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Planta

, Volume 248, Issue 5, pp 1143–1157 | Cite as

Gene expression and metabolite accumulation during strawberry (Fragaria × ananassa) fruit development and ripening

  • Paolo Baldi
  • Saverio Orsucci
  • Mirko Moser
  • Matteo Brilli
  • Lara Giongo
  • Azeddine Si-Ammour
Original Article
  • 197 Downloads

Abstract

Main Conclusion

A coordinated regulation of different metabolic pathways was highlighted leading to the accumulation of important compounds that may contribute to the final quality of strawberry fruit.

Strawberry fruit development and ripening involve complex physiological and biochemical changes, ranging from sugar accumulation to the production of important volatiles compounds that contribute to the final fruit flavor. To better understand the mechanisms controlling fruit growth and ripening in cultivated strawberry (Fragaria × ananassa), we applied a molecular approach combining suppression subtractive hybridization and next generation sequencing to identify genes regulating developmental stages going from fruit set to full ripening. The results clearly indicated coordinated regulation of several metabolic processes such as the biosynthesis of flavonoid, phenylpropanoid and branched-chain amino acids, together with glycerolipid metabolism and pentose and glucuronate interconversion. In particular, genes belonging to the flavonoid pathway were activated in two distinct phases, the first one at the very early stages of fruit development and the second during ripening. The combination of expression analysis with metabolomic data revealed that the functional meaning of these two inductions is different, as during the early stages gene activation of flavonoid pathway leads to the production of proanthocyanidins and ellagic acid-derived tannins, while during ripening anthocyanins are the main product of flavonoid pathway activation. Moreover, the subtractive approach allowed the identification of different members of the same gene family coding for the same or very similar enzymes that in some cases showed opposite regulation during strawberry fruit development. Such regulation is an important trait that can help to understand how plants specifically channel metabolic intermediates towards separate branches of a biosynthetic pathway or use different isoforms of the same enzyme in different organs or developmental stages.

Keywords

SSH Flavonoid Phenylpropanoid Branched-chain amino acids Glycerolipid metabolism Pentose and glucuronate interconversion 

Notes

Acknowledgements

We are grateful to Urska Vrhovsek and Massimo Pindo for technical assistance. We also thank Elisa Asquini for her precious advices during RNA extraction.

Compliance with ethical standards

Conflict of interest

The authors state that they have no conflict of interest.

Supplementary material

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References

  1. 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 465:61–71CrossRefPubMedCentralGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402CrossRefGoogle Scholar
  3. Araguez I, Osorio S, Hoffmann T, Rambla JL, Medina-Escobar N, Granell A, Botella MA, Schwab W, Valpuesta V (2013) Eugenol production in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics. Plant Physiol 163:946–958CrossRefPubMedCentralGoogle Scholar
  4. Baldi P, Moser M, Brilli M, Vrhovsek U, Pindo M, Si-Ammour A (2017) Fine-tuning of the flavonoid and monolignol pathways during apple early fruit development. Planta 245:1021–1035CrossRefPubMedCentralGoogle Scholar
  5. Basu A, Rhone M, Lyons TJ (2010) Berries: emerging impact on cardiovascular health. Nutr Rev 68:168–177CrossRefPubMedCentralGoogle Scholar
  6. Bood KG, Zabetakis I (2002) The biosynthesis of strawberry flavor (II): biosynthetic and molecular biology studies. J Food Sci 67:2–8CrossRefGoogle Scholar
  7. Carbone F, Preuss A, De Vos RCH, D’Amico E, Perrotta G, Bovy AG, Martens S, Rosati C (2009) Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits. Plant Cell Environ 32:1117–1131CrossRefPubMedCentralGoogle Scholar
  8. Chen X, Chen GQ, Truksa M, Snyder CL, Shah S, Weselake RJ (2014) Glycerol-3-phosphate acyltransferase 4 is essential for the normal development of reproductive organs and the embryo in Brassica napus. J Exp Bot 65:4201–4215CrossRefPubMedCentralGoogle Scholar
  9. Chen JJ, Zhang HY, Pang YB, Cheng YJ, Deng XX, Xu J (2015) Comparative study of flavonoid production in lycopene-accumulated and blonde-flesh sweet oranges (Citrus sinensis) during fruit development. Food Chem 184:238–246CrossRefPubMedCentralGoogle Scholar
  10. Cherian S, Figueroa CR, Nair H (2014) ‘Movers and shakers’ in the regulation of fruit ripening: a cross-dissection of climacteric versus non-climacteric fruit. J Exp Bot 65:4705–4722CrossRefPubMedCentralGoogle Scholar
  11. Clancy MA, Rosli HG, Chamala S, Barbazuk WB, Civello PM, Folta KM (2013) Validation of reference transcripts in strawberry (Fragaria spp.). Mol Genet Genomics 288:671–681CrossRefPubMedCentralGoogle Scholar
  12. 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 62:4191–4201CrossRefPubMedCentralGoogle Scholar
  13. Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H, Stymne H (2000) Phospholipid: diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci USA 97:6487–6492CrossRefPubMedCentralGoogle Scholar
  14. Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030CrossRefPubMedCentralGoogle Scholar
  15. Estrada-Johnson E, Csukasi F, Pizarro CM, Vallarino JG, Kiryakova Y, Vioque A, Brumos J, Medina-Escobar N, Botella MA, Alonso JM, Fernie AR, Sanchez-Sevilla JF, Osorio S, Valpuesta V (2017) Transcriptomic analysis in strawberry fruits reveals active auxin biosynthesis and signaling in the ripe receptacle. Front Plant Sci 8:889CrossRefPubMedCentralGoogle Scholar
  16. Fan JL, Yan CS, Xu CC (2013) Phospholipid: diacylglycerol acyltransferase-mediated triacylglycerol biosynthesis is crucial for protection against fatty acid-induced cell death in growing tissues of Arabidopsis. Plant J 76:930–942CrossRefPubMedCentralGoogle Scholar
  17. Fischer TC, Mirbeth B, Rentsch J, Sutter C, Ring L, Flachowsky H, Habegger R, Hoffmann T, Hanke MV, Schwab W (2014) Premature and ectopic anthocyanin formation by silencing of anthocyanidin reductase in strawberry (Fragaria × ananassa). New Phytol 201:440–451CrossRefPubMedCentralGoogle Scholar
  18. Gasperotti M, Masuero D, Guella G, Palmieri L, Martinatti P, Pojer E, Mattivi F, Vrhovsek U (2013) Evolution of ellagitannin content and profile during fruit ripening in Fragaria spp. J Agric Food Chem 61:8597–8607CrossRefPubMedCentralGoogle Scholar
  19. 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 28:9–19CrossRefGoogle Scholar
  20. Gidda SK, Shockey JM, Rothstein SJ, Dyer JM, Mullen RT (2009) Arabidopsis thaliana GPAT8 and GPAT9 are localized to the ER and possess distinct ER retrieval signals: functional divergence of the dilysine ER retrieval motif in plant cells. Plant Physiol Biochem 47:867–879CrossRefPubMedCentralGoogle Scholar
  21. Gottardini E, Cristofori A, Pellegrini E, La Porta N, Nali C, Baldi P, Sablok G (2016) Suppression substractive hybridization and ngs reveal differential transcriptome expression profiles in wayfaring tree (Viburnum lantana L.) treated with Ozone. Front Plant Sci 7:713CrossRefPubMedCentralGoogle Scholar
  22. 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 146:1528–1539CrossRefPubMedCentralGoogle Scholar
  23. Gutierrez E, Garcia-Villaraco A, Lucas JA, Gradillas A, Gutierrez-Manero FJ, Ramos-Solano B (2017) Transcriptomics, Targeted metabolomics and gene expression of blackberry leaves and fruits indicate flavonoid metabolic flux from leaf to red fruit. Front Plant Sci 8:472CrossRefPubMedCentralGoogle Scholar
  24. 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 54:1479–1485CrossRefPubMedCentralGoogle Scholar
  25. Hartl K, Denton A, Franz-Oberdorf K, Hoffmann T, Spornraft M, Usadel B, Schwab W (2017) Early metabolic and transcriptional variations in fruit of natural white-fruited Fragaria vesca genotypes. Sci Rep 7:45113CrossRefPubMedCentralGoogle Scholar
  26. Huang J, Gu M, Lai Z, Fan B, Shi K, Zhou YH, Yu JQ, Chen Z (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153:1526–1538CrossRefPubMedCentralGoogle Scholar
  27. Huntley AL (2009) The health benefits of berry flavonoids for menopausal women: cardiovascular disease, cancer and cognition. Maturitas 63:297–301CrossRefPubMedCentralGoogle Scholar
  28. Jimenez-Bermudez S, Redondo-Nevado J, Munoz-Blanco J, Caballero JL, Lopez-Aranda JM, Valpuesta V, Pliego-Alfaro F, Quesada MA, Mercado JA (2002) Manipulation of strawberry fruit softening by antisense expression of a pectate lyase gene. Plant Physiol 128:751–759CrossRefPubMedCentralGoogle Scholar
  29. Koeduka T, Fridman E, Gang DR, Vassao DG, Jackson BL, Kish CM, Orlova I, Spassova SM, Lewis NG, Noel JP, Baiga TJ, Dudareva N, Pichersky E (2006) Eugenol and isoeugenol, characteristic aromatic constituents of spices, are biosynthesized via reduction of a coniferyl alcohol ester. Proc Natl Acad Sci USA 103:10128–10133CrossRefPubMedCentralGoogle Scholar
  30. Lee YK, Kim IJ (2011) Modulation of fruit softening by antisense suppression of endo-beta-1,4-glucanase in strawberry. Mol Breed 27:375–383CrossRefGoogle Scholar
  31. Leone A, Bleve-Zacheo T, Gerardi C, Melillo MT, Leo L, Zacheo G (2006) Lipoxygenase involvement in ripening strawberry. J Agric Food Chem 54:6835–6844CrossRefPubMedCentralGoogle Scholar
  32. Li J, Yuan R (2008) NAA and ethylene regulate expression of genes related to ethylene biosynthesis, perception, and cell wall degradation during fruit abscission and ripening in ‘Delicious’ apples. J Plant Growth Regul 27:283–295CrossRefGoogle Scholar
  33. Mandave P, Kuvalekar A, Mantri N, Autal Islam M, Ranjekar P (2017) Cloning, expression and molecular modeling of the anthocyanidin reductase (FaANR) gene during strawberry fruit development. Fruits 72:139–147CrossRefGoogle Scholar
  34. Marin-Rodriguez MC, Orchard J, Seymour GB (2002) Pectate lyases, cell wall degradation and fruit softening. J Exp Bot 53:2115–2119CrossRefPubMedCentralGoogle Scholar
  35. 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 168:598–614CrossRefPubMedCentralGoogle Scholar
  36. Meier U, Graf H, Hack H, Hess M, Kennel W, Klose R, Mappes D, Seipp D, Stauss R, Streif J, Tvd Boom (1994) Phenological growth stages of pome fruits (Malus domestica Borkh. and Pyrus communis L.), stone fruits (Prunus species), currants (Ribes species) and strawberry (Fragaria × ananassa Duch.). Nachrichtenblatt des Deutschen Pflanzenschutzdienstes 46:141–153Google Scholar
  37. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucl Acids Res 35:W182–W185CrossRefPubMedCentralGoogle Scholar
  38. Moyano E, Portero-Robles I, Medina-Escobar N, Valpuesta V, Munoz-Blanco J, Caballero JL (1998) A fruit-specific putative dihydroflavonol 4-reductase gene is differentially expressed in strawberry during the ripening process. Plant Physiol 117:711–716CrossRefPubMedCentralGoogle Scholar
  39. Negri AS, Allegra D, Simoni L, Rusconi F, Tonelli C, Espen L, Galbiati M (2015) Comparative analysis of fruit aroma patterns in the domesticated wild strawberries “Profumata di Tortona” (F. moschata) and “Regina delle Valli” (F. vesca). Front. Plant Sci 6:56Google Scholar
  40. Pandey A, Misra P, Choudhary D, Yadav R, Goel R, Bhambhani S, Sanyal I, Trivedi R, Trivedi PK (2015) AtMYB12 expression in tomato leads to large scale differential modulation in transcriptome and flavonoid content in leaf and fruit tissues. Sci Rep 5:12412CrossRefPubMedCentralGoogle Scholar
  41. Panjehkeh N, Backhouse D, Taji A (2010) Role of proanthocyanidins in resistance of the legume Swainsona formosa to Phytophthora cinnamomi. J Phytopathol 158:365–371CrossRefGoogle Scholar
  42. Pasay C, Mounsey K, Stevenson G, Davis R, Arlian L, Morgan M, Vyszenski-Moher D, Andrews K, McCarthy J (2010) Acaricidal activity of eugenol based compounds against scabies mites. PLoS One 5:e12079CrossRefPubMedCentralGoogle Scholar
  43. Peirson SN, Butler JN, Foster RG (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucl Acids Res 31:e73CrossRefPubMedCentralGoogle Scholar
  44. Perkins-Veazie P (2010) Growth and Ripening of Strawberry Fruit. Horticultural Reviews. Wiley, USA, pp 267–297CrossRefGoogle Scholar
  45. 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 66:4455–4467CrossRefPubMedCentralGoogle Scholar
  46. Quesada MA, Blanco-Portales R, Pose S, Garcia-Gago JA, Jimenez-Bermudez S, Munoz-Serrano A, Caballero JL, Pliego-Alfaro F, Mercado JA, Munoz-Blanco J (2009) Antisense down-regulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiol 150:1022–1032CrossRefPubMedCentralGoogle Scholar
  47. Ring L, Yeh SY, Hucherig S, Hoffmann T, Blanco-Portales R, Fouche M, Villatoro C, Denoyes B, Monfort A, Caballero JL, Munoz-Blanco J, Gershenson J, Schwab W (2013) Metabolic interaction between anthocyanin and lignin biosynthesis is associated with peroxidase FaPRX27 in strawberry fruit. Plant Physiol 163:43–60CrossRefPubMedCentralGoogle Scholar
  48. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucl Acids Res 37:e45CrossRefPubMedCentralGoogle Scholar
  49. Salvatierra A, Pimentel P, Moya-Leon MA, Caligari PDS, Herrera R (2010) Comparison of transcriptional profiles of flavonoid genes and anthocyanin contents during fruit development of two botanical forms of Fragaria chiloensis ssp chiloensis. Phytochemistry 71:1839–1847CrossRefPubMedCentralGoogle Scholar
  50. Sanchez-Sevilla JF, Vallarino JG, Osorio S, Bombarely A, Pose D, Merchante C, Botella MA, Amaya I, Valpuesta V (2017) Gene expression atlas of fruit ripening and transcriptome assembly from RNA-seq data in octoploid strawberry (Fragaria × ananassa). Sci Rep 7:13737CrossRefPubMedCentralGoogle Scholar
  51. Santiago-Domenech N, Jimenez-Bemudez S, Matas AJ, Rose JKC, Munoz-Blanco J, Mercado JA, Quesada MA (2008) Antisense inhibition of a pectate lyase gene supports a role for pectin depolymerization in strawberry fruit softening. J Exp Bot 59:2769–2779CrossRefPubMedCentralGoogle Scholar
  52. 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 197:454–467CrossRefPubMedCentralGoogle Scholar
  53. Severo J, Tiecher A, Chaves FC, Silva JA, Rombaldi CV (2011) Gene transcript accumulation associated with physiological and chemical changes during developmental stages of strawberry cv. Camarosa. Food Chem 126:995–1000CrossRefGoogle Scholar
  54. Seymour GB, Ostergaard L, Chapman NH, Knapp S, Martin C (2013) Fruit development and ripening. In: Merchant SS (ed) Annual review of plant biology, vol 64, pp 219–241CrossRefPubMedCentralGoogle Scholar
  55. Singh BK, Shaner DL (1995) Biosynthesis of branched-chain amino-acids—from test-tube to field. Plant Cell 7:935–944CrossRefPubMedCentralGoogle Scholar
  56. Solovchenko A, Schmitz-Eiberger M (2003) Significance of skin flavonoids for UV-B-protection in apple fruits. J Exp Bot 54:1977–1984CrossRefPubMedCentralGoogle Scholar
  57. Song J, Du LN, Li L, Kalt W, Palmer LC, Fillmore S, Zhang Y, Zhang ZQ, Li XH (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 122:1–10CrossRefPubMedCentralGoogle Scholar
  58. Sun W, Meng XY, Liang LJ, Li YQ, Zhou TT, Cai XQ, Wang L, Gao X (2017) Overexpression of a Freesia hybrida flavonoid 3-O-glycosyltransferase gene, Fh3GT1, enhances transcription of key anthocyanin genes and accumulation of anthocyanin and flavonol in transgenic petunia (Petunia hybrida). In Vitro Cell Dev Biol Plant 53:478–488CrossRefGoogle Scholar
  59. Ulrich D, Komes D, Olbricht K, Hoberg E (2006) Diversity of aroma patterns in wild and cultivated Fragaria accessions. Genet Resour Crop Evol 54:1185CrossRefGoogle Scholar
  60. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA (2007) Primer3Plus, an enhanced web interface to Primer3. Nucl Acids Res 35:W71–W74CrossRefPubMedCentralGoogle Scholar
  61. Vauzour D, Vafeiadou K, Rendeiro C, Corona G, Spencer J (2010) The inhibitory effects of berry-derived flavonoids against neurodegenerative processes. J Berry Res 1:45–52Google Scholar
  62. Villarreal NM, Marina M, Nardi CF, Civello PM, Martinez GA (2016) Novel insights of ethylene role in strawberry cell wall metabolism. Plant Sci 252:1–11CrossRefPubMedCentralGoogle Scholar
  63. Vogt T (2010) Phenylpropanoid Biosynthesis. Mol Plant 3:2–20CrossRefGoogle Scholar
  64. Vrhovsek U, Masuero D, Gasperotti M, Franceschi P, Caputi L, Viola R, Mattivi F (2012) A versatile targeted metabolomics method for the rapid quantification of multiple classes of phenolics in fruits and beverages. J Agric Food Chem 60:8831–8840CrossRefGoogle Scholar
  65. Wang SM, Li WJ, Liu YX, Li H, Ma Y, Zhang ZH (2017) Comparative transcriptome analysis of shortened fruit mutant in woodland strawberry (Fragaria vesca) using RNA-Seq. J Integrative Agric 16:828–844CrossRefGoogle Scholar
  66. Willson MF, Whelan CJ (1990) The evolution of fruit color in fleshy-fruited plants. Am Nat 136:790–809CrossRefGoogle Scholar
  67. Yin R, Han K, Heller W, Albert A, Dobrev PI, Zazimalova E, Schaffner AR (2013) Kaempferol 3-O-rhamnoside-7-O-rhamnoside is an endogenous flavonol inhibitor of polar auxin transport in Arabidopsis shoots. New Phytol 201:466–475CrossRefPubMedCentralGoogle Scholar
  68. Youdim KA, Martin A, Joseph JA (2000) Incorporation of the elderberry anthocyanins by endothelial cells increases protection against oxidative stress. Free Radic Biol Med 29:51–60CrossRefGoogle Scholar
  69. Youssef SM, Amaya I, Lopez-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-beta-1,4-glucanase genes on strawberry fruit softening. Mol Breed 31:313–322CrossRefGoogle Scholar
  70. Zabetakis I, Holden MA (1997) Strawberry flavour: analysis and biosynthesis. J Sci Food Agric 74:421–434CrossRefGoogle Scholar
  71. Zhang YC, Li WJ, Dou YJ, Zhang JX, Jiang GH, Miao LX, Han GF, Liu YX, Li H, Zhang ZH (2015) Transcript quantification by RNA-Seq reveals differentially expressed genes in the red and yellow fruits of Fragaria vesca. PLoS One 10:e0144356CrossRefPubMedCentralGoogle Scholar
  72. Zheng ZF, Xia Q, Dauk M, Shen WY, Selvaraj G, Zou JT (2003) Arabidopsis AtGPAT1, a member of the membrane-bound glycerol-3-phosphate acyltransferase gene family, is essential for tapetum differentiation and male fertility. Plant Cell 15:1872–1887CrossRefPubMedCentralGoogle Scholar
  73. Zhou HC, Li G, Zhao X (2016) Comparative analysis of pectate lyase in relation to softening in strawberry fruits. Can J Plant Sci 96:604–612CrossRefGoogle Scholar
  74. Zorrilla-Fontanesi Y, Rambla JL, Cabeza A, Medina JJ, Sanchez-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 159:851–870CrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Paolo Baldi
    • 1
  • Saverio Orsucci
    • 1
  • Mirko Moser
    • 1
  • Matteo Brilli
    • 1
    • 2
  • Lara Giongo
    • 1
  • Azeddine Si-Ammour
    • 1
  1. 1.Department of Genomics and Biology of Fruit Crops, Research and Innovation CentreFondazione Edmund MachSan Michele all’AdigeItaly
  2. 2.Department of BiosciencesUniversity of MilanMilanItaly

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