Environmental and Seasonal Influences on Red Raspberry Flavour

Environmental and Seasonal Influences on Red Raspberry Flavour

Theor Appl Genet DOI 10.1007/s00122-012-1957-9 ORIGINAL PAPER Environmental and seasonal influences on red raspberry flavour volatiles and identification of quantitative trait loci (QTL) and candidate genes Alistair Paterson • Angzzas Kassim • Susan McCallum • Mary Woodhead • Kay Smith • Dzeti Zait • Julie Graham Received: 18 May 2012 / Accepted: 27 July 2012 Ó Springer-Verlag 2012 Abstract Raspberry volatiles are important for percep- Introduction tions of sensory quality, mould resistance and some have nutraceutical activities. Twelve raspberry character vola- Flavour character in fruit originates through interactions tiles were quantified, 11 of them in fruit from two seasons, between sugars, organic acids and a subset of approxi- from plants from the Glen Moy 9 Latham mapping pop- mately 200 volatile compounds (Klesk et al. 2004). Rasp- ulation growing in both open field and under cover (poly- berry fruit produce an array of volatile compounds tunnels). Effects of season and environment were examined (Robertson et al. 1995; Aprea et al. 2010) with content for their impact on the content of a-ionone, a-ionol, showing significant variations influenced by genotype, b-ionone, b-damascenone, linalool, geraniol, benzyl alco- environment and season which impacts on flavour (Moore hol, (Z)-3-hexenol, acetoin, acetic and hexanoic acids, and Burrows 2002; Du and Qian 2010). Of the 230 vola- whilst raspberry ketone was measured in one season. A tiles characterised in raspberry, only 12 have been identi- significant variation was observed in fruit volatiles in all fied as of character impact (Jiang 1991; Larsen et al. 1991): progeny between seasons and method of cultivation. a-, b-ionones, a-ionol, b-damascenone, linalool, geraniol, Quantitative trait loci were determined and mapped to six (Z)-3-hexenol, benzyl alcohol, acetoin, raspberry ketone, of the seven linkage groups, as were candidate genes in the acetic and hexanoic acids (Table 1). These are produced volatiles pathways. from primary metabolites via several pathways during fruit ripening (Buttery and Ling 1993; Schaffer et al. 2007), notably from fatty acids, terpenes and carotenoid break- down and phenylpropanoid biosynthesis (Table 1; Fig. 1). A few genes in volatile biosynthesis pathways have Communicated by H. Nybom. recently been mapped in raspberry (Woodhead et al. 2010). Electronic supplementary material The online version of this Improving fruit flavour, a set of complex, multigenic article (doi:10.1007/s00122-012-1957-9) contains supplementary traits provides unique challenges in fruit breeding. Selec- material, which is available to authorized users. tion for yield, size and shelf-life characteristics have had negative effects on fruit flavour, notably in tomato (Goff A. Paterson Á A. Kassim Á D. Zait Strathclyde Institute of Pharmacy and Biomedical Sciences, and Klee 2006) but also strawberries, where cultivated University of Strathclyde, 161 Cathedral Street, fruits have less flavour than wild berries due to the loss of Glasgow G4 0RE, Scotland, UK enzymic activities during domestication (Aharoni et al. 2004). Cultivars with premium characters including A. Kassim FKAAS, Universiti Tun Hussein Onn Malaysia, improved flavour encourage greater fruit consumption with 86400 Parit Raja, Johor, Malaysia many associated health benefits to the human diet. The breeding process in raspberry is lengthy, up to 15 years & S. McCallum Á M. Woodhead Á K. Smith Á J. Graham ( ) from the first cross to the release of a new cultivar (Graham CMS, The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK and Jennings 2009). A strategy that allows early selections e-mail: [email protected]; [email protected] for sensory quality in terms of flavour volatile content 123 Theor Appl Genet Table 1 Raspberry character volatiles (Jiang 1991; Larsen and Poll 1993) Aroma compound Chemical structure Metabolic pathway Candidate gene Sensory descriptor a-Ionone o Carotenoid Phytoene synthase, PSY Berry, cherry, woody, Carotenoid cleavage enzyme, CCD violet a-Ionol Carotenoid Phytoene synthase, PSY Hot tea, lemon, sweet, Carotenoid cleavage enzyme, CCD violet OH b-Ionone O Carotenoid Phytoene synthase, PSY Almond, balsam, berry, Carotenoid cleavage enzyme, CCD orange, woody, rose b-Damascenone O Carotenoid Phytoene synthase, PSY Apple, smoky, woody, Carotenoid cleavage enzyme, CCD nutty, citrus, rose Linalool HO Monoterpenes 1-deoxy-D-xylulose 5-phosphate Lemon, floral, sweet, synthase, DXS orange Linalool synthase, LIS Geraniol Monoterpenes 1-deoxy-D-xylulose 5-phosphate Apple, apricot, berry, HO synthase, DXS rose, sweet Geraniol synthase, GES Benzyl alcohol Fatty acids Alcohol dehydrogenase, ADH Berry, cherry, citrus, walnut OH Acetic acid O Fatty acids Pungent, sour, vinegar OH Hexanoic acid O Fatty acids Cheese, fatty, sour OH (Z)-3-hexenol OH Fatty acids Alcohol dehydrogenase, ADH Pungent, green, piney Acetoin O Fatty acids HMG-CoA reductase, Butter, creamy Acetoin synthase OH Raspberry ketone O Phenylpropanoid Benzalacetone synthase, BAS Raspberry, sweet HO would be valuable. This requires a greater understanding of susceptible (Baldermann et al. 2005) to oxidation by reg- the genetic control of the pathways involved in volatile iospecific carotenoid cleavage dioxygenases (CCD) char- synthesis, environmental factors influencing volatile pro- acterised in Arabidopsis (Auldridge et al. 2006), tomato duction and contributions of impact volatile compounds to (Simkin et al. 2004), grape (Mathieu et al. 2005) and peach sensory character in raspberry. As in grape (Caˆmara et al. (Brandi et al. 2011). Such volatiles contribute to differen- 2004), a-, b-ionones, a-ionol and b-damascenone (C13 tiating varietal fruits and yield health benefits from con- norisoprenoid volatiles) are important for flavour. These sequent nutraceutical phytochemical intake: b-ionone, for are formed by carotenoid breakdown (Fig. 1) (Winterhalter example, is reported to act as a chemopreventative against and Rouseff 2002) via the plastidial pathway (Hampel et al. colon cancer cells (Janakiram et al. 2008). 2007) and confer desirable ‘‘berry’’, ‘‘honey’’, ‘‘sweet’’ and Raspberry monoterpene volatiles, linalool and geraniol, ‘‘rose’’ notes to fruit (Table 1). Precursor double bonds are are synthesised from isopentenyl pyrophosphate (IPP) by 123 Theor Appl Genet Fig. 1 Isoprenoid metabolism monoterpene synthases (Fig. 1) (Hampel et al. 2007). Such These volatiles can be detected at a distance from a plant, compounds can also be synthesised and accumulated in serving as attractants or deterrents for pollinators or her- roots and rhizomes (Bos et al. 2002; Chen et al. 2004). bivores (Dudareva and Pichersky 2000; Pichersky and 123 Theor Appl Genet Gershenzon 2002), acting also against plant pathogens. Materials and methods Volatile release is thought to be developmentally regulated (Dudareva et al. 2003; Arimura et al. 2004). Geraniol is a Fruit samples natural antioxidant reported to inhibit polyamine biosyn- thesis in human colon cancer cells (Carnesecchi et al. Fruits from a full-sib family from a red raspberry cross, 2001) and suppress pancreatic tumour growth (Burke et al. European cv. Glen Moy 9 North American cv. Latham, 1997). were utilised (Graham et al. 2004). ‘Latham’ yields small, Raspberry fruit accumulate the phenylpropanoid firm, dark glossy fruit, both sweet and aromatic, late in the p-hydroxyphenylbutan-2-one (raspberry ketone) with season, whereas ‘Glen Moy’ produces large, pale, soft content correlated with those of anthocyanins and soluble berries of very sweet flavour character earlier in the season. solids—Brix (Borejsza-Wysocki and Hrazdina 1994). The entire segregating population of 330 individuals and Although only a small proportion of total volatiles both parents were planted at two field locations, one open (Borejsza-Wysocki et al. 1992), it has been reported to be and one under cover (polytunnel, PT) (McCallum et al. a key determinant of raspberry flavour (Hradzina 2006). 2010), in Invergowrie, Dundee, UK in randomised com- Raspberry ketone is produced via a two-stage reaction plete block trials with three replicates and two plant plots at utilising 4-coumaroyl-CoA and malonyl-CoA (Borejsza- both locations. Fruits from a subset of 188 progeny from Wysocki and Hrazdina 1996) with rate-limiting steps two replicate field plants (parents and progeny) were hand catalysed by benzalacetone synthase, a bifunctional harvested in 2006 and 2007 and also from replicate plants polyketide synthase producing both 4-hydroxybenzalace- grown under polytunnel in 2007 when the bush was fully tone and naringenin chalcone. This is encoded by the ripe. Berries, harvested at a similar time of day and raspberry gene, RiPKS4 (Zheng and Hrazdina 2008), from the same side of the plant, were immediately stored at whereas that encoding the enzyme for conversion of -20 °C. p-hydroxyacetone to raspberry ketone (p-hydroxybuta- none) has yet to be identified. Volatiles extraction (HS/SPME) and analysis (GC-FID) Certain volatiles produced by fatty acid metabolism are important: (Z)-3-hexenol, benzyl alcohol, acetoin, acetic Frozen raspberries were thawed overnight at 4 °C, and hexanoic acids. Ethylene and two specific enzymes homogenised with a glass rod, 2.5 g weighed and volumes alcohol acyltransferase (AAT) and alcohol dehydrogenase made up to 5 ml with distilled water. The puree, in a 70 °C (ADH) are also implicated in fruit ripening and flavour jacketed (30 ml) vial, was equilibrated for 15 min with profiles (Speirs et al. 1998). agitation.

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