The history of mapping the apple genome

Open access


This review summarises the research projects that have been conducted with the goal of mapping the apple (Malus × domestica) genome. The generation of apple linkage and physical maps, which was started at the end of the 20th century by many scientific teams, has resulted in rich data useful for further fundamental and applied studies. The mapping efforts mainly contained the choice of mapping populations as well as the choice of types and number of markers. Over the years, scientists have achieved major successes and faced major obstacles. Many economically important traits have been mapped in the apple genome, which has a total length of 2000 cM. The recently published integrated genetic and physical maps summarise the data and will be helpful to modern breeding programs, with a special focus on resistance to various diseases, as well as on fruit quality and other desired apple traits.

Alston F.H., Phillips K.L., Evans K.M., 2000. A Malus gene list. Acta Hort. 538: 561-570.

Andersen J.R., Lübberstedt T., 2003. Functional markers in plants. Trends Plant Sci. 8(11): 554-560.

Antanaviciute L., Fernandez-Fernandes F., Jansen J., Banchi E., Evans K.M., Viola R., et al., 2012.

Development of a dense SNP-based linkage map of apple rootstock progeny using the Malus infinium whole genome genotyping array. Genomics 13: 203.

Boudichevskaia A., Flachowsky H., Peil A., Fischer C., Dunemann F., 2006. Development of a multiallelic SCAR marker for the scab resistance gene Vr1/Vh4/ Vx from R12740-7A apple and its utility for molecular breeding. Tree Genet. Genomes 2: 186-195.

Bus V.G.M., Rikkerink E.H.A., Van De Weg W.E., Rusholme R.L., Gardiner S.E., Bassett H.C.M., et al., 2005. The Vh2 and Vh4 scab resistance genes in two differential hosts derived from Russian apple R12740-7A map to the same linkage group of apple. Mol. Breed. 15: 103-116.

Bus V.G.M., Chagne D., Bassett H.C.M., Bowatte D., Calenge F., Celton M.J., et al., 2007. Genome mapping of three major resistance genes to woolly apple aphid (Eriosoma lanigerum Hausm.). Tree Genet. Genomes 4: 233-236.

Calenge F., Faure A., Goerre M., Gebhardt C., Van De Weg W.E., Parisi L., et al., 2004. Quantitative Trait Loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathol. 94(4): 370-379.

Calenge F., Drouet D., Denance C., Van De Weg W.E., Brisset M.N., Paulin J.P., et al., 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.

Calenge F., Durel C.E., 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.

Cevik V., King G.J., 2002. Resolving the aphid resistance locus Sd1 on BAC contig within a sub-telomeric region of Malus linkage group 7. Genome 45: 939-945.

Cevik V., Ryder C.D., Popovich A., Manning K., King G., Seymour G.B., 2010. A fruitfull-like genes is associated with genetic variation for fruit flesh firmness in apple (Malus x domestica Borkh.). Tree Genet. Genomes 6: 271-279.

Chagne D., Carlisle C.M., Blond C., Volz K.R., Whitworth C.J., Oraguzie N.C., et al., 2007. Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8(212): 1-12.

Cheng F.S., Weeden N.F., Brown S.K., Aldwinckle H.S., Gardiner S.E., Bus V.G., 1998. Development of a DNA marker for Vm, a gene conferring resistance to apple scab. Genome 41: 208-214.

Conner P.J., Brown S.K., Weeden N.F., 1997. Randomly amplified polymorphic DNA-based genetic linkage maps of three apple cultivars. J. Am. Soc. Hortic. Sci. 122: 350-359.

Costa F., Stella S., Van De Weg E.W., Guerra W., Cecchinel M., Dallavia J., et al., 2005. Role of the genes Md-ACO1 and Md-ACS1 in ethylene production and shelf life of apple (Malus x domestica Borkh.). Euphytica 141: 181-190.

Costa F., Van De Weg E.W., Stella S., Dondini L., Pratesi D., Musacch S., et al., 2008. Map position and functional allelic diversity of Md-Exp7, a new putative expansin gene associated with fruit softening in apple (Malus x domestica Borkh.) and pear (Pyrus communis). Trees Genet. Genomes 4: 575-586.

Costa F., Peace C.P., Stella S., Serra S., Musacchi S., Bazzani M., et al., 2010. QTL dynamics for fruit firmness and softening around an ethylene-dependent poligalactouronase gene in apple (Malus x domestica Borkh.). J. Exp. Bot. 61(11): 3029-3039.

Davey M.W., Kenis K., Keulemans J., 2006. Genetic control of fruit Vitamin C contents. Plant Physiol. 142: 343-351.

Dapena E., Minarro M., Blazquez M.D., 2009. Evaluation on the resistance to the rosy apple aphid using a genetic markers. Acta Hort. 814: 787-790.

Dunemann F., Egerer J., 2010. A major resistance gene from Russian apple ‘Antonovka’ conferring field immunity against apple scab is closely linked to the Vf locus. Tree Genet. Genomes 6(5): 627-633.

Dunemann F., Peil A., Urbanietz A., Garcia-Libreros T., 2007. Mapping of the apple powdery mildew resistance gene PL1 and its genetic association with an NBS-LRR candidate resistance gene. Plant Breed. 126: 476-481.

Durel C.E., Van De Weg E., Venisse J.S., Parisi L., 2000. Localization of a major gene for apple scab resistance on the European genetic map of the ‘Prima’ x ‘Fiesta’ cross. Integrated Control of Pome Fruit Diseases IOBC/WPRS Bull. 23(12): 245-248.

Durel C.E., Parisi L., Laurens F., Van De Weg E., Liebha rd R., Koller B., et al., 2003. Genetic dissection of partial resistance against two monoconidial strains of the new race 6 of Venturia inaequalis in apple. Genome 46: 224-234.

Durell C.E., Denance C., Brisset M.N., 2009. Two distinct major QTL for resistance to fire blight colocalize on linkage group 12 in apple genotypes ‘Evereste’ and Malus floribunda clone 821. Genome 52(2): 139-147.

Evans R.C., Campbell C.S., 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.

Evans K.M., James C.M., 2003. Identification of SCAR markers linked to PL-w mildew resistance in apple. Theor. Appl. Genet. 106: 1178-1183.

Erdin E., Tartarini S., Brogg ini G.A.L., Gennari F., Sansavini S., Gessler C., et al., 2006. Mapping of apple scab resistance gene Vb. Genome 49: 1238-1245.

Fernandez-Fernandez F., Evans K.M., Clarke J.B., Govan C.L., James C.M., Marić S., et al., 2008. Development of an STS map of an interspecific progeny of Malus. Tree Genet. Genomes 4: 469 -479.

Gardiner S.E., Murdoch J., Meech S., Rusholme R., Besset H., Cook M., 2003. Candidate resistance genes from an EST database prove a rich source of markers for major genes conferring resistance to important apple pest and diseases. Acta Hort. 622: 141-151.

Gianfranceschi L., Seglias N., Tachini R., Komjanc M., Gessler C., 1998. Simple sequence repeats for the genetic analysis of apple. Theor. Appl. Genet. 96: 1069-1076.

Gessler C., Patocchi A., Sansavini S., Tartarini S., Gianfranceschi L., 2006. Venturia inaequalis resistance in apple. Crit. Rev. Plant Sci. 25: 473-503.

Gygax M., Gianfranceschi L., Liebhard R., Kellerhaus M., Gessler C., Patocchi A., 2004. Molecular markers linked to the apple scab resistance gene Vbj derived from Malus baccata jackii. Theor. Appl. Genet. 109: 1702-1709.

Han S.E., Seo Y.S., Kim D., Sung S.K., Kim W.T., 2007. Expression of MdCAS1 and MdCAS2, encoding apple β-cyanoalanine synthase homologs, is concomitantly induced during ripening and implicates MdCASs in the possible role of the cyanide detoxification in Fuji apple (Malus x domestica Borkh.) fruits. Plant Cell Repository 26: 1321-1331.

Han Y., Korban S.S., 2008. An overview of the apple genome through BAC end sequence analysis. Plant Mol. Biol. 67: 581-588.

Han Y., Chagne D., Gasic K., Rikkerink E.H.A., Beever J.E., Gardiner S.E., et al., 2009. BAC-end sequencebased SNPs and bin mapping for rapid integration of physical and genetic maps in apple. Genomics 93: 282-288.

Han Y., Zheng D., Vimolmangkang S., Khan M.A., Beever J.E., Korban S.S., 2011. Integration of physical and genetic maps in apple confirms wholegenome and segmental duplications in the apple genome. J. Exp. Bot. 10: 1-14.

Harada T., Sunako T., Wakasa Y., Soejima J., Satoh T., Niizeki M., 2000. An allele of the 1-aminocyclopropane-1-carboxylate synthase gene (Md-CAS1) accounts for the low level of ethylene production in climacteric fruits of some apple cultivars. Theor. Appl. Genet. 101: 742-746.

Hemmat M., Weeden N.F., Manganaris A.G., Lawson D.M., 1994. Molecular marker linkage map for apple. J. Hered. 85: 4-11.

Hemmat M., Brown S.K., Aldwinckle H.S., 2003. Identification and mapping of markers for resistance to apple scab from ‘Antonovka’ and ‘Hansen’s baccata #2’. Acta Hort. 622: 153-161.

Hokanson S.C., Szewc-Mcfa dden A.K., Lamboy W.F., Mcferson J.R., 1998. Microsatellite (SSR) markers reveal genetic identities, genetic diversity and relationships in a Malus x domestica Borkh. core subset collection. Theor. Appl. Genet. 97: 671-683.

Huaracha E., Xu M., Korban S.S., 2004. Narrowing down the region of the Vf locus for scab resistance in apple using AFLP-derived SCARs. Theor. Appl. Genet. 108: 274-279.

Hummer K.E., Janick J., 2008. Rosaceae: Taxonomy, Economic Importance, Genomics. In: Genetic and Genomics of Rosaceae. Plant Genetics / Genomics. K.M. Folta and S.E. Gardiner (eds), Springer Science, Business Media: 1-18.

Igarashi M., Abe Y., Hatsuyama Y., Ueda T., Fukasawa- Akada T., Kon T., et al., 2008. Linkage maps of the apple (Malus x domestica Borkh.) cultivars ‘Ralls Janet’ and ‘Delicious’ include newly developed EST markers. Mol. Breed. 22: 95-118.

James C.M., Clarke J.B., Evans K.M., 2004.

Identification of molecular markers linked to the mildew resistance gene Pl-d in apple. Theor. Appl.

Genet. 110: 175-181.

Jha G., Thakur K., Thakur P., 2009 . The Venturia apple pathosystem: Pathogenicity mechanism and plant defense responses. J. Biomed. Biotechnol.: 1-10.

Jung S., Staton M, Lee T., Blenda A., Svancara R., Abbott A., Main D., 2008. GDR (Genome Database for Rosaceae): integrated web-database for Rosaceae genomics and genetics data. Nucleic Acid Res. 36.

Kenis K., Keulemans J., Davey M.W., 2008. Identification and stability of QTLs for fruit quality traits in apple.

Tree Genet. Genomes 4: 647-661.

Kenis K., Keulemans J., 2004. QTL analysis of growth characteristics in apple. Acta Hort. 663: 369-374.

Kenis K., Keulemans J., 2005. Genetic linkage maps of two apple cultivars (Malus x domestica Borkh.) based on AFLP and microsatellite markers. Mol.

Breed. 15: 205-219.

Kell er-Przybyłkowicz S., 2011. Lokalizacja genów związanych jakością owoców na mapie genetycznej odmian jabłoni ‘Retina’ i ‘Topaz’. Ph.D. dissertation, Research Institute of Horticulture, PL.

Khan M.A., Duffy B., Gessler C., Patocchi A., 2006. QTL mapping of fire blight resistance in apple. Mol. Breed. 17: 299-306.

Khan M.A., Durel C.E., Duffy B., Drouet D., Kellerhals M., Gessler C., et al., 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.

Khan M.A., Han Y., Zhao Y.F., Troggio M., Korban S.S., 2012. A multi-population consensus genetic map reveals inconsistent marker order among maps likely attributed to structural variation in the apple genome. PLoS ONE 7(11): 1-12.

King G.J., Maliepaa rd C., Lynn J.R., Alston F.H., Durel C.E., Evans K.M., et al., 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.

Kole C., Abbott A.G., 2008. Fundamentals of plant genome mapping. Principles and practices of plant genomics. Genome mapping. Science Publishers, USA: 2-67.

Lander E.S., Botstein D., 1989. Mapping Mendelian factors underlying Quantitative Traits using RFLP linkage maps. Genetics 121: 185-199.

Le Roux P.M., Khan M.A., Broggini G.A.L., Duffy B., Gessler C., Patocchi A., 2010. Mapping of quantitative trait loci in the apple cultivars ‘Florina’ and ‘Nova Easygro’. Genome 53(9): 710-712.

Liebhard R., Gessler C., 2000. Possible errors in genome mapping. Integrated Control of Pome Fruit Diseases IOBC/WPRS Bull. 23(12): 127-135.

Liebhard R., Gianfranceschi L., Koller B., Ryder C.D., Tarchini R., Van De Weg E., et al., 2002. Development and characterization of 140 new microsatellites in apple (Malus x domestica Borkh.).

Mol. Breed. 10: 217-241.

Liebhard R., Koller B., Gianfranceschi L., Gessler C., 2003a. Creating a saturated reference map for the apple (Malus x domestica Borkh.) genome. Theor. Appl. Genet. 106: 1497-1508.

Liebhard R., Koller B., Patocchi A., Kellerhals M., Pfamma tter W., Jertmini M., et al., 2003b. Mapping quantitative field resistance against apple scab in a ‘Fiesta’ x ‘Discovery’ progeny. Phytopathol. 93(4): 493-501.

Liebhard R., Kellerhals M., Pfamma tter W., Jertmini M., Gessler C., 2003c. Mapping quantitative physiological traits in apple (Malus x domestica Borkh.). Plant Mol. Biol. 52: 511-526.

Ma C.-X., Casella G., Wu R., 2002. Functional Mapping of Quantitative Trait Loci underlying the character process: a theoretical framework. Genetics 161: 1751-1762.

Maliepaard C., Aston F.H., Van Arkel G., Brown L.M., Chevereau E., Dunemann F., et al., 1998. Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor. Appl. Genet. 97: 60-73.

N’diaye A., Van De Weg W.E., Kodde L.P., Koller B., Dunemann F., Thirmann M., et al., 2008. Construction of an integrated consensus map of the apple genome based on four mapping populations. Tree Genet. Genome 4: 727-743.

Patocchi A., Vinatzer B.A., Gianfranceschi L., Tartarini S., Zhang H.B., Sansavini S., et al., 1999 a. Construction of a 550Kb BAC contig spanning the genomic region containing the apple scab resistance gene Vf. Mol. Gen. Genet. 262: 884-891.

Patocchi A., Gianfranceschi L., Gessler C., 1999 b. Towards the map-based cloning of Vf: Fine and physical mapping of the Vf region. Theor. Appl. Genet. 99: 1012-1017.

Patocchi A., Walser M., Tartarini S., Broggini G.A.L., Gennari F., Sansavini S., et al., 2005. Identification by chromosome scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene Vm. Genome 48: 630-636.

Peil A., Garcia-Libreros T., Richter K., Trognitz F.C., Trognitz B., Hanke M.V., et al., 2007 a. Strong evidence for fire blight resistance gene of Malus robusta located on linkage group 3. Plant Breed. 126: 470-475.

Perez-Enciso M., Varona L., 2000. Quantitative trait loci mapping in F2 crosses between outbreed lines. Genetics 155: 391-405.

Roche P., Alston F.H., Maliepaa rd C., Evans K.M., Vrielink R., Dunemann F., et. al. 1997. RFLP and RAPD markers linked to the rosy leaf curling aphid resistance gen (Sd1) in apple. Theor. Appl. Genet. 94: 528-533.

Sanzol J., 2010. Dating and functional characterization of duplicated genes in apple (Malus x domestica Borkh.) by analyzing EST data. BMC Plant Biol. 10(87): 1-22.

Soufflet-Freslon V., Gianfranceschi L., Patocchi A., Durel C.E., 2008. Inheritance studies of apple scab resistance and identification of RVI14, a new major gene that together with other broad-spectrum QTL. Genome 51: 657-667.

Shulaev V., Korban S.S., Sosinski B., Abbot A.G., Aldwinckle H.S., Folta K.M., et al., 2008. Multiple models for Rosaceae Genomics. Plant Physiol. 147: 983-1003.

Silfverberg-Dilworth E., Matasci C.L., Van De Weg W.E., Van Kaauwen M.P.W., Walser M., Kodde L.P., et al., 2006. Microsatellite markers spanning the apple (Malus x domestica Borkh.) genome. Tree Genet. Genomes 2: 202-224.

Soglio V., Costa F., Molthoff J.W., Mieke W., Weemen- Hendriks J., Schouten H.J., et al., 2009. Transcription analysis of apple fruit development using cDNA microarrays. Tree Genet. Genomes 5(4): 685-698.

Soriano J.M., Joshi S.G., Van Kaauwen W., Noordijk Y., Groenwold R., Henken B., et al., 2009. Identification and mapping of the novel apple scab resistance gene Vd3. Tree Genet. Genomes 5: 475-482.

Schouten H.J., Van De Weg W.E., Carling J., Khan A.S., Mckay S.J., Van Kaauwen M.P.W., et al., 2012. Diversity arrays technology (DArT) markers in apple for genetic linkage maps. Mol. Breed. 29: 645-660.

Tartarini S., Gianfranceschi L., Sansavini S., Gessler C., 1999. Development of reliable PCR markers for the selection of the Vf gene conferring scab resistance in apple. Plant Breed. 118: 183-186.

Tartarini S., 2003. Marker-Assisted Selection in Pome fruit breeding. MAS: A fast track to increase genetic gain in plant and animal breeding; Session I: MAS in plants: 23-28.

Tartarini S., Gennari F., Pratesi D., Palazzetti C., Sansavini S., Parisi L., et al., 2004. Characterization and genetic mapping of a major scab resistance gene from the old Italian apple cultivar ‘Durello di Forli’.\ Acta Hort. 663: 129-133.

Van Ooijen J.W., 1999. LOD significance thresholds for QTL analysis in experimental populations of diploid species. Heredity 83: 613-624.

Van Ooijen J.W., Voorrips R.E., 2001. JoinMap 3.0, Software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands.

Velasco R., Zharkikh A., Affourtit J., Dhingra A., Cestaro A., Kalyanaraman A., et al., 2010. The genome of the domesticated apple (Malus x domestica Borkh.). Nature Genet. 42(10): 833-841.

Xu S., Atchley W., 1995. A random model approach to interval mapping of Quantitative Trait Loci. Genetics 141: 1189-1197.

Folia Horticulturae

The Journal of Polish Society for Horticultural Sciences (PSHS)

Journal Information

Web of Science, IMPACT FACTOR 2018: 0,532

CiteScore 2018: 0.6

SCImago Journal Rank (SJR) 2018: 0.198
Source Normalized Impact per Paper (SNIP) 2018: 0.644

Cited By


All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 209 157 11
PDF Downloads 108 95 9