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Apple, from genome to breeding

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Abstract

Genome resources for apple (Malus × domestica Borkh), the main fruit crop of temperate regions, have been developed over the past 10 years, culminating in the sequencing of the ‘Golden Delicious’ genome. The apple genome sequence anchored to a high-density linkage map provides the apple community with new tools to identify genes and other functional elements that will enable the study of the evolution of plant genome structure, as well as facilitating genomic-assisted breeding. Transcriptomics, proteomics and metabolomics studies are greatly benefiting from the availability of an annotated genome. In this review, we report on the status of the apple genome and on current molecular and genetic tools available in apple that will improve the efficiency of the process of cultivar development; we discuss how an integrative ‘omics’ approach could greatly enhance the understanding of biological processes that determine agronomically and economically favorable phenotypes; we review the databases and bioinformatics tools that are available to manage and exploit the large amounts of biological data generated for apple and other plant genomes.

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References

  • Ackermann J, Fischer M, Amado R (1992) Changes in sugars, acids and amino acids during ripening and storage of apples (Cv. Glockenapfel). J Agri Food Chem 40:1131–1134

    Article  CAS  Google Scholar 

  • Aldasoro JJ, Aedo C, Navarro C (2005) Phylogenetic and phytogeographical relationships in Maloideae (Rosaceae) based on morphological and anatomical characters. Blumea 50(1):3–32

    Google Scholar 

  • Allan AC, Crowhurst R, Allan AC, Crowhurst R, Gleave A, Newcomb R, Shaffer (2009) In: Folta KM, Gardiner SE (eds) Genetics and genomics of the Rosaceae. Springer, New York, USA, pp 121–142

    Chapter  Google Scholar 

  • Anderson LK, Stack SM (2002) Meiotic recombination in plants. Curr Genomics 3:507–525

    Article  CAS  Google Scholar 

  • Awad MA, de Jager A, van Westing LM (2000) Flavonoid and chlorogenic acid levels in apple fruit:characterisation and variation. Sci Hort 83:249–263

    Article  CAS  Google Scholar 

  • Baldo A, Norelli JL, Farrel RE Jr, Bassett CL, Aldwinckle HS, Malnoy M (2010) Identification of genes differentially expressed during interaction of resistant and susceptible apple cultivars (Malus × domestica) with Erwinia amylovora. BMC Plant Biol 10:1

    Article  PubMed  CAS  Google Scholar 

  • Beckmann JS, Estivill X, Antonarakis SE (2007) Copy number variants and genetic traits: closer to the resolution of phenotypic to genotypic variability. Nat Rev Genet 8:639–646

    Article  PubMed  CAS  Google Scholar 

  • Bink MCAM, Boer MP, ter Braak CJF, Jansen J, Voorrips RE, van de Weg WE (2008) Bayesian analysis of complex traits in pedigreed plant populations. Euphytica 161:85–96

    Article  Google Scholar 

  • Breyne P, Dreesen R, Cannoot B, Rombaut D, Vandepoele K, Rombauts S, Vanderhaeghen R, Inzé D, Zabeau M (2003) Quantitative cDNA-AFLP analysis for genome-wide expression studies. Mol Genet Genom 269:173–179

    CAS  Google Scholar 

  • Bus VGM, Esmenjaud D, Buck E, Laurens F (2009) Application of genetic markers in rosaceous crops. In: Folta KM, Gardiner SE (eds) Genetics and genomics of the Rosaceae. USA, Springer, New York, pp 563–600

    Chapter  Google Scholar 

  • Bus VGM, Bassett HCM, Bowatte D, Chagne D, Ranatunga CA, Ulluwishewa D, Wiedow C, Gardiner SE (2010) Genome mapping of an apple scab, a powdery mildew and a woolly apple aphid resistance gene from open-pollinated Mildew Immune Selection. Tree Genet Genomes 6:477–487

    Article  Google Scholar 

  • Bushakra JM, Sargent DJ, Cabrera A, Crowhurst R, Girona EL, Velasco R, Symonds VV, van der Knaap E, Troggio M, Gardiner SE, Chagné D (2011) Rosaceae conserved orthologous set (RosCOS) markers as a tool to assess genome synteny between Malus and Fragaria. Tree Genet Genomes. doi:10.1007/s11295-011-0450-y

  • Cabrera A, Kozik A, Howad W, Arus P, Iezzoni AF, Knaap E (2009) Development and bin mapping of a Rosaceae Conserved Ortholog Set (COS) of markers. BMC Genom 10:562

    Article  CAS  Google Scholar 

  • Calenge F, Durel CE (2006) Both stable and unstable QTLs for resistance to powdery mildew are detected in apple after four years of field assessments. Mol Breed 17:329–339

    Article  Google Scholar 

  • Calenge F, Faure A, Goerre M, Gebhardt C, Van de Weg WE, Parisi L, Durel CE (2004) Quantitative Trait Loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 94(4):370–379

    Article  PubMed  CAS  Google Scholar 

  • Calenge F, Drouet D, Denancé C, Van de Weg WE, Brisset MN, Paulin JP, Durel CE (2005) Identification of a major QTL together with several minor additive or epistatic QTLs for resistance to fire blight in apple in two related progenies. Theor Appl Genet 111:128–135

    Article  PubMed  CAS  Google Scholar 

  • Cao S, Zhang Q, Zhu Z, Guo J, Chen Y, Xie H (2008) Preliminary proteomics analysis of the total proteins of flower bud induction of apple trees. Front Agric China 2:467–473

    Article  Google Scholar 

  • Cartwright DA, Troggio M, Velasco R, Gutin A (2007) Genetic mapping in the presence of genotyping errors. Genetics 176:2521–2527

    Article  PubMed  CAS  Google Scholar 

  • Celton J-M, Husselmann LHH, Madduri M, Labuschagne IF, Rees DJG (2009b) Whole transcriptome sequencing analysis of apple leaves infected by Venturia inaequalis, using Solexa sequencing technology. In: Proceedings of the Plant & Animal Genome Conference XVII: San Diego, CA, USA:W212

  • Celton JM, Tustin DS, Chagne D, Gardiner SE (2009b) Construction of a dense genetic linkage map for apple rootstocks using SSRs developed from Malus ESTs and Pyrus genomic sequences. Tree Genet Genomes 5(1):93–107

    Article  Google Scholar 

  • Cevik V, Ryder CD, Popovich A, Manning K, King GJ, Seymour GB (2010) A FRUITFULL-like gene is associated with genetic variation for fruit flesh firmness in apple (Malus domestica Borkh.). Tree Genet Genomes 6:271–279

    Article  Google Scholar 

  • Chagné D, Gasic K, Crowhurst RN, Han Y, Bassett HC, Bowatte DR, Lawrence TJ, Rikkerink EHA, Gardiner SE, Korban SS (2008) Development of a set of SNP markers present in expressed genes of the apple. Genomics 92:353–358

    Article  PubMed  CAS  Google Scholar 

  • Chagné D, Crowhurst RN, Troggio M, Davey MW, Gilmore B et al. (2012) Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS ONE 7: e31745. doi:10.1371/journal.pone.0031745

  • Churchill GA, Airey DC, Allayee H, Angel JM, Attie AD, Beatty J et al (2004) The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nat Genet 36:1133–1137

    Article  PubMed  CAS  Google Scholar 

  • Cooper M, van Eeuwijk FA, Hammer GL, Podlich DW, Messina C (2009) Modeling QTL for complex traits: detection and context for plant breeding. Curr Opin Plant Biol 12:231–240

    Article  PubMed  CAS  Google Scholar 

  • Crow KD, Wagner GP (2006) What is the role of genome duplication in the evolution of complexity and diversity? Mol Biol Evol 23:887–892

    Article  PubMed  CAS  Google Scholar 

  • Crowhurst RN, Davy M, Deng C (2006) BioView—an enterprise bioinformatics system for automated analysis and annotation of non-genomic DNA sequence. In: Proceedings of the 3rd International Rosaceae Genomics Conference, 19–22 March, Napier, New Zealand

  • Dal Cin V, Barbaro E, Danesin M, Murayama H, Velasco R, Ramina A (2009) Fruitlet abscission: A cDNA-AFLP approach to study genes differentially expressed during shedding of immature fruits reveals the involvement of a putative auxin hydrogen symporter in apple (Malus domestica L. Borkh). Gene 442:26–36

    Article  PubMed  CAS  Google Scholar 

  • Dalrymple BP, Kirkness EF, Nefedov M et al (2007) Using comparative genomics to reorder the human genome sequence into a virtual sheep genome. Genome Biol 8:R152

    Article  PubMed  CAS  Google Scholar 

  • Davey MW, Keulemans J (2004) Determining the potential to breed for enhanced antioxidant status in Malus: mean inter- and intravarietal fruit vitamin C and glutathione content at harvest and their evolution during storage. J Agri Food Chem 52:8031–8038

    Article  CAS  Google Scholar 

  • Degenhardt J, Al-Masri AN, Kurkcuoglu S, Szankowski I, Gau AE (2005) Characterisation by suppression subtractive hybridization of transcripts that are differentially expressed in leaves of apple scab-resistant and susceptible cultivars of Malus domestica. Mol Genet Genom 273:326–335

    Article  CAS  Google Scholar 

  • Demura T, Fukuda H (2007) Transcriptional regulation in wood formation. Trends Plant Sci 12:64–70

    Article  PubMed  CAS  Google Scholar 

  • Dirlewanger E, Graziano E, Joobeur T, Garriga-Caldere F, Cosson P, Howad W, Arus P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA 101(26):9891–989

    Article  PubMed  CAS  Google Scholar 

  • Dondini L, Lain O, Geuna F, Banfi R, Gaiotti F, Tartarini S, Bassi D, Testolin R (2007) Development of a new SSR-based linkage map in apricot and analysis of synteny with existing Prunus maps. Tree Genet Genomes 3:239–249

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Durel CE, Van de Weg WE, Venisse JS, Parisi L (1999) Localisation of a major gene for apple scab resistance on the European genetic map of the Prima × Fiesta cross. 5th Workshop on Integrated Control of Pome Fruit Diseases, 24–27 August 1999, Fontevraud l'Abbaye, France. IOBC Bull 23: 245–248.

  • Escarpa A, Gonzalez MC (1998) High-performance liquid chromatography with diode-array detection for the determination of phenolic compounds in peel and pulp from different apple varieties. J Chromotog 823:331–337

    Article  CAS  Google Scholar 

  • Evans RC, Campbell CS (2002) The origin of the apple subfamily (Maloideae; Rosaceae) is clarified by DNA sequence data from duplicated GBSSI genes. Am J Bot 89(9):1478–1484

    Article  PubMed  CAS  Google Scholar 

  • Eveland AL, McCarty DR, Koch KE (2008) Transcript profiling by 3'-untranslated region sequencing resolves expression of gene families. Plant Physiol 146:32–44

    Article  PubMed  CAS  Google Scholar 

  • Freeman JL, Perry GH, Feuk L, Redon R, McCarroll SA, Altshuler DM, Aburatani H, Jones KW, Tyler-Smith C, Hurles ME, Carter NP, Scherer SW, Lee C (2006) Copy number variation: new insights in genome diversity. Genome Res 16:949–961

    Article  PubMed  CAS  Google Scholar 

  • Fuleki T, Pelayo E, Palabay RB (1994) Sugar composition of varietal juices produced from fresh and stored apples. J Agri Food Chem 42:1266–1275

    Article  CAS  Google Scholar 

  • Gardiner SE, Bus VGM, Rushholme RL, Chagné D, Rikkerink E (2007) Apple. In: Kole C (ed) Genome mapping and molecular breeding in plants, vol 4. Springer, Berlin, Heidelberg, Gemany pp 1–62

  • Garkava-Gustavsson L, Brantestam AK, Sehic J, Nybom H (2008) Molecular characterisation of indigenous Swedish apple cultivars based on SSR and S-allele analysis. Hereditas 145:99–112

    Article  PubMed  CAS  Google Scholar 

  • Gasic K, Gonzalez DO, Thimmapuram J, Liu L, Malnoy M, Gong G, Han YP, Vodkin LO, Aldwinckle HS, Carroll NJ, Orvis KS, Goldsbrough P, Clifton S, Pape D, Fulton L, Martin J, Theising B, Wisniewski ME, Fazio G, Feltus FA, Korban SS (2009) Comparative analysis and functional annotation of a large expressed sequence tag collection of apple. Plant Genome 2(1):23–38

    Article  CAS  Google Scholar 

  • Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155:463–473

    PubMed  CAS  Google Scholar 

  • Guarino C, Arena S, De Simone L, D’Ambrosio C, Santoro S, Rocco M, Scaloni A, Marra M (2007) Proteomic analysis of the major soluble components in Annurca apple flesh. Mol Nutr Food Res 51:2550262

    Article  CAS  Google Scholar 

  • Guyot S, Marnet N, Sanoner P, Drilleau J-F (2003) Variability of the polyphenolic composition of cider apple (Malus domestica) fruit and juices. J Agri Food Chem 51:6240–6247

    Article  CAS  Google Scholar 

  • Han Y, Gasic K, Marron B, Beever JE, Korban SS (2007) A BAC-based physical map of the apple genome. Genomics 89:630–637

    Article  PubMed  CAS  Google Scholar 

  • Hanada K, Takakashi K, Myouga F, Toyada T, Li W-H, Shinozaki K (2009) Evolutionary Persistence of functional compensation by duplicate genes in Arabidopsis. Genome Biol Evol 1:409–414

    Article  PubMed  CAS  Google Scholar 

  • Harris SA, Robinson JP, Juniper BE (2002) Genetic clues to the origin of the apple. Trends Genet 18:426–430

    Article  PubMed  CAS  Google Scholar 

  • Hokanson SC, Szewc-McFadden AK, Lamboy WF, McFerson JR (1998) Microsatellite (SSR) markers reveal genetic identities, genetic diversity and relationships in a Malus × domestica Borkh. core subset collection. Theor Appl Genet 97:671–683

    Article  CAS  Google Scholar 

  • Holland JB (2007) Genetic architecture of complex traits in plants. Curr Opin Plant Biol 10:156–161

    Article  PubMed  CAS  Google Scholar 

  • Huang X, Feng Q, Qian Q, Zhao Q, Wang L, Wang A, Guan J, Fan D, Weng Q, Huang T, Dong G, Sang T, Han B (2009) High-throughput genotyping by whole-genome resequencing. Genome Res 19:1068–1076

    Article  PubMed  CAS  Google Scholar 

  • Hummer KE, Janick J (2009) Rosaceae: taxonomy, economic importance, genomics. In: Folta K, Gardiner S (eds) Genetics and genomics of Rosaceae. Springer, New York, pp 1–17

    Chapter  Google Scholar 

  • Iafrate AJ, Feuk L, Rivera MN, Listewnik ML, Donahoe PK, Qi Y, Scherer SW, Lee C (2004) Detection of large-scale variation in the human genome. Nat Genet 36:949–951

    Article  PubMed  CAS  Google Scholar 

  • Illa E, Sargent DJ, Lopez Girona E, Bushakra J, Cestaro A, Crowhurst R, Pindo M, Cabrera A, van der Knaap E, Iezzoni A, Gardiner S, Velasco R, Arús P, Chagné D, Troggio M (2011) Comparative analysis of rosaceous genomes and the reconstruction of a putative ancestral genome for the family. BMC Evol Biol 11:9. doi:101186/1471-2148-11-9

    Article  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Noel B et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–U465

    Article  PubMed  CAS  Google Scholar 

  • Janick J, Cummins JV, Brown SK, Hemmat M (1996) Apples. In: Janick J, Moore JN (eds) Fruit breeding, vol I—tree and tropical fruits. Wiley, New York, pp 1–66

    Google Scholar 

  • Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, Boweb JH, Crowhurst RN, Gleave AP, Ledger S, McArtney S, Pichler FB, Snowden KC, Ward S (2008) Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol 8:16

    Article  PubMed  CAS  Google Scholar 

  • Jensen PJ, Rytter J, Detwiler EA, Travis JW, McNellis TW (2003) Rootstock effects on gene expression patterns in apple tree scions. Plant Mol Biol 493:493–511

    Article  Google Scholar 

  • Jensen PJ, Makalowska I, Altman N, Fazio G, Praul C, Maximova SN, Crassweller RM, Travis JW, McNellis TW (2010) Rootstock-regulated gene expression patterns in apple scions. Tree Genet Genomes 6:57–72

    Article  Google Scholar 

  • Kenis K, Keulemans J, Davey MW (2008) Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genomes 4:647–661

    Article  Google Scholar 

  • Khan MA, Durel CE, Duffy B, Drouet D, Kellerhals M, Gessler C, Patocchi A (2007) Development of molecular markers linked to the ‘Fiesta’ linkage group 7 major QTL for fire blight resistance and their application for marker-assisted selection. Genome 50:568–577

    Article  PubMed  CAS  Google Scholar 

  • King GJ, Maliepaard C, Lynn JR, Alston FH, Durel CE, Evans KM, Griffon B, Laurens F, Manganaris AG, Chrevens T, Tartarini S, Verhaegh J (2000) Quantitative genetic analysis and comparison of physical and sensory descriptors relating to fruit flesh firmness in apple (Malus pumila Mill.). Theor Appl Genet 100:1074–1084

    Article  Google Scholar 

  • King GJ, Lynn JR, Dover CJ, Evans KM, Seymour GB (2001) Resolution of quantitative trait loci for mechanical measures accounting for genetic variation in fruit texture of apple (Malus pumila Mill.). Theor Appl Genet 102:1227–1235

    Article  CAS  Google Scholar 

  • Knee M, Hatfield SGS (1981) The metabolism of alcohols by apple fruit tissue. J Sci Food Agri 32:593–600

    Article  CAS  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 R, Weskett R (2011) Genetic architecture of fruit quality traits in Malus x domestica (Borkh.) compared between own-rooted seedlings and vegetative propagules on ‘M. 9’ rootstock. Tree Genet Genomes 7:1079–1088. doi:10.1007/s11295-011-0396-0

  • Kumar S, Chagné D, Bink MCAM, Volz RK, Whitworth C, Carlisle C (2012) Genomic selection for fruit quality traits in apple (Malus × domestica Borkh.) PLoS ONE 7: e36674. doi:10.1371/journal.pone.0036674

  • Kurkcuoglu S, Piotrowski M, Gau AE (2004) Up-regulation of pathogenesis-related proteins in the apoplast of Malus domestica after application of a non-pathogenic bacterium. J Biosci 59(843–848):7

    Google Scholar 

  • Lee Y-P, Yu G-H, Seo YS, Han SE, Choi Y-O, Kim D, Mok I-G, Kim WT, Sung S-K (2007) Microarray analysis of apple gene expression engaged in early fruit development. Plant Cell Rep 26:917–926

    Article  PubMed  CAS  Google Scholar 

  • Lespinasse Y, Bouvier L, Djulbic M, Chevreau E (1999) Haploidy in apple and pear. Acta Hort 484:49–54

    Google Scholar 

  • Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C (2003) Mapping quantitative physiological traits in apple (Malus × domestica Borkh.). Plant Mol Biol 52:511–526

    Article  PubMed  CAS  Google Scholar 

  • Liew M, Pryor R, Palais R, Meadows C, Erali M, Lyon E, Wittwer C (2004) Genotyping of single-nucleotide polymorphisms by high-resolution melting of small amplicons. Clin Chem 50:1156–1164

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386–3399

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  PubMed  CAS  Google Scholar 

  • Meuwissen THE, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829

    PubMed  CAS  Google Scholar 

  • Micheletti D, Troggio M, Baldi P, Costa F, Pindo M, Komjanc M, Malnoy M, Zharkikh A, Magnago P, Velasco R, Salvi S (2010) LD estimation and analysis of diversity in apple. In: Proceedings of Plant & Animal Genomes XVIII Conference, San Diego, CA, USA W255.

  • Myles S, Chia JM, Hurwitz B, Simon C, Zhong GY, Buckler E, Ware D (2010) Rapid genomic characterization of the genus Vitis. PLoS One 5(1):e8219

    Article  PubMed  CAS  Google Scholar 

  • Newcomb RD, Crowhurst RN, Gleave AP, Rikkerink EHA, Allan AC, Beuning LL, Bowen JH, Gera E, Jamieson KR, Janssen BJ, Laing WA, McArtney S, Nain B, Ross GS, Snowden KC, Souleyre EJF, Walton EF, Yauk Y-K (2006) Analyses of expressed sequence tags from apple. Plant Physiol 141:147–166

    Article  PubMed  Google Scholar 

  • Noiton DAM, Alspach PA (1996) Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J Am Soc Hort Sci 121:773–782

    Google Scholar 

  • Norelli JL, Farrell RE Jr, Basset CL, Baldo AM, Lalli DA, Aldwinckle HS, Wisniewski ME (2009) Rapid transcriptional response of apple to fire blight disease revealed by cDNA suppression subtractive hybridisation analysis. Tree Genet Genomes 5:27–40

    Article  Google Scholar 

  • Olmstead JW, Sebolt AM, Cabrera A, Sooriyapathirana SS, Hammar S, Iriarte G, Wang D, Chen CY, van der Knaap E, Iezzoni AF (2008) Construction of an intra-specific sweet cherry (Prunus avium L.) genetic linkage map and synteny analysis with the Prunus reference map. Tree Genet Genom 4:897–910

    Article  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  PubMed  CAS  Google Scholar 

  • Paris R, Dondini L, Tartarini S, Bastia D, Mantovani V, Sansavini S (2009a) An optimized cDNA-AFLP protocol for the identification of TDFs Involved in the Malus-Venturia inaequalis interaction. Acta Hort 814:841–844

    CAS  Google Scholar 

  • Paris R, Dondini L, Tartarini S, Sansavini S (2009b) First evidence of d-HPLC efficiency for and automated cDNA-AFLP in the apple scab resistance model. Acta Hort 839:457–462

    CAS  Google Scholar 

  • Park S, Sugimoto N, Larson MD, Beaudry R, van Nocker S (2006) Identification of genes with potential roles in apple fruit development and biochemistry through large-scale statistical analysis of expressed sequence tags. Plant Physiol 141:811–824

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556

    Article  PubMed  CAS  Google Scholar 

  • Patocchi A, Frei A, Frey JE, Kellerhals M (2009) Towards improvement of marker assisted selection of apple scab resistant cultivars: Venturia inaequalis virulence surveys and standardization of molecular marker alleles associated with resistance genes. Mol Breed 24:337–347

    Article  CAS  Google Scholar 

  • Pichler FB, Walton EF, Davey M, Triggs C, Janssen B, Wunsche JN, Putterill J, Schaffer RJ (2007) Relative developmental, environmental and tree-to-tree variability in buds from fieldgrown apple trees. Tree Genet Genomes 3:329–339

    Article  Google Scholar 

  • Proost S, Van Bel M, Sterck L, Billiau K, Van Parys T, Van de Peer Y, Vandepoele K (2009) PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell 21(12):3718–31

    Article  PubMed  CAS  Google Scholar 

  • Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13:174–180

    Article  PubMed  CAS  Google Scholar 

  • Rowan DD, Allen JM, Fielder S, Hunt MB (1999) Biosynthesis of straightchain ester volatiles in red delicious and granny smith apples using deuterium-labelled precursors. J Agric Food Chem 47:2553–2562

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rudell DR, Mattheis JP (2009) Superficial scald development and related metabolism is modified by postharvest light irradiation. Postharvest Biol Technol 51:174–182

    Article  CAS  Google Scholar 

  • Rudell DR, Mattheis JP, Curry EA (2008) Prestorage ultraviolet-white light irradiation alters apple peel metabolome. J Agri Food Chem 56:1138–1147

    Article  CAS  Google Scholar 

  • Ruiz R, Garca-Luis A, Monerri C, Guardiola JL (2001) Carbohydrate availability in relation to fruitlet abscission in citrus. Ann Bot 87:805–812

    Article  CAS  Google Scholar 

  • Sargent DJ, Rys A, Nier S, Simpson DW, Tobutt KR (2007) The development and mapping of functional markers in Fragaria and their transferability and potential for mapping in other genera. Theor Appl Genet 114:373–384

    Article  PubMed  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 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  CAS  Google Scholar 

  • Schaffer SM, Krishnan V, Kalyanaraman A, Dhingra (2010) A comparative transcriptomics in apple using quantitative 3' untranslated region (UTR) pyrosequencing. In: Proceedings of the Plant & Animal Genome Conference XVIII, San Diego, CA USA P087

  • Schmutz J, Cannon SB, Schlueter J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  PubMed  CAS  Google Scholar 

  • Sebat J, Lakshmi B, Troge J, Alexander J, Young J, Lundin P, Maner S, Massa H, Walker M, Chi MY, Navin N, Lucito R, Healy J, Hicks J, Ye K, Reiner A, Gilliam TC, Trask B, Patterson N, Zetterberg A, Wigler M (2004) Large-scale copy number polymorphism in the human genome. Science 305:525–528

    Article  PubMed  CAS  Google Scholar 

  • Sebat J, Lakshmi B, Malhotra D, Troge J, Lese-Martin C, Walsh T, Yamrom B, Yoon S, Krasnitz A, Kendall J, Leotta A, Pai D, Zhang R, Lee YH, Hicks J, Spence SJ, Lee AT, Puura K, Lehtimaki T, Ledbetter D, Gregersen PK, Bregman J, Sutcliffe JS, Jobanputra V, Chung W, Warburton D, King MC, Skuse D, Geschwind DH, Gilliam TC, Ye K, Wigler M (2007) Strong association of de novo copy number mutations with autism. Science 316:445–449

    Article  PubMed  CAS  Google Scholar 

  • Stoeckli S, Mody K, Patocchi A, Kellerhals M, Dorn S (2009) Rust mite resistance in apple assessed by quantitative trait loci analysis. Tree Genet Genomes 5:257–267

    Article  Google Scholar 

  • Tang HB, Wang XY, Bowers JE, Ming R, Alam M, Paterson AH (2008) Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 18(12):1944–1954

    Article  PubMed  CAS  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP, de-Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Roder MS, Wing RA, Wu W, Young ND (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    PubMed  CAS  Google Scholar 

  • Taylor JE, Whitelaw CA (2001) Signals in abscission. New Phytol 151:323–339

    Article  CAS  Google Scholar 

  • Tsao R, Yang R, Young JC, Honghui Zhu H (2003) Polyphenolic profiles in eight apple cultivars using high-performance liquid chromatography (HPLC). J Agric Food Chem 51:6347–6353

    Article  PubMed  CAS  Google Scholar 

  • Van de Peer Y, Fawcett JA, Proost S, Sterck L, Vandepoele K (2009) The flowering world: a tale of duplications. Trends Plant Sci 14(12):680–688

    Article  PubMed  CAS  Google Scholar 

  • Vandepoele K, Saeys Y, Simillion C, Raes J, Van de Peer Y (2002) The Automatic Detection of Homologous Regions (ADHoRe) and its application to microcolinearity between Arabidopsis and Rice. Genome Res 12:1792–801

    Article  PubMed  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A et al (2007) High quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2:e1326

    Article  PubMed  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839

    Article  PubMed  CAS  Google Scholar 

  • Veyrieras JB, Goffinet B, Charcosset A (2007) MetaQTL: a package of new computational methods for the meta-analysis of QTL mapping experiments. BMC Bioinformatics 8:49

    Article  PubMed  CAS  Google Scholar 

  • Vilanova S, Sargent DJ, Arús P, Monfort A (2008) Synteny conservation between two distantly-related Rosaceae genomes: Prunus (the stone fruits) and Fragaria (the strawberry). BMC Plant Biol 8:67

    Article  PubMed  CAS  Google Scholar 

  • Volz RK, Rikkerink E, Austin P, Lawrence T, Bus VGM (2009) “Fast Breeding” in apple: a strategy to accelerate introgression of new traits into elite germplasm. Acta Hort 814:163–168

    Google Scholar 

  • Wang W, Tai F, Chen S (2008) Optimizing Protein extraction from plant tissues for enhanced preoteomics analysis. J Sep Sci 31:2032–2039

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Li P, Brutnell TP (2010) Exploring plant transcriptomes using ultra high-throughput sequencing. Briefings Functional Genom 9:118–128

    Article  CAS  Google Scholar 

  • Weigel D, Mott R (2009) The 1001 genomes project for Arabidopsis thaliana. Genome Biol 10(5):107

    Article  PubMed  Google Scholar 

  • Wiedow C, Chagné D, Souleyre E, Rowan D, Hunt M, Lambert C, Cestaro A, Velasco R, Volz R, Gardiner SE (2010) QTL and candidate gene mapping of ‘Ripe Apple’ aroma. In: Proceedings of Plant & Animal Genome XVIII Conference, January 9–13, 2010 San Diego, CA USA P476

  • Wisniewski M, Bassett C, Macarisin D, Norelli J, Artlip T (2009) Transcriptomic and proteomic response of fruit trees to abiotic stress. Acta Hort 839:681–688

    CAS  Google Scholar 

  • Wolfe J, Wehr WJA (1988) Rosaceous Chamaebatiaria-like foliage from the Paleogene of western North America. Aliso 12:177–200

    Google Scholar 

  • Youens-Clark K, Faga B, Stein L, Ware D (2009) CMap 1.01: a comparative mapping application for the Internet. Bioinformatics 25(22):3040–3042

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Holland JB, McMullen MD, Buckler ES (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178:539–551

    Article  PubMed  Google Scholar 

  • Zhang H, Cha S, Yeung ES (2007) Colloidal graphite-assisted laser desorption/ionization MS and MSn of small molecules. 2. Direct profiling and MS imaging of small metabolites from fruit. Anal Chem 79:6575–6584

    Article  PubMed  CAS  Google Scholar 

  • Zharkikh A, Troggio M, Pruss D, Cestaro A, Eldrdge G, Pindo M, Mitchell JT, Vezzulli S, Bhatnagar S, Fontana P, Viola R, Gutin A, Salamini F, Skolnick M, Velasco R (2008) Sequencing and assembly of highly heterozygous genome of Vitis vinifera L. cv Pinot Noir: Problems and solutions. J Biotechnol 136(1–2):38–43

    Article  PubMed  CAS  Google Scholar 

  • Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge partial funding for PFR authors by the New Zealand Foundation for Research, Science and Technology, contract nos. CO6X0810 and C06X0812 and SNP mapping by Heather Bassett. Apple genome research and comparative genomics at FEM are supported by the research office of the Provincia autonoma di Trento.

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Correspondence to S. E. Gardiner.

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Communicated by A. Abbott

A contribution to the Special Issue “The genomes of the giants: a walk through the forest of tree genomes”

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Troggio, M., Gleave, A., Salvi, S. et al. Apple, from genome to breeding. Tree Genetics & Genomes 8, 509–529 (2012). https://doi.org/10.1007/s11295-012-0492-9

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  • DOI: https://doi.org/10.1007/s11295-012-0492-9

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