Skip to main content
Log in

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

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • 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 465:61–71

    Article  CAS  PubMed Central  Google Scholar 

  • 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 25:3389–3402

    Article  CAS  Google Scholar 

  • 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 163:946–958

    Article  CAS  PubMed Central  Google Scholar 

  • 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 245:1021–1035

    Article  CAS  PubMed Central  Google Scholar 

  • Basu A, Rhone M, Lyons TJ (2010) Berries: emerging impact on cardiovascular health. Nutr Rev 68:168–177

    Article  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 32:1117–1131

    Article  CAS  PubMed Central  Google Scholar 

  • 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 65:4201–4215

    Article  CAS  PubMed Central  Google Scholar 

  • 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 184:238–246

    Article  CAS  PubMed Central  Google Scholar 

  • 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 65:4705–4722

    Article  CAS  PubMed Central  Google Scholar 

  • Clancy MA, Rosli HG, Chamala S, Barbazuk WB, Civello PM, Folta KM (2013) Validation of reference transcripts in strawberry (Fragaria spp.). Mol Genet Genomics 288:671–681

    Article  CAS  PubMed Central  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 62:4191–4201

    Article  CAS  PubMed Central  Google Scholar 

  • 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 97:6487–6492

    Article  CAS  PubMed Central  Google Scholar 

  • 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 93:6025–6030

    Article  CAS  PubMed Central  Google Scholar 

  • 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 8:889

    Article  PubMed Central  Google Scholar 

  • 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 76:930–942

    Article  CAS  PubMed Central  Google Scholar 

  • 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 201:440–451

    Article  CAS  PubMed Central  Google Scholar 

  • 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 61:8597–8607

    Article  CAS  PubMed Central  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  CAS  Google Scholar 

  • 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 47:867–879

    Article  CAS  PubMed Central  Google Scholar 

  • 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 7:713

    Article  PubMed Central  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 146:1528–1539

    Article  CAS  PubMed Central  Google Scholar 

  • 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 8:472

    Article  PubMed Central  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 54:1479–1485

    Article  CAS  PubMed Central  Google Scholar 

  • 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 7:45113

    Article  PubMed Central  Google Scholar 

  • 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 153:1526–1538

    Article  CAS  PubMed Central  Google Scholar 

  • Huntley AL (2009) The health benefits of berry flavonoids for menopausal women: cardiovascular disease, cancer and cognition. Maturitas 63:297–301

    Article  CAS  PubMed Central  Google Scholar 

  • 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 128:751–759

    Article  CAS  PubMed Central  Google Scholar 

  • 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 103:10128–10133

    Article  CAS  PubMed Central  Google Scholar 

  • Lee YK, Kim IJ (2011) Modulation of fruit softening by antisense suppression of endo-beta-1,4-glucanase in strawberry. Mol Breed 27:375–383

    Article  CAS  Google Scholar 

  • Leone A, Bleve-Zacheo T, Gerardi C, Melillo MT, Leo L, Zacheo G (2006) Lipoxygenase involvement in ripening strawberry. J Agric Food Chem 54:6835–6844

    Article  CAS  PubMed Central  Google Scholar 

  • 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 27:283–295

    Article  CAS  Google Scholar 

  • 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 72:139–147

    Article  Google Scholar 

  • Marin-Rodriguez MC, Orchard J, Seymour GB (2002) Pectate lyases, cell wall degradation and fruit softening. J Exp Bot 53:2115–2119

    Article  CAS  PubMed Central  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 168:598–614

    Article  CAS  PubMed Central  Google Scholar 

  • 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 46:141–153

    Google Scholar 

  • 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–W185

    Article  PubMed Central  Google Scholar 

  • 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 117:711–716

    Article  CAS  PubMed Central  Google Scholar 

  • 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 6:56

    Google Scholar 

  • 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 5:12412

    Article  PubMed Central  Google Scholar 

  • Panjehkeh N, Backhouse D, Taji A (2010) Role of proanthocyanidins in resistance of the legume Swainsona formosa to Phytophthora cinnamomi. J Phytopathol 158:365–371

    Article  CAS  Google Scholar 

  • 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:e12079

    Article  PubMed Central  Google Scholar 

  • 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:e73

    Article  PubMed Central  Google Scholar 

  • Perkins-Veazie P (2010) Growth and Ripening of Strawberry Fruit. Horticultural Reviews. Wiley, USA, pp 267–297

    Chapter  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 66:4455–4467

    Article  CAS  PubMed Central  Google Scholar 

  • 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 150:1022–1032

    Article  CAS  PubMed Central  Google Scholar 

  • 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 163:43–60

    Article  CAS  PubMed Central  Google Scholar 

  • 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:e45

    Article  CAS  PubMed Central  Google Scholar 

  • 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 71:1839–1847

    Article  CAS  PubMed Central  Google Scholar 

  • 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 7:13737

    Article  PubMed Central  Google Scholar 

  • 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 59:2769–2779

    Article  CAS  PubMed Central  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 197:454–467

    Article  CAS  PubMed Central  Google Scholar 

  • 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 126:995–1000

    Article  CAS  Google Scholar 

  • 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 219–241

    Article  CAS  PubMed Central  Google Scholar 

  • Singh BK, Shaner DL (1995) Biosynthesis of branched-chain amino-acids—from test-tube to field. Plant Cell 7:935–944

    Article  CAS  PubMed Central  Google Scholar 

  • Solovchenko A, Schmitz-Eiberger M (2003) Significance of skin flavonoids for UV-B-protection in apple fruits. J Exp Bot 54:1977–1984

    Article  CAS  PubMed Central  Google Scholar 

  • 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 122:1–10

    Article  CAS  PubMed Central  Google Scholar 

  • 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 53:478–488

    Article  CAS  Google Scholar 

  • Ulrich D, Komes D, Olbricht K, Hoberg E (2006) Diversity of aroma patterns in wild and cultivated Fragaria accessions. Genet Resour Crop Evol 54:1185

    Article  Google Scholar 

  • 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–W74

    Article  PubMed Central  Google Scholar 

  • Vauzour D, Vafeiadou K, Rendeiro C, Corona G, Spencer J (2010) The inhibitory effects of berry-derived flavonoids against neurodegenerative processes. J Berry Res 1:45–52

    CAS  Google Scholar 

  • Villarreal NM, Marina M, Nardi CF, Civello PM, Martinez GA (2016) Novel insights of ethylene role in strawberry cell wall metabolism. Plant Sci 252:1–11

    Article  CAS  PubMed Central  Google Scholar 

  • Vogt T (2010) Phenylpropanoid Biosynthesis. Mol Plant 3:2–20

    Article  CAS  Google Scholar 

  • 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 60:8831–8840

    Article  CAS  Google Scholar 

  • 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 16:828–844

    Article  CAS  Google Scholar 

  • Willson MF, Whelan CJ (1990) The evolution of fruit color in fleshy-fruited plants. Am Nat 136:790–809

    Article  Google Scholar 

  • 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 201:466–475

    Article  PubMed Central  Google Scholar 

  • Youdim KA, Martin A, Joseph JA (2000) Incorporation of the elderberry anthocyanins by endothelial cells increases protection against oxidative stress. Free Radic Biol Med 29:51–60

    Article  CAS  Google Scholar 

  • 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 31:313–322

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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:e0144356

    Article  PubMed Central  Google Scholar 

  • 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 15:1872–1887

    Article  CAS  PubMed Central  Google Scholar 

  • Zhou HC, Li G, Zhao X (2016) Comparative analysis of pectate lyase in relation to softening in strawberry fruits. Can J Plant Sci 96:604–612

    Article  CAS  Google Scholar 

  • 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 159:851–870

    Article  CAS  PubMed Central  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paolo Baldi.

Ethics declarations

Conflict of interest

The authors state that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baldi, P., Orsucci, S., Moser, M. et al. Gene expression and metabolite accumulation during strawberry (Fragaria × ananassa) fruit development and ripening. Planta 248, 1143–1157 (2018). https://doi.org/10.1007/s00425-018-2962-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-2962-2

Keywords

Navigation