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

Theoretical and Applied Genetics

Volumn 126, Issue 1, 2013, Pages 33-48

  Paterson, Alistair ^a   Kassim, Angzzas ^a,b   McCallum, Susan ^c   Woodhead, Mary ^c   Smith, Kay ^c   Zait, Dzeti ^a   Graham, Julie ^c  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b UNIVERSITI TUN HUSSEIN ONN MALAYSIA   (Malaysia)

^c SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETOIN; BENZYL ALCOHOL; CANDIDATE GENES; FRUIT VOLATILES; HEXANOIC ACIDS; LINKAGE GROUPS; MAPPING POPULATIONS; NUTRACEUTICALS; QUANTITATIVE TRAIT LOCUS; RED RASPBERRY; SENSORY QUALITIES;

CULTIVATION; FATTY ACIDS; FRUITS; GENES; KETONES;

PLANTS (BOTANY);

ACETIC ACID; ACETOIN; ALKENE; BENZYL ALCOHOL; BUTYLCRESOL; CYCLOHEXANE DERIVATIVE; DAMASCENONE; GERANIOL; HEXANOIC ACID DERIVATIVE; HEXANOL; KETONE; LINALOOL; NORISOPRENOID; TERPENE;

ARTICLE; BIOLOGICAL MODEL; CHEMICAL MODEL; CHEMISTRY; CROSS BREEDING; ENVIRONMENT; FRUIT; GAS CHROMATOGRAPHY; GENETIC MARKER; GENETICS; METHODOLOGY; PLANT GENE; QUANTITATIVE TRAIT LOCUS; SEASON; STATISTICAL MODEL; TASTE;

ACETIC ACID; ACETOIN; ALKENES; BENZYL ALCOHOL; BUTYLATED HYDROXYTOLUENE; CAPROATES; CHROMATOGRAPHY, GAS; CROSSES, GENETIC; CYCLOHEXANES; ENVIRONMENT; FRUIT; GENES, PLANT; GENETIC MARKERS; HEXANOLS; KETONES; MODELS, CHEMICAL; MODELS, GENETIC; MODELS, STATISTICAL; MONOTERPENES; NORISOPRENOIDS; QUANTITATIVE TRAIT LOCI; SEASONS; TASTE; TERPENES;

RUBUS GLAUCUS; RUBUS IDAEUS;

EID: 84871923670     PISSN: 00405752     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00122-012-1957-9     Document Type: Article

References (82)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. Baldermann S, Naim M, Fleischmann P (2005) Enzymatic carotenoid degradation and aroma formation in nectarines (Prunus persica). Food Res Intern 38: 833-836.
7. Barry CS, Giovannoni JJ (2007) Ethylene and fruit ripening. J Plant Growth Reg 26: 143-159.
8. 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.
9. 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.
10. Borejsza-Wysocki W, Hrazdina G (1994) Biosynthesis of p-hydroxyphenylbutan-2-one in raspberry fruits and tissue cultures. Phytochemistry 35: 623-628.
11. 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.
12. 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.
13. Bos R, Koulman A, Woerdenbag HJ, Quax WJ, Pras N (2002) Volatile components of Anthriscus sylvestris (L.) Hoffm. J Chromatog A 966: 233-238.
14. 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.
15. 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.
16. 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.
17. 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.
18. Câmara JS, Herbert P, Marques JC, Alves A (2004) Varietal flavour of grape varieties producing Madeira wines. Anal Chim Acta 513: 203-207.
19. 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.
20. 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.
21. Du X, Qian M (2010) Flavour and health benefits of small fruits. ACS Symp Ser 1035: 27-43.
22. 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.
23. Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122: 627-633.
24. 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.
25. 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.
26. Fernie AR, Tadmor Y, Zamir D (2006) Natural genetic variation for improving crop quality. Curr Opin Plant Biol 9: 196-202.
27. Goff SA, Klee HJ (2006) Plant volatile compounds: sensory cues for health and nutritional value? Science 311: 815-819.
28. Graham J, Jennings N (2009) Raspberry breeding. In: Jain SM, Priyadarshan PM (eds) Breeding plantation tree crops, Temperate species. Springer, New York.
29. 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.
30. 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.
31. 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.
32. 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.
33. Grierson D, Tucker GA (1983) Timing of ethylene and polygalacturonase synthesis in relation to the control of tomato fruit ripening. Planta 157: 174-179.
34. 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.
35. 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.
36. Hradzina G (2006) Aroma production by tissue cultures. J Agric Food Chem 54: 1116-1123.
37. 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.
38. 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.
39. Jennings DL (1988) Raspberries and blackberries: their breeding, diseases and growth. Academic Press, London.
40. Jiang JP (1991) Variation in raspberry composition and sensory qualities as influenced by variety, season and processing. PhD thesis, University of Strathclyde, Glasgow, UK.
41. 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.
42. 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.
43. 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.
44. Kendrick MD, Chang C (2008) Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol 11: 479-485.
45. Klee HJ (2010) Improving the flavor of fresh fruits: genomics, biochemistry, and biotechnology. New Phytol 187: 44-56.
46. 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.
47. 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.
48. Lalel HJD, Singh Z, Tan SC (2003) The role of ethylene in mango fruit aroma volatiles biosynthesis. J Hortic Sci Biotech 78: 485-496.
49. Larsen M, Poll L (1993) Odour thresholds of some important aroma compounds in raspberries. Z Lebensm Unters Forsch 196: 207-213.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. Moore PP, Burrows C (2002) Genotype × environment variation in raspberry fruit aroma volatiles. Acta Hortic 585: 511-516.
58. 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.
59. 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.
60. 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.
61. Rodríguez-Concepción M (2010) Supply of precursors for carotenoid biosynthesis in plants. Arch Biochem Biophys 504: 118-122.
62. Rozen S, Skaletsky H (2000) P3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.
68. 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.
69. Singh R, Rastogi S, Dwivedi UN (2010) Phenylpropanoid metabolism in ripening fruits. Compr Rev Food Sci Food Safety 9: 398-416.
70. 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.
71. 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.
72. 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.
73. van Ooijen JW (2004) MapQTL 5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma B. V, Wageningen.
74. ® 3. 0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands.
75. Verdonk JC, Haring MA, van Tunen AJ, Schruuink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17: 1612-1624.
76. 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.
77. Winterhalter P, Rouseff R (2002) Carotenoid-derived aroma compounds: an introduction. In: ACS Symposium Series, vol 802, Oxford University Press, pp 1-19.
78. 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.
79. 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.
80. 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).
81. 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.
82. 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.