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Environmental and seasonal influences on red raspberry flavour volatiles and identification of quantitative trait loci (QTL) and candidate genes

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Abstract

Raspberry volatiles are important for perceptions of sensory quality, mould resistance and some have nutraceutical activities. Twelve raspberry character volatiles were quantified, 11 of them in fruit from two seasons, from plants from the Glen Moy × Latham mapping population growing in both open field and under cover (polytunnels). Effects of season and environment were examined for their impact on the content of α-ionone, α-ionol, β-ionone, β-damascenone, linalool, geraniol, benzyl alcohol, (Z)-3-hexenol, acetoin, acetic and hexanoic acids, whilst raspberry ketone was measured in one season. A significant variation was observed in fruit volatiles in all progeny between seasons and method of cultivation. Quantitative trait loci were determined and mapped to six of the seven linkage groups, as were candidate genes in the volatiles pathways.

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References

  • Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier Sun Z, Jongsma MA, Schwab W, Bouwmeester HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16:3110–3131

    Article  PubMed  CAS  Google Scholar 

  • Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17:2954–2965

    Article  PubMed  CAS  Google Scholar 

  • Aprea E, Carlin S, Giongo L, Grisenti M, Gaspari F (2010) Characterization of 14 raspberry cultivars by solid phase microextraction and relationship with gray mold susceptibility. J Agric Food Chem 58:1100–1105

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Huber DPW, Bohlmann J (2004) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa × deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (−)-germacrene d synthase, PtdTPS1. Plant J 37:603–616

    Article  PubMed  CAS  Google Scholar 

  • Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ (2006) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45:982–993

    Article  PubMed  CAS  Google Scholar 

  • Baldermann S, Naim M, Fleischmann P (2005) Enzymatic carotenoid degradation and aroma formation in nectarines (Prunus persica). Food Res Intern 38:833–836

    Article  CAS  Google Scholar 

  • Barry CS, Giovannoni JJ (2007) Ethylene and fruit ripening. J Plant Growth Reg 26:143–159

    Article  CAS  Google Scholar 

  • Battilana J, Costantini L, Emanuelli F, Sevini F, Segala C, Moser S, Velasco R, Versini G, Grando MS (2009) The 1-deoxy-d-xylulose 5-phosphate synthase gene co-localizes with a major QTL affecting monoterpene content in grapevine. Theor Appl Genet 118:653–669

    Article  PubMed  CAS  Google Scholar 

  • Beekwilder J, van der Meer IM, Simic A, Uitdewilligen J, van Arkel J, de Vos RCH, Jonker H, Verstappen FWA, Bouwmeester HJ, Sibbesen O, Qvist I, Mikkelsen JD, Hall RD (2008) Metabolism of carotenoids and apocarotenoids during ripening of raspberry fruit. BioFactors 34:57–66

    PubMed  Google Scholar 

  • Borejsza-Wysocki W, Hrazdina G (1994) Biosynthesis of p-hydroxyphenylbutan-2-one in raspberry fruits and tissue cultures. Phytochemistry 35:623–628

    Article  CAS  Google Scholar 

  • Borejsza-Wysocki W, Hrazdina G (1996) Aromatic polyketide synthases: purification, characterization and antibody development to benzalacetone synthase from raspberry fruits. Plant Physiol 110:791–799

    PubMed  CAS  Google Scholar 

  • Borejsza-Wysocki W, Goers SK, McArdle RN, Hrazdina G (1992) (p-Hydroxyphenyl) butan-2-one levels in raspberries determined by chromatographic and organoleptic methods. J Agric Food Chem 40:1176–1177

    Article  CAS  Google Scholar 

  • Bos R, Koulman A, Woerdenbag HJ, Quax WJ, Pras N (2002) Volatile components of Anthriscus sylvestris (L.) Hoffm. J Chromatog A 966:233–238

    Article  CAS  Google Scholar 

  • Brandi F, Bar E, Mourgues F, Horvath G, Turcsi E, Giuliano G, Liverani A, Tartarini S, Lewinsohn E, Rosati C (2011) Study of ‘Redhaven’ peach and its white-fleshed mutant suggests a key role of CCD4 carotenoid dioxygenase in carotenoid and norisoprenoid volatile metabolism. BMC Plant Biol 11:24

    Article  PubMed  CAS  Google Scholar 

  • Burke YD, Stark MJ, Roach SL, Sen SE, Crowell PL (1997) Inhibition of pancreatic cancer growth by the dietary isoprenoids farnesol and geraniol. AOCS Press 32:151–156

    CAS  Google Scholar 

  • Bushakra J, Stephens M, Atmadjaja A, Lewers K, Symonds V, Udall J, Chagne D, Buck E, Gardiner S (2012) Construction of black (Rubus occidentalis) and red (R. idaeus) raspberry linkage maps and their comparison to the genomes of strawberry, apple and peach. Theor Appl Genet. doi:10.1007/s00122-112-1835-5

  • Buttery RG, Ling LC (1993) Bioactive volatiles compounds from plants. In: Teranishi R, Buttery RG, and Sugisawa H (eds) ACS Symp Ser, vol 525, p 23

  • Câmara JS, Herbert P, Marques JC, Alves A (2004) Varietal flavour of grape varieties producing Madeira wines. Anal Chim Acta 513:203–207

    Article  Google Scholar 

  • Carnesecchi S, Schneider Y, Ceraline J, Duranton B, Gosse F, Seiler N, Raul F (2001) Geraniol, a component of plant essential oils, inhibits growth and polyamine biosynthesis in human colon cancer cells. J Pharmacol Exp Ther 298:197–200

    PubMed  CAS  Google Scholar 

  • Chen F, Ro DK, Petri J, Gershenzon J, Pichersky JBE, Tholl D (2004) Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiol 135:1956–1966

    Article  PubMed  CAS  Google Scholar 

  • Du X, Qian M (2010) Flavour and health benefits of small fruits. ACS Symp Ser 1035:27–43

    Article  CAS  Google Scholar 

  • Duchêne E, Butterlin G, Claudel P, Dumas V, Jaegli N, Merdinoglu D (2009) A grapevine (Vitis vinifera L.) deoxy-d-xylulose synthase gene colocates with a major quantitative trait loci for terpenol content. Theor Appl Genet 188:541–552

    Article  Google Scholar 

  • Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–633

    Article  PubMed  CAS  Google Scholar 

  • Dudareva N, Martin D, Kish CM, Kolosova N (2003) (E)-β-Ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell 15:1227–1241

    Article  PubMed  CAS  Google Scholar 

  • Dunemann F, Ulrich D, Boudichevskaia A, Grafe C (2009) QTL mapping of aroma compounds analysed by headspace solid-phase microextraction gas chromatography in the apple progeny ‘Discovery’ × ‘Prima’. Mol Breed 23:501–521

    Article  CAS  Google Scholar 

  • Fernie AR, Tadmor Y, Zamir D (2006) Natural genetic variation for improving crop quality. Curr Opin Plant Biol 9:196–202

    Article  PubMed  Google Scholar 

  • Goff SA, Klee HJ (2006) Plant volatile compounds: sensory cues for health and nutritional value? Science 311:815–819

    Article  PubMed  CAS  Google Scholar 

  • Graham J, Jennings N (2009) Raspberry breeding. In: Jain SM, Priyadarshan PM (eds) Breeding plantation tree crops, Temperate species. Springer, New York

    Google Scholar 

  • Graham J, Smith K, MacKenzie K, Jorgenson L, Hackett C, Powell W (2004) The construction of a genetic linkage map of red raspberry (Rubus idaeus subsp. idaeus) based on AFLPs, genomic-SSR and EST-SSR markers. Theor Appl Genet 109:740–749

    Article  PubMed  CAS  Google Scholar 

  • Graham J, Smith K, Tierney I, MacKenzie K, Hackett CA (2006) Mapping gene H controlling cane pubescence in raspberry and its association with resistance to cane botrytis and spur blight, rust and cane spot. Theor Appl Genet 112:818–831

    Article  PubMed  CAS  Google Scholar 

  • Graham J, Hackett C, Smith K, Woodhead M, Hein I, McCallum S (2009) Mapping QTL for developmental traits in raspberry from bud break to ripe fruit. Theor Appl Genet 118:1143–1155

    Article  PubMed  CAS  Google Scholar 

  • Graham J, Hackett CA, Smith K, Woodhead M, MacKenzie K, Tierney I, Cooke D, Bayer M (2011) Towards an understanding of the nature of resistance to Phytophthora root rot in red raspberry: is it mainly root vigour? Theor Appl Genet 123:585–601

    Article  PubMed  CAS  Google Scholar 

  • Grierson D, Tucker GA (1983) Timing of ethylene and polygalacturonase synthesis in relation to the control of tomato fruit ripening. Planta 157:174–179

    Article  CAS  Google Scholar 

  • Hamid NSA (1996) Relationships between aroma quality in juices from two frozen Scottish raspberries and thermal and enzymic treatments in processing. PhD thesis, University of Strathclyde, Glasgow, UK

  • Hampel D, Swatski A, Mosandl A, Wüst M (2007) Biosynthesis of monoterpenes and norisoprenoids in raspberry fruits (Rubus idaeus L.): the role of cytosolic mevalonate and plastidial methylerythritol phosphate pathway. J Agric Food Chem 55:9296–9304

    Article  PubMed  CAS  Google Scholar 

  • Hradzina G (2006) Aroma production by tissue cultures. J Agric Food Chem 54:1116–1123

    Article  Google Scholar 

  • Ianetta PPM, Van Den Berg J, Wheatley RE, McNicol RJ, Davies HV (1999) The role of ethylene and cell wall modifying enzymes in raspberry (Rubus idaeus) fruit ripening. Physiol Plant 105:337–346

    Article  Google Scholar 

  • Janakiram NB, Cooma I, Mohammed A, Steele VE, Rao CV (2008) β-ionone inhibits colonic aberrant crypt foci formation in rats, suppresses cell growth, and induces retinoid X receptor-α in human colonic cancer cells. Mol Cancer Ther 7:181–190

    Article  PubMed  CAS  Google Scholar 

  • Jennings DL (1988) Raspberries and blackberries: their breeding, diseases and growth. Academic Press, London

    Google Scholar 

  • Jiang JP (1991) Variation in raspberry composition and sensory qualities as influenced by variety, season and processing. PhD thesis, University of Strathclyde, Glasgow, UK

  • Josuttis M, Dietrich H, Treutter D, Will F, Linnemannsto L, Krüger E (2010) Solar UVB response of bioactives in strawberry (Fragaria × ananassa Duch. L.): a comparison of protected and open-field cultivation. J Agric Food Chem 58:12692–12702

    Article  PubMed  CAS  Google Scholar 

  • Kassim A, Poette J, Paterson A, Zait D, McCallum S, Woodhead M, Smith K, Hackett C, Graham J (2009) Environmental and seasonal influences on red raspberry anthocyanin antioxidant contents and identification of QTL. Mol Nutr Food Res 53:625–634

    Article  PubMed  CAS  Google Scholar 

  • Katzir N, Harel-Beja R, Portnoy V, Tzuri G (2008) Melon fruit quality: a genomic approach. Cucurbitaceae In: Pitrat M (ed) Proceedings of the IXth EUCARPIA meeting on genetics and breeding of Cucurbitaceae, INRA, Avignon, France, pp 231–240

  • Kendrick MD, Chang C (2008) Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol 11:479–485

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Klesk K, Qian M, Martin RR (2004) Aroma extract dilution analysis of cv. Meeker (Rubus idaeus L.) red raspberries from Oregon and Washington. J Agric Food Chem 52:5155–5161

    Article  PubMed  CAS  Google Scholar 

  • Kondo S, Yazama F, Sungcome K, Kanlayanarat S, Seto H (2004) Changes in jasmonates of mangoes during development and storage after varying harvest times. J Am Soc Hortic Sci 129:152–157

    CAS  Google Scholar 

  • Lalel HJD, Singh Z, Tan SC (2003) The role of ethylene in mango fruit aroma volatiles biosynthesis. J Hortic Sci Biotech 78:485–496

    CAS  Google Scholar 

  • Larsen M, Poll L (1993) Odour thresholds of some important aroma compounds in raspberries. Z Lebensm Unters Forsch 196:207–213

    Article  Google Scholar 

  • Larsen M, Poll L, Callesen O, Lewis M (1991) Relations between the content of aroma compounds and the sensory evaluation of 10 raspberry varieties (Rubus idaeus L.). Acta Agric Scand 41:447–454

    Article  CAS  Google Scholar 

  • Lay-Lee M, Dellapenna D, Ross GS (1990) Changes in mRNA and protein during ripening in apple fruit (Malus domestica Borkh. cv. ‘Golden Delicious’). Plant Physiol 94:850–853

    Article  Google Scholar 

  • Lutz-Wahl S, Fischer P, Schmidt-Dannert C, Wohlleben W (1993) Stereo- and regioselective hydroxylation of α-ionone by Streptomyces strains. Appl Environ Microbiol 64:3878–3881

    Google Scholar 

  • Marais J, Van Wyck CJ, Rapp A (1991) Carotenoid levels in maturing grapes as affected by climate regions, sunlight and shade. S Afr J Enol Vitic 12:84–89

    Google Scholar 

  • Mathieu S, Terrier N, Procureur J (2005) A carotenoid cleavage dioxygenase from Vitis vinifera L.: functional characterization and expression during grape berry development in relation to C13-norisoprenoid accumulation. J Exp Bot 56:2721–2731

    Article  PubMed  CAS  Google Scholar 

  • Mathieu S, Dal Cin V, Fei Z, Li H, Bliss P, Taylor MG, Klee HJ, Tieman DM (2009) Flavour compounds in tomato fruits: identification of loci and potential pathways affecting volatile composition. J Exp Bot 60:325–337

    Article  PubMed  CAS  Google Scholar 

  • McCallum S, Woodhead M, Hackett CA, Kassim A, Paterson A, Graham J (2010) Influence of environment and season on measures of red raspberry colour, association with anthocyanin content and identification of QTL and potential candidate gene sequences. Theor Appl Genet 121:611–627

    Article  PubMed  CAS  Google Scholar 

  • Moore PP, Burrows C (2002) Genotype × environment variation in raspberry fruit aroma volatiles. Acta Hortic 585:511–516

    CAS  Google Scholar 

  • Mukkun L, Singh Z (2009) Methyl jasmonate plays a role in fruit ripening of ‘Pajaro’ strawberry through stimulation of ethylene biosynthesis. Sci Hortic 123:5–10

    Article  CAS  Google Scholar 

  • Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

    Article  PubMed  CAS  Google Scholar 

  • Robertson GW, Griffiths DW, Woodford JAT, Birch ANE (1995) Changes in the chemical composition of volatiles released by flowers and fruits of the red raspberry (Rubus idaeus) cultivar Glen Prosen. Phytochemistry 38:1175–1179

    Article  CAS  Google Scholar 

  • Rodríguez-Concepción M (2010) Supply of precursors for carotenoid biosynthesis in plants. Arch Biochem Biophys 504:118–122

    Article  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) P3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    PubMed  CAS  Google Scholar 

  • Saliba-Colombani V, Causse M, Langlois D, Philouze J, Buret M (2001) Genetic analysis of organoleptic quality in fresh market tomato. 1. Mapping QTLs for physical and chemical traits. Theor Appl Genet 102:259–272

    Article  CAS  Google Scholar 

  • Schaffer RJ, Friel EN, Souleyre EJF, Bolitho K, Thodey K, Ledger S, Bowen JH, Ma JH, Nain B, Cohen D, Gleave AP, Crowhurst RN, Janssen BJ, Yao JL, Newcomb RD (2007) A genomics approach reveals that aroma production in apple is controlled by ethylene predominantly at the final step in each biosynthetic pathway. Plant Physiol 144:1899–1912

    Article  PubMed  CAS  Google Scholar 

  • Sevini F, Marino R, Grando MS, Moser S, Versini G (2004) Mapping candidate genes and QTLs for aroma content in grape. Acta Hortic 652:439–446

    CAS  Google Scholar 

  • Sheng J, Luo Y, Wainwright H (2000) Studies on the lipoxygenase and the formation of ethylene in tomato. J Hortic Sci Biotech 75:69–71

    CAS  Google Scholar 

  • Shualev V, Korban SS, Sosinski B, Abbott AG, Aldwinckle HS, Folta KM, Iezzoni A, Main D, Arus P, Dandekar PM, Lewers K, Brown SK, Davis TM, Gardiner SE, Potter D, Veilleux RE (2008) Multiple models for Rosaceae genomics. Plant Physiol 147:985–1003

    Article  Google Scholar 

  • Simkin AJ, Schwartz SH, Auldridge M (2004) The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone, and geranylacetone. Plant J 40:882–892

    Article  PubMed  CAS  Google Scholar 

  • Singh R, Rastogi S, Dwivedi UN (2010) Phenylpropanoid metabolism in ripening fruits. Compr Rev Food Sci Food Safety 9:398–416

    Article  CAS  Google Scholar 

  • Song J, Bangerth F (1996) The effect of harvest date on aroma compound production from ‘Golden Delicious’ apple fruit and relationship to respiration and ethylene production. Postharvest Biol Technol 8:259–269

    Article  CAS  Google Scholar 

  • Speirs J, Lee E, Holt K, Yong-Duk K, Scot NS, Loveys B, Schuch W (1998) Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiol 117:1047–1058

    Article  PubMed  CAS  Google Scholar 

  • Tieman DM, Zeigler M, Schmelz EA, Taylor MG, Bliss P, Kirst M, Klee HJ (2006) Identification of loci affecting flavour volatiles emissions in tomato fruits. J Exp Bot 57:887–896

    Article  PubMed  CAS  Google Scholar 

  • van Ooijen JW (2004) MapQTL 5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma B.V, Wageningen

    Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap® 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands

  • Verdonk JC, Haring MA, van Tunen AJ, Schruuink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17:1612–1624

    Article  PubMed  CAS  Google Scholar 

  • von Lintig J, Welsch R, Bonk M, Giuliano G, Batschauer A, Kleinig H (1997) Light dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis thaliana seedlings. Plant J 12:625–634

    Article  Google Scholar 

  • Winterhalter P, Rouseff R (2002) Carotenoid-derived aroma compounds: an introduction. In: ACS Symposium Series, vol 802, Oxford University Press, pp 1–19

  • Woodhead M, McCallum S, Smith K, Cardle L, Mazzitelli L, Graham J (2008) Identification, characterisation and mapping of simple sequence repeat (SSR) markers from raspberry root and bud ESTs. Mol Breed 22:555–563

    Article  CAS  Google Scholar 

  • Woodhead M, Weir A, Smith K, McCallum S, Mackenzie K, Graham J (2010) Functional markers for red raspberry. J Am Soc Hortic Sci 135:418–427

    Google Scholar 

  • Woodhead M, Weir A, Smith K, McCallum S, Jennings N, Hackett C, Graham J (2012) Identification of QTLs for cane splitting in red raspberry (Rubus idaeus). Mol Breed (accepted)

  • Zheng D, Hrazdina G (2008) Molecular and biochemical characterization of benzalacetone synthase and chalcone synthase genes and their proteins from raspberry (Rubus idaeus L.). Arch Biochem Biophys 470:139–145

    Article  PubMed  CAS  Google Scholar 

  • Zini E, Biasioli F, Gasperi F, Mott D, Aprea E, Mark TD, Patocchi A, Gessler C, Komjanc M (2005) QTL mapping of volatile compounds in ripe apples detected by proton transfer reaction-mass spectrometry. Euphytica 145:269–279

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Christine Hackett of Bioinformatics and Statistics Scotland, Dundee Unit, JHI for statistical support in data analysis and Magali Vandroux, Elaine Reynauld and Ankit Joshi at Strathclyde University for support and help with GC-FID analysis and Micha Bayer, Linda Milne and Pete Hedley for assistance with the raspberry transcriptome database development. This work was supported by RERAD and the Horticulture LINK programme.

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Correspondence to Julie Graham.

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Communicated by H. Nybom.

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Volatile distributions across years and environments (DOCX 482 kb)

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Paterson, A., Kassim, A., McCallum, S. et al. Environmental and seasonal influences on red raspberry flavour volatiles and identification of quantitative trait loci (QTL) and candidate genes. Theor Appl Genet 126, 33–48 (2013). https://doi.org/10.1007/s00122-012-1957-9

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