Abstract
The apple, Malus × domestica Borkh., is one of the most important fruit trees grown worldwide. A bacterial artificial chromosome (BAC)-based physical map of the apple genome has been recently constructed. Based on this physical map, a total of ∼2,100 clones from different contigs (overlapping BAC clones) have been selected and sequenced at both ends, generating 3,744 high-quality BAC end sequences (BESs) including 1,717 BAC end pairs. Approximately 8.5% of BESs contain simple sequence repeats (SSRs), most of which are AT/TA dimer repeats. Potential transposable elements are identified in ∼21% of BESs, and most of these elements are retrotransposons. About 11% of BESs have homology to the Arabidopsis protein database. The matched proteins cover a broad range of categories. The average GC content of the predicted coding regions of BESs is 42.4%; while, that of the whole BESs is 39%. A small number of BES pairs were mapped to neighboring chromosome regions of A. thaliana and Populus trichocarpa; whereas, no pairs are mapped to the Oryza sativa genome. The apple has a higher degree of synteny with the closely related Populus than with the distantly related Arabidopsis. BAC end sequencing can be used to anchor a small proportion of the apple genome to the Populus and possibly to the Arabidopsis genomes.
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Abbreviations
- BAC:
-
Bacterial artificial chromosome
- BES:
-
BAC end sequence
- SSR:
-
Simple sequence repeat
- TE:
-
Transposable element
- EST:
-
Expressed seqeuence tag
References
Blanc G, Barakat A, Guyot R, Cooke R, Delseny M (2000) Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12:1093–1102
Chen M, Presting G, Barbazuk WG, Goicoechea JL, Blackmon B, Fang G, Kim H, Frisch D, Yu Y, Sun S, Higingbottom S, Phimphilai J, Phimphilai D, Thurmond S, Gaudette B, Li P, Liu J, Hatfield J, Main D, Farrar K, Henderson C, Barnett L, Costa R, Williams B, Walser S, Atkins M, Hall C, Budiman MA, Tomkins JP, Luo M, Bancroft I, Salse J, Regad F, Mohapatra T, Singh NK, Tyagi AK, Soderlund C, Dean RA, Wing RA (2002) An integrated physical and genetic map of the rice genome. Plant Cell 14:537–545
Cheung F, Town CD (2007) A BAC end view of the Musa acuminata genome. BMC Plant Biol 7:29
Chevreau E, Lespinasse Y, Gallet M (1985) Inheritance of pollen enzymes and polyploid origin of apple (Malus × domestica Borkh). Theor Appl Genet 71:268–277
Choi S, Creelman RA, Mullet JE, Wing RA (1995) Construction and characterization of a bacterial artificial chromosome library from Arabidopsis thaliana. Weed World 2:17–20
Coburn J, Temnykh S, Paul E, McCouch SR (2002) Design and application of microsatellite marker panels for semi-automated genotyping of rice (Oryza sativa L.). Crop Sci 42:2092–2099
Devos KM, Gale MD (2000) Genome relationships: the grass model in current research. Plant Cell 12:636–646
Eustice M, Yu Q, Lai CW, Hou S, Thimmapuram J, Liu L, Alam M, Moore PH, Presting GG, Ming R (2007) Development and application of microsatellite markers for genomic analysis of papaya. Tree Genet Genomes doi: 10.1007/s11295-007-0112-2
Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185
Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: Where genetics meets genomics. Nat Rev Genet 3:329–341
Frelichowski JE, Palmer MB, Main D, Tomkins JP, Cantrell RG, Stelly DM, Yu J, Kohel RJ, Ulloa M (2006) Cotton genome mapping with new microsatellites from Acala ‘Maxxa’ BAC-ends. Mol Gen Genomics 275:479–491
Gao LF, Jing RL, Huo NX, Li Y, Li XP, Zhou RH, Chang XP, Tang JF, Ma ZY, Jia JZ (2004) One hundred and one new microsatellite loci derived from ESTs (EST-SSRs) in bread wheat. Theor Appl Genet 108:1392–1400
Han Y, Korban SS (2007) Spring: a novel family of miniature inverted-repeat transposable elements is associated with genes in apple. Genomics 90:195–200
Han Y, Gasic K, Marron B, Beever JE, Korban SS (2007) A BAC-based physical map of the apple genome. Genomics 89:630–637
Ilic K, San Miguel PJ, Bennetzen JL (2003) A complex history of rearrangements in an orthologous region of the maize, sorghum, and rice genomes. Proc Natl Acad Sci USA 100:12265–12270
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Katti MV, Ranjekar PK, Gupta VS (2001) Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol 18:1161–1167
Klein PE, Klein RR, Cartinhour SW, Ulanch PE, Dong J, Obert JA, Morishige DT, Schlueter SD, Childs KL, Ale M, Mullet JE (2000) A high-throughput AFLP-based method for constructing integrated genetic and physical maps: progress toward a sorghum genome map. Genome Res 10:789–807
La Rota M, Kantety RV, Yu JK, Sorrells ME (2005) Nonrandom distribution and frequencies of genomic and EST-derived microsatellite markers in rice wheat and barley. BMC Genomics 6:23–35
Lai CWJ, Yu Q, Hou S, Skelton RL, Jones MR, Lewis KLT, Murray J, Eustice M, Guan P, Agbayani R, Moore PH, Ming R, Presting GG (2006) Analysis of papaya BAC end sequences reveals first insights into the organization of a fruit tree genome. Mol Genet Genomics 276:1617–4615
Larkin DM, Everts-van der Wind A, Rebeiz M, Schweitzer PA, Bachman S, Green C, Wright CL, Campos EJ, Benson LD, Edwards J, Liu L, Osoegawa K, Womack JE, de Jong PJ, Lewin HA (2003) A cattle-human comparative map built with cattle BAC-ends and human genome sequence. Genome Res 13:1966–1972
Mahairas GG, Wallace JC, Smith K, Swartzell S, Holzman T, Keller A, Shaker R, Furlong J, Young J, Zhao S, Adams MD, Hood L (1999) Sequence-tagged connectors: a sequence approach to mapping and scanning the human genome. Proc Natl Acad Sci USA 96:9739–9744
McCouch SR, Teytelman L, Xu Y, Lobos KB, Clare K, Walton M, Fu B, Maghirang R, Li Z, Xing Y, Zhang Q, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L (2002) Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Res 9:199–207
Meksem K, Zobrist K, Hyten D, Quangzhou T, Zhang H, Lightfoot DA (2000) Two large-insert soybean genomic libraries constructed in a binary vector: applications in chromosome walking and genome wide physical mapping. Theor Appl Genet 101:747–755
Ming R, Moore PH, Zee F, Abbey CA, Ma H, Paterson AH (2001) Construction and characterization of a papaya BAC library as a foundation for molecular dissection of a tree-fruit genome. Theor Appl Genet 102:892–899
Mozo T, Dewar K, Dunn P, Ecker JR, Fischer S, Kloska S, Lehrach H, Marra M, Martienssen R, Meier-Ewert S et al (1999) A complete BAC-based physical map of the Arabidopsis thaliana genome. Nat Genet 22:271–275
Newcomb RE, 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) Analysis of expressed sequence tags from apple. Plant Physiol 141:147–166
O’Neill CM, Bancroft I (2000) Comparative physical mapping of segments of the genome of Brassica oleracea var. alboglabra that are homeologous to sequenced regions of chromosomes 4 and 5 of Arabidopsis thaliana. Plant J 23:233–243
Paterson AH, Lan T, Reischmann KP, Chang C, Lin Y, Liu S, Burow MD, Kowalski SP, Katsar CS, DelMonte TA, Feldmann KA, Schertz KF, Wendel JF (1996) Toward a unified genetic map of higher plants, transcending the monocot–dicot divergence. Nat Genet 14:380–382
Salimath SS, Bhattacharyya MK (1999) Generation of a soybean BAC library, and identification of DNA sequences tightly linked to the Rps1-k disease resistance gene. Theor Appl Genet 98:712–720
Sharopova N, McMullen MD, Schultz L, Schroeder S, Sanchez-Villeda H, Gardiner J, Bergstrom D, Houchins K, Melia-Hancock S, Musket T, Duru N, Polacco M, Edwards K, Ruff T, Register JC, Brouwer C, Thompson R, Velasco R, Chin E, Lee M, Woodman-Clikeman W, Long MJ, Liscum E, Cone K, Davis G, Coe EH Jr (2002) Development and mapping of SSR markers for maize. Plant Mol Biol 48:463–481
Shoemaker RC, Polzin K, Labate J, Specht J, Brummer EC, Olson T, Young N, Concibido V, Wilcox J, Tamulonis JP, Kochert GA, Boerma HR (1996) Genome duplication in soybean (Glycine subgenus soja). Genetics 144:329–338
Shultz JL, Kurunam D, Shopinski K, Iqbal MJ, Kazi S, Zobrist K, Bashir R, Yaegashi S, Lavu N, Afzal AJ, Yesudas CR, Kassem MA, Wu C, Zhang HB, Town CD, Meksem K, Lightfoot DA (2006) The Soybean Genome Database (SoyGD): a browser for display of duplicated, polyploid, regions and sequence tagged sites on the integrated physical and genetic maps of Glycine max. Nucleic Acids Res 34:D758–D765
Shultz JL, Kazi S, Bashir R, Afzal JA, Lightfoot DA (2007a) The development of BAC-end sequence-based microsatellite markers and placement in the physical and genetic maps of soybean. Theor Appl Genet 114:1081–1090
Shultz JL, Ali S, Ballard L, Lightfoot DA (2007b) Development of a physical map of the soybean pathogen Fusarium virguliforme based on synteny with Fusarium graminearum genomic DNA. BMC Genomics 8:262–268
Tamanna A, Khan AU (2005) Mapping and analysis of simple sequence repeats in the Arabidopsis thaliana genome. Bioinformation 1:64–68
Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160
Tatum T, Stepanovic S, Biradar DP, Rayburn AL, Korban SS (2005) Variation in nuclear DNA content in Malus species and cultivated apples. Genome 48:924–930
The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the fowering plant Arabidopsis thaliana. Nature 408:796–815
Tomkins JP, Mahalingam R, Smith H, Goicoechea JL, Knap HT, Wing RA (1999) A bacterial artificial chromosome library for soybean PI 437654 and identification of clones associated with cyst nematode resistance. Plant Mol Biol 41:25–32
Tóth G, Gáspári Z, Jurka J (2000) Microastellites in different eukaryotic genomes: survey and analysis. Genome Res 10:967–981
Venter JC, Smith HO, Hood L (1996) A new strategy for genome sequencing. Nature 381:364–366
Vinatzer BA, Zhang H-B, Sansavini S (1998) Construction and characterization of a bacterial artificial chromosome library of apple. Theor Appl Genet 97:1183–1190
Wang GL, Holsten TE, Song WY, Wang HP, Ronald PC (1995) Construction of a rice bacterial artificial chromosome library and identification of clones linked to the Xa-21 disease resistance locus. Plant J 7:525–533
Woo SS, Jiang J, Gill BS, Paterson AH, Wing RA (1994) Construction and characterization of a bacterial artificial chromosome library of Sorghum bicolor. Nucleic Acids Res 22:4922–4931
Xia X, Xie Z, Li W (2003) Effects of GC content and mutational pressure on the lengths of exons and coding sequences. J Mol Evol 56:362–370
Xu M, Korban SS (2002) A cluster of four receptor-like genes resides in the Vf locus that confers resistance to apple scab disease. Genetics 162:1995–2006
Xu M, Song J, Cheng Z, Jiang J, Korban SS (2001) A bacterial artificial chromosome (BAC) library of Malus floribunda 821 and contig construction for positional cloning of the apple scab resistance gene Vf. Genome 44:1104–1113
Yim YS, Davis GL, Duru NA, Musket TA, Linton EW, Messing JW, McMullen MD, Soderlund CA, Polacco ML, Gardiner JM, Coe EH Jr (2002) Characterization of three maize bacterial artificial chromosome libraries toward anchoring of the physical map to the genetic map using high-density bacterial artificial chromosome filter hybridization. Plant Physiol 130:1686–1696
Acknowledgements
This project was supported by the USDA Cooperative State Research, Education and Extension Service—National Research Initiative—Plant Genome Program grant No. 2005-35300-15538
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Han, Y., Korban, S.S. An overview of the apple genome through BAC end sequence analysis. Plant Mol Biol 67, 581–588 (2008). https://doi.org/10.1007/s11103-008-9321-9
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DOI: https://doi.org/10.1007/s11103-008-9321-9