Abstract
Malus sieversii is a progenitor species of domestic apple M. × domestica. Using population “GMAL 4595” of 188 individuals derived from a cross of Royal Gala × PI 613988 (apple scab resistant, M. sieversii), 287 SSR (simple sequence repeats) loci were mapped. Of these SSRs, 80 are published anchors and 207 are newly developed EST (expressed sequence tag) contig-based SSRs, representing 1,630 Malus EST accessions in GenBank. Putative gene functions of these EST contigs are diverse, including regulating plant growth, development and response to environmental stresses. Among the 80 published SSRs, 18 are PI 613988 specific, 38 are common and 24 are Royal Gala specific. Out of the 207 newly developed EST contig-based SSRs, 79 are PI 613988 specific, 45 are common and 83 are Royal Gala specific. These results led to the construction of a M. sieversii map (1,387.0 cM) of 180 SSR markers and a Royal Gala map (1,283.4 cM) of 190 SSR markers. Mapping of scab resistance was independently conducted in two subsets of population “GMAL 4595” that were inoculated with Ventura inaequalis races (1) and (2), respectively. In combination with the two major resistance reactions Chl (chlorotic lesions) and SN (stellate necrosis) to each race, four subsets of resistance data, i.e., Chl/race (1), SN/race (1), Chl/race (2) and SN/race (2), were constituted and analyzed, leading to four resistance loci mapped to the linkage group 2 of PI 613988; SNR1 (stellate necrosis resistance to race (1)) and SNR2 are tightly linked in a region of known scab resistance genes, and ChlR1 (Chlorotic lesion resistance to race (1)) and ChlR2 are also linked tightly but in a region without known scab resistance genes. The utility of the two linkage maps, the new EST contig-based markers and M. sieversii as sources of apple scab resistance are discussed.
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Beckerman J, Chatfield J, Draper E (2009) A 33-year evaluation of resistance and pathogenicity in the apple scab-crabapples pathosystem. Hort Sci 44:599–608
Bus VGM, Laurens FND, van de Weg WE, Rusholme RL, Rikkerink EHA, Gardiner SE, Bassett HCM, Kodde LP, Plummer KM (2005a) The Vh8 locus of a new gene-for-gene interaction between Venturia inaequalis and the wild apple Malus sieversii is closely linked to the Vh2 locus in Malus pumila R12740-7A. New Phytol 166:1035–1049
Bus VGM, Rikkerink EHA, Van de Weg WE, Rusholme RL, Gardiner SE, Bassett HCM, Kodde LP, Parisi L, Laurens FND, Meulenbroek EJ, Plummer KM (2005b) 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, Rikkerink E, Aldwinckle HS, Caffier V, Durel CE, Gardiner S, Gessler C, Groenwold R, Laurens F, Cam BL, Luby J, Meulenbroek B, Kellerhals M, Parisi L, Patocchi A, Plummer K, Schouten HJ, Tartarini S, van de Weg WE (2009) A proposal for the nomenclature of Venturia inaequalis races. Acta Hort 814:739–746
Bus V, Bassett H, Bowatte D, Chagné D, Ranatunga C, Ulluwishewa D, Wiedow C, Gardiner S (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
Celton J-M, Chagné D, Tustin SD, Terakami S, Nishitani C, Yamamoto T, Gardiner SE (2009a) Update on comparative genome mapping between Malus and Pyrus. BMC Res Notes 2:182
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 5:93–107
Chagne 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
Chiu JC, Brenner ED, DeSalle R, Nitabach MN, Holmes TC, Coruzzi GM (2002) Phylogenetic and expression analysis of the glutamate-receptor-like gene family in Arabidopsis thaliana. Mol Biol Evol 19:1066–1082
Conner PJ, Brown SK, Weeden NF (1997) Randomly amplified polymorphic DNA-based genetic linkage maps of three apple cultivars. J Am Soc Hort Sci 122:350–359
Cullings KW (1992) Design and testing of a plant-specific PCR primer for ecological and evolutionary studies. Mol Ecol 1:233–240
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Erdin N, Tartarini S, Broggini GAL, Gennari F, Sansavini S, Gessler C, Patocchi A (2006) Mapping of the apple scab-resistance gene Vb. Genome 49:1238–1245
Fernandez-Fernandez F, Evans KM, Clarke JB, Govan CL, James CM, Maric S, Tobutt KR (2008) Development of an STS map of an interspecific progeny of Malus. Tree Genet Genomes 4:469–479
Forsline PL, Hummer KE (2007) Fruit exploration supported by the National Plant Germplasm System, 1980 to 2004. Hort Sci 42:200–202
Forsline PL, Aldwinckle HS, Dickson EE, Luby JJ, Hokanson SC (2003) Collection, maintenance, characterization and utilization of wild apples of Central Asia. In: Janick J (ed) Horticultural reviews. Wiley, New York, pp 1–61
Galli P, Broggini G, Kellerhals M, Gessler C, Patocchi A (2010a) High-resolution genetic map of the Rvi15 (Vr2) apple scab resistance locus. Mol Breed 26:561–572
Galli P, Patocchi A, Broggini GAL, Gessler C (2010b) The Rvi15 (Vr2) apple scab resistance locus contains three TIR-NBS-LRR genes. Mol Plant Microbe Interact 23:608–617
Gasic K, Gonzalez DO, Thimmapuram J, Liu L, Malnoy M, Gong G, Han Y, 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 (2009a) Comparative analysis and functional annotation of a large expressed sequence tag collection of apple. Plant Genome 2:23–38
Gasic K, Han YP, Kertbundit S, Shulaev V, Iezzoni AF, Stover EW, Bell RL, Wisniewski ME, Korban SS (2009b) Characteristics and transferability of new apple EST-derived SSRs to other Rosaceae species. Mol Breed 23:397–411
Gessler C, Patocchi A, Sansavini S, Tartarini S, Gianfranceschi L (2006) Venturia inaequalis resistance in apple. Crit Rev Plant Sci 25:473–503
Gharghani A, Zamani Z, Talaie A, Oraguzie NC, Fatahi R, Hajnajari H, Wiedow C, Gardiner SE (2009) Genetic identity and relationships of Iranian apple (Malus × domestica Borkh.) cultivars and landraces, wild Malus species and representative old apple cultivars based on simple sequence repeat (SSR) marker analysis. Genet Resour Crop Evol 56:829–842
Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137
Guerin F, Le Cam B (2004) Breakdown of the scab resistance gene Vf in apple leads to a founder effect in populations of the fungal pathogen Venturia inaequalis. Phytopathology 94:364–369
Gygax M, Gianfranceschi L, Liebhard R, Kellerhals 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 YP, Chagne D, Gasic K, Rikkerink EHA, Beever JE, Gardiner SE, Korban SS (2009) BAC-end sequence-based SNPs and Bin mapping for rapid integration of physical and genetic maps in apple. Genomics 93:282–288
Harris SA, Robinson JP, Juniper BE (2002) Genetic clues to the origin of the apple. Trends Genet 18:426–430
Hemmat M, Weeden NF, Manganaris AG, Lawson DM (1994) Molecular marker linkage map for apple. J Hered 85:4–11
Igarashi M, Abe Y, Hatsuyama Y, Ueda T, Fukasawa-Akada T, Kon T, Kudo T, Sato T, Suzuki M (2008) Linkage maps of the apple (Malus × domestica Borkh.) cvs ‘Ralls Janet’ and ‘Delicious’ include newly developed EST markers. Mol Breed 22:95–118
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 Acids Res 36:D1034–D1040
Juniper BE (2007) The mysterious origin of the sweet apple—on its way to a grocery counter near you, this delicious fruit traversed continents and mastered coevolution. Am Sci 95:44–51
Juniper BE, Watkins R, Harris SA (1999) The origin of the apple. Acta Hort 484:27–33
Kim SA, Kwak JM, Jae SK, Wang MH, Nam HG (2001) Overexpression of the AtGluR2 gene encoding an arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants. Plant Cell Physiol 42:74–84
Korban SS, Wannarat W, Rayburn CM, Tatum TC, Rayburn AL (2009) Genome size and nucleotypic variation in Malus germplasm. Genome 52:148–155
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Lalli D, Wisniewski M, Norelli JL, Malnoy M, Pindo M, Fazio G, Forsline P, Aldwinckle H, Gardiner S, Chagné D (2010) Mapping Malus sieversii: a valuable genetic resource for apple breeding. Plant & Animal Genomes XVIII Conference, San Diego, CA, p 206
Li J, Zhu SH, Song XW, Shen Y, Chen HM, Yu J, Yi KK, Liu YF, Karplus VJ, Wu P, Deng XW (2006) A rice glutamate receptor-like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 18:340–349
Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van de Weg E, Gessler C (2002) Development and characterisation of 140 new microsatellites in apple (Malus × domestica Borkh.). Mol Breed 10:217–241
Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003) Creating a saturated reference map for the apple (Malus × domestica Borkh.) genome. Theor Appl Genet 106:1497–1508
Luby J, Forsline P, Aldwinckle H, Bus V, Geibel M (2001) Silk road apples—collection, evaluation, and utilization of Malus sieversii from Central Asia. Hort Sci 36:225–231
Luby J, Hokanson K, Forsline P, Aldwinckle H, Gustafson H, Gardiner S, Bone R, Cook M, Bus V (2006) Evaluation of horticulturally elite Malus sieversii germplasm for apple scab resistance genes using phenotypic and marker-based screening. In: The 3rd international Rosaceae genomics conference, Napier
Maliepaard C, Alston FH, van Arkel G, Brown LM, Chevreau E, Dunemann F, Evans KM, Gardiner S, Guilford P, van Heusden AW, Janse J, Laurens F, Lynn JR, Manganaris AG, den Nijs APM, Periam N, Rikkerink E, Roche P, Ryder C, Sansavini S, Schmidt H, Tartarini S, Verhaegh JJ, Vrielink-van Ginkel M, King GJ (1998) Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet 97:60–73
Malnoy M, Xu M, Borejsza-Wysocka E, Korban SS, Aldwinckle HS (2008) Two receptor-like genes, Vfa1 and Vfa2, confer resistance to the fungal pathogen Venturia inaequalis inciting apple scab disease. Mol Plant Microbe Interact 21:448–458
N’Diaye A, de Weg WEV, Kodde LP, Koller B, Dunemann F, Thiermann M, Tartarini S, Gennari F, Durel CE (2008) Construction of an integrated consensus map of the apple genome based on four mapping populations. Tree Genet Genomes 4:727–743
Naik S, Hampson C, Gasic K, Bakkeren G, Korban SS (2006) Development and linkage mapping of E-STS and RGA markers for functional gene homologues in apple. Genome 49:959–968
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 YK (2006) Analyses of expressed sequence tags from apple. Plant Physiol 141:147–166
Patocchi A, Bigler B, Koller B, Kellerhals M, Gessler C (2004) Vr(2): a new apple scab resistance gene. Theor Appl Genet 109:1087–1092
Patocchi A, Walser M, Tartarini S, Broggini GAL, Gennari F, Sansavini S, Gessler C (2005) Identification by genome scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene Vm. Genome 48:630–636
Patocchi A, Fernández-Fernández F, Evans K, Gobbin D, Rezzonico F, Boudichevskaia A, Dunemann F, Stankiewicz-Kosyl M, Mathis-Jeanneteau F, Durel C, Gianfranceschi L, Costa F, Toller C, Cova V, Mott D, Komjanc M, Barbaro E, Kodde L, Rikkerink E, Gessler C, van de Weg W (2009a) Development and test of 21 multiplex PCRs composed of SSRs spanning most of the apple genome. Tree Genet Genomes 5:211–223
Patocchi A, Frei A, Frey JE, Kellerhals M (2009b) 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
Pilcher RLR, Celton JM, Gardiner SE, Tustin DS (2008) Genetic markers linked to the dwarfing trait of apple rootstock ‘Malling 9’. J Am Soc Hort Sci 133:100–106
Richards CM, Volk GM, Reeves PA, Reilley AA, Henk AD, Forsline PL, Aldwinckle HS (2009a) Selection of stratified core sets representing wild apple (Malus sieversii). J Am Soc Hort Sci 134:228–235
Richards CM, Volk GM, Reilley AA, Henk AD, Lockwood DR, Reeves PA, Forsline PL (2009b) Genetic diversity and population structure in Malus sieversii, a wild progenitor species of domesticated apple. Tree Genet Genomes 5:339–347
Robinson JP, Harris SA, Juniper BE (2001) Taxonomy of the genus Malus Mill. (Rosaceae) with emphasis on the cultivated apple, Malus domestica Borkh. Plant Syst Evol 226:35–58
Sargent D, Marchese A, Simpson D, Howad W, Fernández-Fernández F, Monfort A, Arús P, Evans K, Tobutt K (2009) Development of “universal” gene-specific markers from Malus spp. cDNA sequences, their mapping and use in synteny studies within Rosaceae. Tree Genet Genomes 5:133–145
Segura V, Durel CE, Costes E (2009) Dissecting apple tree architecture into genetic, ontogenetic and environmental effects: QTL mapping. Tree Genet Genomes 5:165–179
Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning thess apple (Malus × domestica Borkh.) genome. Tree Genet Genomes 2:202–224
Soriano JM, Joshi SG, van Kaauwen M, Noordijk Y, Groenwold R, Henken B, van de Weg WE, Schouten HJ (2009) Identification and mapping of the novel apple scab resistance gene Vd3. Tree Genet Genomes 5:475–482
Sun L, John Bukovac M, Forsline P, van Nocker S (2009) Natural variation in fruit abscission-related traits in apple (Malus). Euphytica 165:55–67
Tapken D, Hollmann M (2008) Arabidopsis thaliana glutamate receptor ion channel function demonstrated by ion pore transplantation. J Mol Biol 383:36–48
Tatum TC, Stepanovic S, Biradar DP, Rayburn AL, Korban SS (2005) Variation in nuclear DNA content in Malus species and cultivated apples. Genome 48:924–930
Troggio M, Zharkikh A, Pindo M, Baldi P, Costa F, Chagné D, Micheletti D, Coppola G, Cestaro A, Lasserre P, Crowhurst RN, Bus V, Magnago P, Komjanc M, Lespinasse Y, Salvi S, Durel C-E, Gardiner SE, Velasco R (2010) A sequence-anchored integrated genetic linkage map for apple, Malus × domestica Borkh. Plant & Animal Genomes XVIII Conference, San Diego
Van Ooijen JW, Voorrips RE (2001) JoinMap® 3.0, Software for the calculation of genetic linkage maps. Plant Research International, Wageningen
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C-E, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839
Volk GM, Richards CM, Reilley AA, Henk AD, Forsline PL, Aldwinckle HS (2005) Ex situ conservation of vegetatively propagated species: development of a seed-based core collection for Malus sieversii. J Am Soc Hort Sci 130:203–210
Volk GM, Richards CM, Henk AD, Reilley A, Miller DD, Forsline PL (2009) Novel diversity identified in a wild apple population from the Kyrgyz Republic. Hort Sci 44:516–518
Voorrips RE (2002) MapChart: Software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang D, Shi J, Carlson SR, Cregan PB, Ward RW, Diers BW (2003) A low-cost, high-throughput polyacrylamide gel electrophoresis system for genotyping with microsatellite DNA markers. Crop Sci 43:1828–1832
Williams EB, Kuc J (1969) Resistance in Malus to Venturia Inaequalis. Annu Rev Phytopathol 7:223–246
Wisniewski M, Bassett C, Norelli J, Macarisin D, Artlip T, Gasic K, Korban S (2008) Expressed sequence tag analysis of the response of apple (Malus × domestica ‘Royal Gala’) to low temperature and water deficit. Physiol Plant 133:298–317
Yao L, Zheng X, Cai D, Gao Y, Wang K, Cao Y, Teng Y (2010) Exploitation of Malus EST-SSRs and the utility in evaluation of genetic diversity in Malus and Pyrus. Genet Resour Crop Evol 57:841–851
Yepes LM, Aldwinckle HS (1993) Pathogenesis of Venturia inaequalis on shoot-tip cultures and on greenhouse-grown apple cultivars. Phytopathology 83:1155–1162
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This work was supported in part by the New York State Apple Research and Development Program.
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Wang, A., Aldwinckle, H., Forsline, P. et al. EST contig-based SSR linkage maps for Malus × domestica cv Royal Gala and an apple scab resistant accession of M. sieversii, the progenitor species of domestic apple. Mol Breeding 29, 379–397 (2012). https://doi.org/10.1007/s11032-011-9554-1
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DOI: https://doi.org/10.1007/s11032-011-9554-1