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Two apple repetitive sequence elements: characterisation and potential use as genetic markers

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Abstract

Within the 5′ flanking regions of two ripening-related genes from apple (Malus pumila), two short repeat sequences were identified and named Ars1 andArs2 (Apple repetitivesequences). Both elements were present in the promoter of the Md-ACS1-1 ACC synthase gene and Ars2was also found in the promoter of a gene homologous to the ABG1 β-galactosidase gene. Database searches revealed other examples of each element in apple genomic sequences and a partial Ars2element in a sequence from Asian pear (Pyrus pyrifolia). DNA dot blot analysis demonstrated that both elements are present in high numbers in the apple genome. Ars1 is thought to represent a MITEminiature inverted-repeat transposable element) related to the MITE Alien, while the identity ofArs2, though it is undoubtedly a transposable element, remains undetermined. DNA dot blot analysis and PCR amplification using primers designed from Ars1and Ars2 showed that elements similar to Ars1 and Ars2 are present across the Rosaceae. The amplification patterns obtained using Ars1- and Ars2-specific primers with genomic DNA from different cultivars or mapping populations suggest that these elements could be used for finger printing and segregation analysis in Rosaceae. Evidence from DNA database searches suggests that they may be applicable to genetic studies in a wide range of other organisms.

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References

  • Altschul, S.F., W. Gish, W. Miller, E.W. Myers & D.J. Lipman, 1990. Basic local alignment search tool. J Mol Biol 215: 403-410.

    Article  PubMed  CAS  Google Scholar 

  • Bureau, T.E. & S.R. Wessler, 1994. Stowaway: A new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. Plant Cell 6: 907-916.

    Article  PubMed  CAS  Google Scholar 

  • Bureau, T.E., P.C. Ronald & S.R. Wessler, 1996. A computer-based systematic survey reveals the predominance of small invertedrepeat elements in wild-type rice genes. Proc Natl Acad Sci USA 93: 8524-8529.

    Article  PubMed  CAS  Google Scholar 

  • Casa, A.M., C. Brouwer, A. Nagel, L. Wang, Q. Zhang, S. Kresovich & S.R. Wessler, 2000. The MITE family Heartbreaker (Hbr): Molecular markers in maize. Proc Natl Acad Sci USA 97: 10083-10089.

    Article  PubMed  CAS  Google Scholar 

  • Casacuberta, E., J.M. Casacuberta, P. Puigdomènech & A. Monfort, 1998. Presence of miniature inverted-repeat transposable elements (MITEs) in the genome of Arabidopsis thaliana: characterisation of the Emigrant family of elements. Plant J 16: 79-85.

    Article  PubMed  CAS  Google Scholar 

  • Chang, R.Y., L.S. O'Donoughue & T.E. Bureau, 2001. Inter-MITE polymorphisms (IMP): a high throughput transposon-based genome mapping and fingerprinting approach. Theor Appl Genet 102: 773-781.

    Article  CAS  Google Scholar 

  • Charlesworth, B., P. Sniegowski & W. Stephen, 1994. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215-220.

    Article  PubMed  CAS  Google Scholar 

  • Dellaporta, S.L., J. Wood & J.B. Hicks, 1984. Molecular Biology of Plants: A laboratory Course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.

    Google Scholar 

  • Dong, J.G., W.T. Kim, W.K. Yip, G.A. Thompson, L. Li, A.B. Bennet & S.F. Yang, 1991. Cloning of a cDNA encoding 1-aminocyclopropane-1-carboxylate synthase and expression of its mRNA in ripening apple fruit. Planta 185: 38-45.

    Article  CAS  Google Scholar 

  • Finnegan, D.J., 1992. Transposable elements. Curr Opin Genet Dev 2: 861-867.

    Article  PubMed  CAS  Google Scholar 

  • Flavell, A.J., M.R. Knox, S.R. Pearce & T.H.N. Ellis, 1998. Retrotransposon-based insertion polymorphisms for high throughput marker analysis. Plant J 16: 643-650.

    Article  PubMed  CAS  Google Scholar 

  • Gilbert, N. & D. Labuda, 1999. CORE-SINEs: Eukaryotic short interspersed retroposing elements with common sequence motifs. Proc Natl Acad Sci USA 96: 2869-2874.

    Article  PubMed  CAS  Google Scholar 

  • Harada, T., T. Sunako, W. Sakuraba, S. Goto, S. Akada, M. Senda, R. Ishikawa & M. Niizeki, 1997. Genomic nucleotide sequence of a ripening-related 1-aminocyclopropane-1-carboxylate synthase gene (MdACS-1) in apple. Plant Physiol 113: 1465.

    Google Scholar 

  • Higgins, D.G., J.D. Thompson, T.J. Gibson, 1996. Using CLUSTAL for multiple sequence alignments. Met Enzymol 266: 383-402.

    CAS  Google Scholar 

  • James, D.J., J.R. Gittins, A.J. Massiah, T.K. Pelny, E.R. Hiles, S. Biricolti, A.J. Passey & S.P. Vaughan, 2001. Using heterologous and homologous promoters to study tissue specific transgene expression in fruit crops. Acta Hort 560: 55-62.

    CAS  Google Scholar 

  • Jiang, N., Z. Bao, X. Zhang, H. Hirochika, S.R. Eddy, S.R. Mc-Couch & S.R. Wessler, 2003. An active DNA tranposon family in rice. Nature 421: 163-167.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, A. & J.L. Bennetzen, 1999. Plant retrotransposons. Ann Rev Genet 33: 479-532.

    Article  PubMed  CAS  Google Scholar 

  • Le, Q.H., S. Wright, Z. Yu & T. Bureau, 2000. Transposon diversity in Arabidopsis thaliana. Proc Natl Acad Sci USA 97: 7376-7381.

    Article  PubMed  CAS  Google Scholar 

  • Pearce, S.R., C. Stuart-Rogers, M.R. Knox, A. Kumar, T.H.N. Ellis & A.J. Flavell, 1999. Rapid isolation of plant Ty1-copia group retrotransposon LTR sequences for molecular marker studies. Plant J 19: 711-717.

    Article  PubMed  CAS  Google Scholar 

  • Pearson, W.R., 1990. Rapid and sensitive sequence comparison with FASTP and FASTA. Met Enzymol 183: 63-98.

    Article  CAS  Google Scholar 

  • Peleman, J., B. Cottyn, W. Van Camp, M. Van Montagu & D. Inzé, 1991. Transient occurrence of extrachromosomal DNA of an Arabidopsis thaliana transposon-like element, Tat1. Proc Natl Acad Sci USA 88: 3618-3622.

    Article  PubMed  CAS  Google Scholar 

  • Pozueta-Romero, J., G. Houlné & R. Schantz, 1996. Nonautonomous inverted repeat Alien transposable elements are associated with genes of both monocotyledonous and dicotyledonous plants. Gene 171: 147-153.

    Article  PubMed  CAS  Google Scholar 

  • Purugganan, M.D. & S.R. Wessler, 1995. Transposon signatures: species-specific molecular markers that utilize a class of multiple-copy nuclear DNA. Mol Ecol 4: 265-269.

    PubMed  CAS  Google Scholar 

  • Ross, G.S., T. Wegrzyn, E.A. MacRae & R.J. Redgwell, 1994. Apple beta-galactosidase: Activity against cell wall polysaccharides and characterization of a related cDNA clone. Plant Physiol 106: 521-528.

    Article  PubMed  CAS  Google Scholar 

  • Rowold, D.J. & R.J. Herrera, 2000. Alu elements and the human genome. Genetica 108: 57-72.

    Article  PubMed  CAS  Google Scholar 

  • Sambrook, J., E.F. Fritsch & T. Maniatis, 1989. Molecular Cloning: A laboratory Manual (2nd Edition). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.

    Google Scholar 

  • Sunako, T., W. Sakuraba, M. Senda, S. Akada, R. Ishikawa, M. Niizeki & T. Harada, 1999. An allele of the ripening-specific 1-aminocyclopropane-1-carboxylic acid synthase gene (ACS1) in apple fruit with a long storage life. Plant Physiol 119: 1297-1303.

    Article  PubMed  CAS  Google Scholar 

  • Surzycki, S.A. & W.R. Belknap, 1999. Characterization of repetitive DNA elements in Arabidopsis. J Mol Evol 48: 684-691.

    Article  PubMed  CAS  Google Scholar 

  • Turcotte, K., S. Srinivasan & T. Bureau, 2001. Survey of transposable elements in rice genomic sequences. Plant J 25: 169-179.

    Article  PubMed  CAS  Google Scholar 

  • Voytas, D.F., 1996. Retroelements in genome organization. Science 274: 737-738.

    Article  PubMed  CAS  Google Scholar 

  • Watillon, B., R. Kettmann, P. Boxus & A. Burny, 1992. Cloning and characterization of an apple (Malus pumila) calmodulin gene. Plant Sci 82: 201-212.

    Article  CAS  Google Scholar 

  • Wessler, S.R., T.E. Bureau & S.E. White, 1995. LTR-retrotransposons and MITEs: important players in the evolution of plant genes. Curr Opin Genet Devel 5: 814-821.

    Article  CAS  Google Scholar 

  • Wessler, S.R., 1998. Transposable elements associated with normal plant genes. Physiol Plant 103: 581-586.

    Article  CAS  Google Scholar 

  • Wright, D.A. & D.F. Voytas, 1998. Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins. Genetics 149: 703-715.

    PubMed  CAS  Google Scholar 

  • Yang, H., J. McLeese, M. Weisbart, J.L. Dionne, I. Lemaire & R.A. Aubin, 1993. Simplified high throughput protocol for Northern hybridization. Nucl Acids Res 21: 3337-3338.

    PubMed  CAS  Google Scholar 

  • Yao, J.L., Y.H. Dong & B.A.M. Morris, 2001. Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc Natl Acad Sci USA 98: 1306-1311.

    Article  PubMed  CAS  Google Scholar 

  • Yoshioka, Y., S. Matsumoto, S. Kojima, K. Ohshima, N. Okada & Y. Machida, 1993. Molecular characterization of a short interspersed repetitive element from tobacco that exhibits sequence homology to specific tRNAs. Proc Natl Acad Sci USA 90: 6562-6566.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Q., J. Arbuckle & S.R. Wessler, 2000. Recent, extensive, and preferential insertion of members of the miniature inverted-repeat transposable element family Heartbreaker into genic regions of maize. Proc Natl Acad Sci USA 97: 1160-1165.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, X., C. Feschotte, Q. Zhang, N. Jiang, W.B. Eggleston & S.R. Wessler, 2001. P instability factor: An active maize transposon system associated with the amplification of Tourist-like MITEs and a new superfamily of transposases. Proc Natl Acad Sci USA 98: 12572-12577.

    Article  PubMed  CAS  Google Scholar 

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Hadonou, A., Gittins, J., Hiles, E. et al. Two apple repetitive sequence elements: characterisation and potential use as genetic markers. Euphytica 131, 177–187 (2003). https://doi.org/10.1023/A:1023927230958

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