Skip to main content
SpringerLink
Log in
Book cover

The Genomes of Rosaceous Berries and Their Wild Relatives pp 95–113Cite as

Fruit Ripening and QTL for Fruit Quality in the Octoploid Strawberry

  • Chapter
  • First Online:

Part of the book series: Compendium of Plant Genomes ((CPG))

Abstract

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.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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):4395–4406

    Article  PubMed  CAS  Google Scholar 

  • 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):4032–4040

    Article  PubMed  CAS  Google Scholar 

  • 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):177–181

    Article  PubMed  CAS  Google Scholar 

  • 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 12:647–662

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):319–332

    Article  PubMed  CAS  Google Scholar 

  • 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):1019–1031

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aharoni A, O’Connell AP (2002) Gene expression analysis of strawberry achene and receptacle maturation using DNA microarrays. J Exp Bot 53(377):2073–2087

    Article  PubMed  CAS  Google Scholar 

  • 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):61–71

    Article  PubMed  CAS  Google Scholar 

  • 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:e25878

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 5:71–80

    Article  CAS  Google Scholar 

  • 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 203:178–184

    Article  CAS  Google Scholar 

  • 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):1156–1162

    Article  CAS  Google Scholar 

  • 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):633–645

    Article  PubMed  CAS  Google Scholar 

  • 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):887–890

    Article  PubMed  CAS  Google Scholar 

  • Bood KG, Zabetakis I (2002) The biosynthesis of strawberry flavor (II): biosynthetic and molecular biology studies. J Food Sci 67(1):2–8

    Article  CAS  Google Scholar 

  • Burdock GA, Fenaroli G (2009) Fenaroli’s handbook of flavor ingredients

    Google Scholar 

  • 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):49–56

    Article  CAS  Google Scholar 

  • 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):35322–35332

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):909–918

    Article  PubMed  CAS  Google Scholar 

  • 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 36:138

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Civello PM, Powell ALT, Sabehat A, Bennett AB (1999) An expansin gene expressed in ripening strawberry fruit. Plant Physiol 121(4):1273–1279

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 363:557–572

    Article  PubMed  CAS  Google Scholar 

  • 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 4:575–586

    Article  Google Scholar 

  • 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):4191–4201

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):131

    Article  CAS  Google Scholar 

  • 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):47–57

    Article  PubMed  CAS  Google Scholar 

  • 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):376–390

    Article  PubMed  CAS  Google Scholar 

  • 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):4275–4290

    Article  PubMed  CAS  Google Scholar 

  • Chai YM, Jia HF, Li CL, Dong QH, Shen YY (2011) FaPYR1 is involved in strawberry fruit ripening. J Exp Bot 62(14):5079–5089

    Article  PubMed  CAS  Google Scholar 

  • Darrow GM (1966) The strawberry: history, breeding and physiology. Holt, Rinehart, and Winston, New York

    Google Scholar 

  • 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):825–860

    Article  CAS  Google Scholar 

  • 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):1155–1161

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):2401–2411

    Article  PubMed  CAS  Google Scholar 

  • Douillard C, Guichard E (1989) Comparison by multidimensional analysis of concentrations of volatile compounds in fourteen frozen strawberry varieties [aroma, furaneol, mesifurane]. Sci Aliments 9:53–76

    CAS  Google Scholar 

  • 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):730–750

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):3688–3696

    Article  PubMed  CAS  Google Scholar 

  • 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 28:9–19

    Article  PubMed  CAS  Google Scholar 

  • Gillaspy G, Bendavid H, Gruissem W (1993) Fruits—a developmental perspective. Plant Cell 5(10):1439–1451

    Article  PubMed  PubMed Central  Google Scholar 

  • Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16(suppl 1):S170–S180

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Given NK, Venis MA, Grierson D (1988) Hormonal-regulation of ripening in the strawberry, a non-climacteric fruit. Planta 174(3):402–406

    Article  PubMed  CAS  Google Scholar 

  • 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):1528–1539

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):1479–1485

    Article  PubMed  CAS  Google Scholar 

  • 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):915–930

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hancock JF (1999) Strawberries. Crop production science in horticulture series. CABI, Wallingford, UK

    Google Scholar 

  • 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 

  • Hanson AD, Gregory JF (2011) Folate biosynthesis, turnover, and transport in plants. Annu Rev Plant Biol 62(1):105–125

    Article  PubMed  CAS  Google Scholar 

  • 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):1307–1316

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 6:29017

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):1574–1587

    Article  PubMed  CAS  Google Scholar 

  • Huber DJ (1984) Strawberry fruit softening: the potential roles of polyuronides and hemicelluloses. J Food Sci 49(5):1310–1315

    Article  CAS  Google Scholar 

  • 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):247–259

    Article  CAS  Google Scholar 

  • Jain AK, Nessler CL (2000) Metabolic engineering of an alternative pathway for ascorbic acid biosynthesis in plants. Mol Breed 6(1):73–78

    Article  CAS  Google Scholar 

  • 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–S496

    Article  PubMed  CAS  Google Scholar 

  • 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):351–357

    Article  CAS  PubMed  Google Scholar 

  • 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):188–199

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):453–465

    Article  PubMed  CAS  Google Scholar 

  • 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 14:2045–2065

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 14:2120–2133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):1277–1284

    Article  PubMed  CAS  Google Scholar 

  • Klee HJ (2010) Improving the flavor of fresh fruits: genomics, biochemistry, and biotechnology. New Phytol 187(1):44–56

    Article  PubMed  CAS  Google Scholar 

  • 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 195:536–539

    Article  CAS  Google Scholar 

  • 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 107:619–628

    Article  PubMed  CAS  Google Scholar 

  • 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 124:1059–1077

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):e0130037

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 38:1187–1193

    Article  PubMed  CAS  Google Scholar 

  • 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):2145–2153

    Article  PubMed  CAS  Google Scholar 

  • 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 57:2445–2453

    Article  PubMed  CAS  Google Scholar 

  • Manning K (1994) Changes in gene expression during strawberry fruit ripening and their regulation by auxin. Planta 194(1):62–68

    Article  CAS  Google Scholar 

  • 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):622–631

    Article  PubMed  CAS  Google Scholar 

  • 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):139–146

    Article  CAS  Google Scholar 

  • 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):89–96

    Article  PubMed  CAS  Google Scholar 

  • 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):365–371

    Article  PubMed  Google Scholar 

  • 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 1–22

    Google Scholar 

  • 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):401–417

    Article  PubMed  CAS  Google Scholar 

  • 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):598–614

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ménager I, Jost M, Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (Cv. Cigaline) during maturation. J Agric Food Chem 52:1248–1254

    Article  PubMed  CAS  Google Scholar 

  • 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):4421–4439

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):394–403

    CAS  Google Scholar 

  • 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):1471–1483

    Article  PubMed  CAS  Google Scholar 

  • 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):4901–4917

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 54:218–236

    Article  PubMed  CAS  Google Scholar 

  • 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):113–124

    Article  PubMed  CAS  Google Scholar 

  • 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 591–596

    Google Scholar 

  • 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):87–93

    Google Scholar 

  • 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 59:944–952

    Article  PubMed  CAS  Google Scholar 

  • 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):372–381

    Article  CAS  Google Scholar 

  • 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):619–631

    Google Scholar 

  • 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):3620–3624

    Article  Google Scholar 

  • Perkins-Veazie P (1995) Growth and ripening of strawberry fruit. Hortic Rev 17(8):267–297

    Google Scholar 

  • 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):105–116

    Article  CAS  Google Scholar 

  • 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):4455–4467

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):111–118

    Article  PubMed  CAS  Google Scholar 

  • 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 18:1023–1037

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 203:162–173

    Article  CAS  Google Scholar 

  • 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 163:43–60

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):272–281

    Article  PubMed  CAS  Google Scholar 

  • 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):823–831

    Article  PubMed  CAS  Google Scholar 

  • 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 179:2045–2060

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):1–15

    Article  CAS  Google Scholar 

  • 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:e0144960

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 462:665–668

    Article  PubMed  CAS  Google Scholar 

  • 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 24:293–303

    Article  CAS  Google Scholar 

  • 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 242:140–150

    Article  PubMed  CAS  Google Scholar 

  • 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):454–467

    Article  PubMed  CAS  Google Scholar 

  • 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):105–115

    Article  CAS  Google Scholar 

  • Schwab W, Davidovich-Rikanati R, Lewinsohn E (2008) Biosynthesis of plant-derived flavor compounds. Plant J 54(4):712–732

    Article  PubMed  CAS  Google Scholar 

  • 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 457–486

    Chapter  Google Scholar 

  • 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 45:227–232

    Article  CAS  Google Scholar 

  • 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):e88446

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seymour GB, Østergaard L, Chapman NH, Knapp S, Martin C (2013) Fruit development and ripening. Annu Rev Plant Biol 64:219–241

    Article  PubMed  CAS  Google Scholar 

  • Shackel KA, Greve C, Labavitch JM, Ahmadi H (1991) Cell turgor changes associated with ripening in tomato pericarp tissue. Plant Physiol 97(2):814–816

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):823–826

    Article  PubMed  CAS  Google Scholar 

  • Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, et al. (2011) The genome of woodland strawberry (Fragaria vesca), vol 43. Nature Publishing Group, pp 109–116

    Google Scholar 

  • 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 171:139–151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 122:1–10

    Article  PubMed  CAS  Google Scholar 

  • 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):461–470

    Article  CAS  Google Scholar 

  • 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 63:4741–4750

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):1–15

    Article  CAS  Google Scholar 

  • 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 6:3295–3313

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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):2037–2046

    Article  PubMed  CAS  Google Scholar 

  • 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):1635–1645

    PubMed  CAS  Google Scholar 

  • 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):1821–1832

    Article  PubMed  CAS  Google Scholar 

  • 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):1656–1662

    Article  PubMed  Google Scholar 

  • 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):696–704

    Article  PubMed  CAS  Google Scholar 

  • 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 205:218–223

    Article  CAS  Google Scholar 

  • Ulrich D, Komes D, Olbricht K, Hoberg E (2007) Diversity of aroma patterns in wild and cultivated Fragaria accessions. Genet Resour Crop Evol 54:1185–1196

    Article  CAS  Google Scholar 

  • 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 86:37–46

    Google Scholar 

  • 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 89:223–234

    CAS  Google Scholar 

  • Valpuesta V, Botella MA (2004) Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci 9(12):573–577

    Article  PubMed  CAS  Google Scholar 

  • 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):482–496

    Article  PubMed  CAS  Google Scholar 

  • 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):62–70

    Article  CAS  Google Scholar 

  • 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):2099–2106

    Article  PubMed  CAS  Google Scholar 

  • 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):141–150

    Article  CAS  Google Scholar 

  • 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 127:94–101

    Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid Biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126(2):485–493

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wyllie SG, Fellman JK (2000) Formation of volatile branched chain esters in bananas (Musa sapientum L.). J Agric Food Chem 48(8):3493–3496

    Article  PubMed  CAS  Google Scholar 

  • 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):313–322

    Article  CAS  Google Scholar 

  • Zabetakis I, Holden MA (1997) Strawberry flavour: analysis and biosynthesis. J Sci Food Agric 74(4):421–434

    Article  CAS  Google Scholar 

  • 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):1275–1284

    Article  PubMed  CAS  Google Scholar 

  • 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):1103–1118

    Article  PubMed  CAS  Google Scholar 

  • 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 123:755–778

    Article  PubMed  Google Scholar 

  • 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 159:851–870

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Biology and Biochemistry, Instituto de Hortofruticultura Subtropical y Mediterránea ‘La Mayora’, University of Malaga-Consejo Superior de Investigaciones Científicas, Campus de Teatinos, 29071, Málaga, Spain

    Delphine M. Pott, José G. Vallarino & Sonia Osorio

  2. Instituto Andaluz de Investigación y Formación Agraria y Pesquera (IFAPA), Centro de Churriana, 29140, Málaga, Spain

    Iraida Amaya

Authors
  1. Delphine M. Pott
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José G. Vallarino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sonia Osorio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Iraida Amaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Iraida Amaya .

Editor information

Editors and Affiliations

  1. Department of Agricultural Sciences, University of Helsinki, Helsinki, Finland

    Timo Hytönen

  2. Cell and Molecular Sciences, The James Hutton Institute, Dundee, United Kingdom

    Julie Graham

  3. Genetics, Genomics and Breeding, NIAB EMR, East Malling, Kent, United Kingdom

    Richard Harrison

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Pott, D.M., Vallarino, J.G., Osorio, S., Amaya, I. (2018). Fruit Ripening and QTL for Fruit Quality in the Octoploid Strawberry. In: Hytönen, T., Graham, J., Harrison, R. (eds) The Genomes of Rosaceous Berries and Their Wild Relatives. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-319-76020-9_8

Download citation

Publish with us

Policies and ethics

Search

Navigation