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Genome-wide scans reveal genetic architecture of apple flavour volatiles

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Abstract

Flavour is an important food trait, yet little is known about the genetic architecture and mode of inheritance of apple flavour compounds. The objectives of this study were to: understand the inheritance of flavour volatiles in a clonally replicated germplasm population; unravel correlation networks of volatiles; and to use genome-wide single nucleotide polymorphism (SNP) markers to identify genomic regions that play a role in the expression of flavour volatiles. This analysis revealed that more than half of the 37 volatiles (measured by gas chromatography–mass spectrometry) showed high heritability (h 2 > 0.4), with only a small number (3 of the 37) displaying low heritability (h 2 < 0.2). Majority (~85 %) of the significant SNP loci displayed the additive mode of inheritance. Our results supported the roles of MdAAT, MdCXE and MdLOX genes in the expression of apple flavour volatiles. Effect sizes of SNP loci, some of which are associated with multiple compounds, were small (<10 %), which is consistent with a polygenic quantitative inheritance model. New genomic locations associated with multiple flavour compounds were found, and some SNPs were associated with both sensory flavour and some flavour volatiles. Simultaneous genome-wide association study for sensory flavour and flavour compounds is recommended for unravelling genetic mechanisms to facilitate marker-assisted breeding for targeted flavours.

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References

  • Arkin A, Shen P, Ross J (1997) A test case of correlation metric construction of a reaction pathway from measurements. Science 277:1275–1279

    Article  CAS  Google Scholar 

  • Baldwin EA, Scott JW, Einstein MA, Malundo TMM, Carr BT, Shewfelt RL, Tandon KS (1998) Relationship between sensory and instrumental analysis for tomato. J Am Soc Hort Sci 123:906–915

    CAS  Google Scholar 

  • Bolormaa S, Pryce JE, Hayes BJ, Goddard ME (2010) Multivariate analysis of a genome-wide association study in dairy cattle. J Dairy Sci 93:3818–3833

    Article  CAS  PubMed  Google Scholar 

  • Bolormaa S, Pyrce JE, Reverter A, Zhang YD, Barendse W, Goddard ME (2013) Multi-trait QTL mapping in beef cattle. Proc Assoc Adv Anim Breed Genet 20:515–518

    Google Scholar 

  • Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing data inference for whole genome association studies using localized haplotype clustering. Am J Hum Genet 81:1084–1097

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chagné D, Crowhurst RN, Troggio M, Davey MW, Gilmore B, Lawley C, Vanderzande S, Hellens RP, Kumar S, Cestaro A, Velasco R, Main D, Rees JD, Iezzoni A, Mockler T, Wilhelm L, van de Weg E, Gardiner SE, Bassil N, Peace C (2012a) Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS ONE 7:e31745

    Article  PubMed Central  PubMed  Google Scholar 

  • Chagné D, Krieger C, Rassam M, Sullivan M, Fraser J, André C, Pindo M, Troggio M, Gardiner SE, Henry RA, Allan AC, McGhie TK, Laing WA (2012b) QTL and candidate gene mapping for polyphenolic composition in apple fruit. BMC Plant Biol 12:12

    Article  PubMed Central  PubMed  Google Scholar 

  • Costa F, Cappellin L, Zini E, Patocchi A, Kellerhals M, Komjanc M, Gessler C, Biasioli F (2013) QTL validation and stability for volatile organic compounds (VOCs) in apple. Plant Sci 211:1–7

    Article  CAS  PubMed  Google Scholar 

  • Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–9

  • Defilippi BG, Dandekar AM, Kader AA (2005) Relationship of ethylene biosynthesis to volatile production, related enzymes, and precursor availability in apple peel and flesh tissues. J Agric Food Chem 53:3133–3141

    Article  CAS  PubMed  Google Scholar 

  • Dimick PS, Hoskin JC (1983) Review of apple flavour—state of the art. CRC Crit Rev Food Sci Nutr 18:387–409

    Article  CAS  Google Scholar 

  • Dixon J, Hewett E (2000) Factors affecting apple aroma/flavour volatile concentration: a review. NZ J Crop Hort Sci 28:155–173

    Article  CAS  Google Scholar 

  • Duan LL, Tian LL, Guo YR, Deng H, Li Z, Wang XY (2012) Principal component analysis and classification of aroma components of six apple cultivars. Sci Tech Food Ind 3:85–88

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dunemann F, Ulrich D, Malysheva-Otto L, Weber WE, Longhi S, Velasco R, Costa F (2012) Functional allelic diversity of the apple alcohol acyl-transferase gene MdAAT1 associated with fruit ester volatile contents in apple cultivars. Mol Breed 29:609–625

    Article  CAS  Google Scholar 

  • Durel C-E, Laurens F, Fouillet A, Lespinasse Y (1998) Utilisation of pedigree information to estimate genetic parameters from large, unbalanced data sets in apple. Theor Appl Genet 96:1077–1085

    Article  Google Scholar 

  • Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD, Krutovsky KV, Clair JBS, Neale DB (2009) Association genetics of coastal douglas fir (Pseudotsuga menziesu var. menziesii, Pinaceae). I. Cold-hardiness related traits. Genetics 182:1289–1302

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Flint J, Mackay TFC (2009) Genetic architecture of quantitative traits in flies, mice and humans. Genome Res 19:723–733

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2006) ASReml user guide release 2.0. VSN International Ltd, Hemel Hempstead

    Google Scholar 

  • Harker FR, Marsh KB, Young H, Murray SH, Gunson FA, Walker SB (2002) Sensory interpretation of instrumental measurements 2: sweet and acid taste of apple fruit. Postharvest Biol Technol 24:241–250

    Article  Google Scholar 

  • Hayes BJ, Goddard ME (2001) The distribution of the effects of genes affecting quantitative traits in livestock. Genet Sel Evol 33:209–229

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karlsen AM, Aaby K, Sivertsen H, Baardseth P, Ellekjær MR (1999) Instrumental and sensory analysis of fresh Norwegian and imported apples. Food Qual Prefer 10:305–314

    Article  Google Scholar 

  • Khan SA, Chibon P-Y, de Vos RCH, Schipper BA, Walraven E, Beekwilder J, van Dijk T, Finkers R, Visser RGF, van de Weg EW, Bovy A, Cestaro A, Velasco R, Jacobsen E, Schouten HJ (2012) Genetic analysis of metabolites in apple fruit indicates an mQTL hotspot for phenolic compounds on linkage group 16. J Expr Bot 63:2895–2908

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Klee HJ, Tieman DM (2013) Genetic challenges of flavour improvement in tomato. Trends Genet 29:4

    Article  Google Scholar 

  • Kumar SK, Volz RK, Alspach PA, Bus VGM (2010) Development of a recurrent apple breeding programme in New Zealand: a synthesis of results, and a proposed revised breeding strategy. Euphytica 173:207–222

    Article  Google Scholar 

  • Kumar S, Volz RK, Weskett R (2011) Genetic architecture of fruit quality traits in Malus × domestica (Borkh.) compared between own-rooted seedlings and vegetative propagules on ‘M. 9’ rootstock. Tree Genet Genomes 7:1079–1088

    Article  Google Scholar 

  • Kumar S, Garrick DG, Bink MCAM, Whitworth C, Chagné D, Volz RK (2013) Novel genomic approaches unravel genetic architecture of complex traits in apple. BMC Genomic 14:393

    Article  CAS  Google Scholar 

  • Kumar S, Raulier P, Chagné D, Whitworth C (2014) Molecular-level and trait-level differentiation between the cultivated apple (Malus × domestica Borkh.) and its main progenitor Malus sieversii. Plant Genet Resour 12:330–340

    Article  Google Scholar 

  • Laurens F (1999) Review of the current apple breeding programmes in the world: objectives for scion cultivar improvement. Acta Hortic 484:163–170

    Google Scholar 

  • Li D, Xu Y, Xu G, Gu L, Li D, Shu H (2006) Molecular cloning and expression of a gene encoding alcohol acyltransferase (MdAAT2) from apple (cv. Golden Delicious). Phytochemistry 67:658–667

    Article  CAS  PubMed  Google Scholar 

  • Lindgren D, Mullin TJ (1998) Relatedness and status number in seed orchard crops. Can J For Res 28:276–283

    Article  Google Scholar 

  • Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399

    Article  CAS  PubMed  Google Scholar 

  • Mehinagic E, Royer G, Symoneaux R, Jourjon F, Prost C (2006) Characterization of odor-active volatiles in apples: influence of cultivars and maturity stage. J Agric Food Chem 54:2678–2687

    Article  CAS  PubMed  Google Scholar 

  • Nieuwenhuizen NJ, Sa Green, Chen X, Bailleul EJD, Matich AJ, Wang MY, Atkinson RG (2013) Functional genomics reveals that a compact terpene synthase gene family can account for terpene volatile production in apple. Plant Physiol 161:787–804

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paillard NMM (1990) The flavour of apples, pears and quinces. In: Morton ID, MacLeod AJ (eds) Food flavours, Part C. The flavour of fruit. Elsevier Science Publishing Company Inc., Amsterdam, pp 1–41

    Google Scholar 

  • Rowan DD, Hunt MB, Alspach PA, Whitworth C, Oraguzie N (2009a) Heritability, genetic and phenotypic correlations of apple fruit volatiles in a genetically diverse breeding population. J Agric Food Chem 57:7944–7952

    Article  CAS  PubMed  Google Scholar 

  • Rowan DD, Hunt MB, Dimouro A, Alspach PA, Weskett R, Volz RK, Gardiner SE, Chagné D (2009b) Profiling fruit volatiles in the progeny of a ‘Royal Gala’ × ‘Granny Smith’ apple (Malus × domestica) cross. J Agric Food Chem 57:7953–7961

    Article  CAS  PubMed  Google Scholar 

  • Schaffer RJ, Friel EN, Souleyre EJF, Bolitho K, Thodey K, Ledger S, Bowen JH, Ma J-H, Nain B, Cohen D, Gleave AP, Crowhurst RN, Janssen BJ, Yao J-L, 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 Central  CAS  PubMed  Google Scholar 

  • Shepherd G (2006) Smell images and the flavour system in the human brain. Nature 444:316–321

    Article  CAS  PubMed  Google Scholar 

  • Souleyre EJF, Greenwood DR, Friel EN, Karunairetnam S, Newcomb RD (2005) An alcohol acyl transferase from apple (cv. Royal Gala), MpAAT1, produces esters involved in apple fruit flavour. FEBS J 272:3132–3144

    Article  CAS  PubMed  Google Scholar 

  • Souleyre EJF, Marshall SDG, Oakeshott JG, Russell RJ, Plummer KM, Newcomb R (2011) Biochemical characterisation of MdCXE1, a carboxylesterase from apple that is expressed during fruit ripening. Phytochemistry 7:564–571

    Article  Google Scholar 

  • Souleyre EJF, Chagné D, Chen X, Tomes S, Turner RM, Wang MY, Maddumage R, Hunt MB, Winz RA, Wiedow C, Hamiaux C, Gardiner SE, Rowan DD, Atkinson RG (2014) The AAT1 locus is critical for the biosynthesis of esters contributing to ‘ripe apple’ flavour in ‘Royal Gala’ and ‘Granny Smith’ apples. Plant J 78:903–915

    Article  CAS  PubMed  Google Scholar 

  • Steuer R (2006) On the analysis and interpretation of correlations in metabolomic data. Brief Bioinform 7:151–158

    Article  CAS  PubMed  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440–9445

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tieman D, Bliss P, McIntyre LM, Blandon-Ubeda A, Bies D, Odabasi AZ, Rodrıguez GR, van der Knaap E, Taylor MG, Goulet C, Mageroy MH, Snyder DJ, Colquhoun T, Moskowitz H, Clark DG, Sims C, Bartoshuk L, Klee HJ (2012) The chemical interactions underlying tomato flavor preferences. Curr Biol 22:1035–1039

    Article  CAS  PubMed  Google Scholar 

  • Ulrich D, Dunemann F (2012) Towards the development of molecular markers for apple volatiles. Flavour Fragr J 27:286–289

    Article  CAS  Google Scholar 

  • Ursem R, Tikunov Y, Bovy A, Van Berloo R, Van Eeuwijk F (2008) A correlation network approach to metabolic data analysis for tomato fruit. Euphytica 161:181–193

    Article  CAS  Google Scholar 

  • Vogt J, Schiller D, Ulrich D, Schwab W, Dunemann F (2013) Identification of lipoxygenase (LOX) genes putatively involved in fruit flavour formation in apple (Malus × domestica). Tree Genet Genomes 9:1493–1511

    Article  Google Scholar 

  • Wang HB, Chen XS, Xin PG, Feng T, Shi J, Ci ZJ (2007) GC–MS analysis of volatile components in several early apple cultivars. J Fruit Sci 1:003

    Google Scholar 

  • Young H, Gilbert JM, Murray SH, Ball RD (1996) Causal effects of aroma compounds on Royal Gala apple flavours. J Sci Food Agri 71:329–336

    Article  CAS  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Vroh-Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Barritt BH (2008) Md-ACS1 and Md-ACO1 genotyping of apple (Malus × domestica Borkh.) breeding parents and suitability for marker-assisted selection. Tree Genet Genomes 4:555–562

    Article  Google Scholar 

  • Zhu Y, Rudell DR, Mattheis JP (2008) Characterization of cultivar differences in alcohol acyltransferase and 1-aminocyclopropane-1-carboxylate synthase gene expression and volatile ester emission during apple fruit maturation and ripening. Postharvest Biol Technol 49:330–339

    Article  CAS  Google Scholar 

  • Zini E, Biasioli F, Gasperi F, Mott D, Aprea E, Mark T, 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

The PFR Markers and Mapping Team is thanked for help in collecting leaf samples. Slipstream Automation Ltd, New Zealand, is thanked for providing high-throughput DNA extraction services. We also thank AgResearch Invermay, New Zealand, for providing Illumina® SNP array genotyping. This research was partly supported by the New Zealand Ministry of Business, Innovation and Employment (MBIE). PFR colleagues Richard Volz and Nigel Perry are thanked for their constructive feedback.

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Authors and Affiliations

  1. The New Zealand Institute for Plant and Food Research Limited (PFR), Hawke’s Bay Research Centre, Havelock North, New Zealand

    Satish Kumar & Claire Whitworth

  2. PFR, Palmerston North Research Centre, Palmerston North, New Zealand

    Daryl Rowan, Martin Hunt & David Chagné

  3. PFR, Mount Albert Research Centre, Auckland, New Zealand

    Edwige Souleyre

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  1. Satish Kumar
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  2. Daryl Rowan
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  3. Martin Hunt
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  4. David Chagné
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  5. Claire Whitworth
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  6. Edwige Souleyre
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Correspondence to Satish Kumar.

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Kumar, S., Rowan, D., Hunt, M. et al. Genome-wide scans reveal genetic architecture of apple flavour volatiles. Mol Breeding 35, 118 (2015). https://doi.org/10.1007/s11032-015-0312-7

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