual 89:223–234Google Scholar
  131. Valpuesta V, Botella MA (2004) Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci 9(12):573–577PubMedCrossRefPubMedCentralGoogle Scholar
  132. Vallarino JG, Osorio S, Bombarely A, Casañal A, Cruz-Rus E, Sánchez-Sevilla JF, Amaya I, Giavalisco P, Fernie AR, Botella MA, Valpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening. New Phytol 208(2):482–496PubMedCrossRefGoogle Scholar
  133. Vandendriessche T, Vermeir S, Mayayo Martinez C, Hendrickx Y, Lammertyn J, Nicolaï BM, Hertog MLATM (2013) Effect of ripening and inter-cultivar differences on strawberry quality. Lebens Wiss Technol 52(2):62–70CrossRefGoogle Scholar
  134. Verhoeyen ME, Bovy A, Collins G, Muir S, Robinson S, de Vos CHR, Colliver S (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53(377):2099–2106PubMedCrossRefGoogle Scholar
  135. Villarreal NM, Rosli HG, Martínez GA, Civello PM (2008) Polygalacturonase activity and expression of related genes during ripening of strawberry cultivars with contrasting fruit firmness. Postharvest Biol Technol 47(2):141–150CrossRefGoogle Scholar
  136. 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
  137. Winkel-Shirley B (2001) Flavonoid Biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126(2):485–493PubMedPubMedCentralCrossRefGoogle Scholar
  138. Wyllie SG, Fellman JK (2000) Formation of volatile branched chain esters in bananas (Musa sapientum L.). J Agric Food Chem 48(8):3493–3496PubMedCrossRefPubMedCentralGoogle Scholar
  139. Youssef SM, Amaya I, López-Aranda JM, Sesmero R, Valpuesta V, Casadoro G, Blanco-Portales R, Pliego-Alfaro F, Quesada MA, Mercado JA (2013) Effect of simultaneous down-regulation of pectate lyase and endo-β-1,4-glucanase genes on strawberry fruit softening. Mol Breed 31(2):313–322CrossRefGoogle Scholar
  140. Zabetakis I, Holden MA (1997) Strawberry flavour: analysis and biosynthesis. J Sci Food Agric 74(4):421–434CrossRefGoogle Scholar
  141. Zhai R, Wang Z, Zhang S, Meng G, Song L, Wang Z, Li P, Ma F, Xu L (2016) Two MYB transcription factors regulate flavonoid biosynthesis in pear fruit (Pyrus bretschneideri Rehd.). J Exp Bot 67(5):1275–1284PubMedCrossRefPubMedCentralGoogle Scholar
  142. Zhang J, Wang X, Yu O, Tang J, Gu X, Wan X, Fang C (2011) Metabolic profiling of strawberry (Fragaria × ananassa Duch.) during fruit development and maturation. J Exp Bot 62(3):1103–1118PubMedCrossRefPubMedCentralGoogle Scholar
  143. Zorrilla-Fontanesi Y, Cabeza A, Domínguez P, Medina JJ, Valpuesta V, Denoyes-Rothan B, Sánchez-Sevilla JF, Amaya I (2011) Quantitative trait loci and underlying candidate genes controlling agronomical and fruit quality traits in octoploid strawberry (Fragaria × ananassa). Theor Appl Genet 123:755–778PubMedCrossRefGoogle Scholar
  144. Zorrilla-Fontanesi Y, Rambla J-L, Cabeza A, Medina JJ, Sánchez-Sevilla JF, Valpuesta V, Botella MA, Granell A, Amaya I (2012) Genetic analysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation in mesifurane content. Plant Physiol 159:851–870PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Delphine M. Pott
    • 1
  • José G. Vallarino
    • 1
  • Sonia Osorio
    • 1
  • Iraida Amaya
    • 2
    Email author
  1. 1.Department of Molecular Biology and BiochemistryInstituto de Hortofruticultura Subtropical y Mediterránea ‘La Mayora’, University of Malaga-Consejo Superior de Investigaciones CientíficasMálagaSpain
  2. 2.Instituto Andaluz de Investigación y Formación Agraria y Pesquera (IFAPA), Centro de ChurrianaMálagaSpain

Personalised recommendations