Advertisement

Plant Molecular Biology

, Volume 51, Issue 5, pp 703–718 | Cite as

Identification and characterisation of a melon genomic region containing a resistance gene cluster from a constructed BAC library. Microcolinearity between Cucumis melo and Arabidopsis thaliana

  • Hans van Leeuwen
  • Amparo Monfort
  • Hong-Bin Zhang
  • Pere Puigdomènech
Article

Abstract

A bacterial artificial chromosome (BAC) library from the dihaploid melon line `PIT92' was constructed with a 6 times coverage of the haploid melon genome. A contig of four BACs around the MRGH63 resistance gene homologue fragment was created. The complete sequence of a 117-kb BAC clone allowed to determine two clearly defined regions, the first one containing a cluster of three resistance gene homologues. Separated by a retrotransposon, that contains large long terminal repeats, the second region presents a group of genes with a conserved distribution in two regions of the Arabidopsis genome. The detailed analysis of this region provides a description of the gene structure and the presence of repetitive sequences in a defined fragment of the genome of Cucumis melo.

Bacterial Artificial Chromosome colinearity Cucurbitaceae genome organisation simple sequence repeats and retrotransposons synteny 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389–3402.Google Scholar
  2. Apweiler, R., Attwood, T.K., Bairoch, A., Bateman, A., Birney, E., Biswas, M., Bucher, P., Cerutti, L., Corpet, F., Croning, M.D.R., et al. 2001. The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res. 29: 37–40.Google Scholar
  3. Arumuganathan, K. and Earle, E.D. 1991. Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9: 208–218.Google Scholar
  4. Bendich, A.J. and Anderson, R.S. 1974. Novel properties of satellite DNA from muskmelon. Proc. Natl. Acad. Sci. USA 71: 1511–1515.Google Scholar
  5. Borodovsky, M. and McIninch, J. 1993. GeneMark: parallel gene recognition for both DNA strands. Computers & Chemistry 17: 123–133.Google Scholar
  6. Burge, C. and Karlin, S. 1997. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268: 78–94.Google Scholar
  7. Casacuberta, E., Puigdomènech, P. and Monfort, A. 2000. Distribution of microsatellites in relation to coding sequences within the Arabidopsis thaliana genome. Plant Sci. 157: 97–104.Google Scholar
  8. Church, G.M. and Gilbert, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991–1995.Google Scholar
  9. Danin-Poleg, Y., Reis, N., Baudracco-Arnas, S., Pitrat, M., Staub, J.E., Oliver, M., ArÚs, P., deVicente, C.M. and Katzir, N. 2000. Simple sequence repeats in Cucumis mapping and map merging. Genome 43: 963–974.Google Scholar
  10. Dixon, M.S., Jones, D.A., Keddie, J.S., Thomas, C.M., Harrison, K. and Jones, J.D. 1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84: 451–459.Google Scholar
  11. Durrant, W.E., Rowland, O., Piedras, P., Hammond-Kosack, K.E. and Jones, J.D.G. 2000. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12: 963–977.Google Scholar
  12. Emanuelsson, O., Nielsen, H., Brunak, S. and von Heijne, G. 2000. Predicting subcellular localisation of proteins based on their Nterminal amino acid sequence. J. Mol. Biol. 300: 1005–1016.Google Scholar
  13. Feinberg, A.P. and Vogelstein, B. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132: 6–13.Google Scholar
  14. Frijters, A.C.J., Zhang, Z., van Damme, M., Wang, G.L., Ronald, P.C. and Michelmore, R.W. 1997. Construction of a bacterial artificial chromosome library containing large EcoRI and HindIII genomic fragments of lettuce. Theor. Appl. Genet. 94: 390–399.Google Scholar
  15. Garcia-Mas, J., van Leeuwen, H., Monfort, A., de Vicente, M.C., Puigdomènech, P. and ArÚs, P. 2001. Cloning and mapping of resistance gene homologues in melon. Plant Sci. 161: 165–172.Google Scholar
  16. Gorelick, R.J., Henderson, L.E., Hanser, J.P. and Rein, A. 1988. Point mutants of Moloney murine leukemia virus that fail to package viral RNA: evidence for specific RNA recognition by a 'zinc finger-like’ protein sequence. Proc. Natl. Acad. Sci. USA 85: 8420–8424.Google Scholar
  17. Hamilton, C.M., Frary, A., Xu, Y., Tanksley, S.D. and Zhang, H.B. 1999. Construction of tomato genomic DNA libraries in a binary-BAC (BIBAC) vector. Plant J. 18: 223–229.Google Scholar
  18. Hassanain, H.H., Sharma, Y.K., Moldovan, L., Khramtsov, V., Berliner, L.J., Duvick, J.P. and Goldschmidt-Clermont, P.J. 2000. Plant rac proteins induce superoxide production in mammalian cells. Biochem. Biophys. Res. Commun. 272: 783–788.Google Scholar
  19. Hebsgaard, S.M., Korning, P.G., Tolstrup, N., Engelbrecht, J., Rouze, P. and Brunak, S. 1996. Splice site prediction in Arabidopsis thaliana DNA by combining local and global sequence information. Nucleic Acids Res. 24: 3439–3452.Google Scholar
  20. Jentoft, J.E., Smith, L.M., Fu, X.D., Johnson, M. and Leis, J. 1988. Conserved cysteine and histidine residues of the avian myeloblastosis virus nucleocapsid protein are essential for viral replication but are not 'zinc-binding fingers'. Proc. Natl. Acad. Sci. USA 85: 7094–7098.Google Scholar
  21. Ku, H.M., Vision, T., Liu, J. and Tanksley, S.D. 2000. Comparing sequenced segments of the tomato and Arabidopsis genomes: Large-scale duplication followed by selective gene loss creates a network of synteny. Proc. Natl. Acad. Sci. USA 97: 9121–9126.Google Scholar
  22. Langdon, T., Seago, C., Mende, M., Leggett, M., Thomas, H., Forster, J.W., Thomas, H., Jones, R.N. and Jenkins, G. 2000. Retrotransposition evolution in diverse plant genomes. Genetics 156: 313–325.Google Scholar
  23. Letunic, I., Goodstadt, L., Dickens, N.J., Doerks, T., Schultz, J., Mott, R., Ciccarelli, F., Copley, R.R., Ponting, C.P. and Bork, P. 2002. Recent improvements to the SMART domain-based sequence annotation resource. Nucleic Acids Res. 30: 242–244.Google Scholar
  24. Lukashin A. and Borodovsky M. 1998. GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26: 1107–1115.Google Scholar
  25. Mayer, K., Murphy, G., Tarchini, R., Wambutt, R., Volckaert, G., Pohl, T., Düsterhöft, A., Stiekema, W., Entian, K., Terryn, N. et al. 2001. Conservation ofMicrostructure between a Sequenced Region of the Genome of Rice and Multiple Segments of the Genome of Arabidopsis thaliana. Genome Res. 11: 1167–1174.Google Scholar
  26. Morales, M., Luís-Arteaga, M., Alvarez, J.M., Dolcet-Sanjuan, R., Monfort, A., ArÚs, P. and Garcia-Mas, J. 2002. Marker saturation of the region flanking the gene NSV conferring resistance to the Melon Necrotic Spot Carmovirus (MNSV) in melon. J. Amer. Soc. Hort. Sci. 127: 540–544.Google Scholar
  27. Nicholas, K.B., Nicholas H.B. Jr. and Deerfield, D.W. II. 1997. GeneDoc: Analysis and Visualization of Genetic Variation, EMBNET.NEWS 4: 14, http://www.hgmp.mrc.ac.uk/embnet.news/vol4-2/genedoc.html.Google Scholar
  28. Oliver, M., Garcia-Mas, J., Cardus, M., Pueyo, N., Lopez-Sese, A.L., Arroyo, M., Gomez-Paniagua, H., Arus, P. and de Vicente, M.C. 2001. Construction of a reference linkage map for melon. Genome 44: 836–845.Google Scholar
  29. Parniske, M., Hammond-Kosack, K.E., Golstein, C., Thomas, C.M., Jones, D.A., Harrison, K., Wulff, B.B. and Jones, J.D. 1997. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 12: 821–832.Google Scholar
  30. Reese, M.G., Eeckman, F.H., Kulp, D. and Haussler, D. 1997. Improved splice site detection in Genie. Proceedings of the First Annual International Conference on Computational Molecular Biology (RECOMB), Santa Fe, NM, ACM Press, New York.Google Scholar
  31. Rice, P., Longden, I. and Bleasby, A. 2000. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16: 276–277.Google Scholar
  32. Richter, T.E. and Ronald, P.C. 2000. The evolution of disease resistance genes. Plant Mol. Biol. 42: 195–204.Google Scholar
  33. Rogozin, I.B. and Milanesi, L. 1997. Analysis of donor splice signals in different organisms. J. Mol. Evol. 45: 50–59.Google Scholar
  34. Rossberg, M., Theres, K., Acarkan, A., Herrero, R., Schmitt, T., Schumacher, K., Schmitz, G. and Schmidt, R. 2001. Comparative sequence analysis reveals extensive microcolinearity in the Lateral Suppressor regions of the tomato, Arabidopsis, and Capsella genomes. Plant Cell 13: 979–988.Google Scholar
  35. Salinas-Mondragón, R.E., Garcidueñas-Piña, C. and Guzmán, P. 1999. Early elicitor induction in members of a novel multigene family coding for highly related RING-H2 proteins in Arabidopsis thaliana. Plant Mol. Biol. 40: 579–590.Google Scholar
  36. Salzberg, S.L., Pertea, M., Delcher, A.L., Gardner, M.J. and Tettelin, H. 1999. Interpolated Markov models for eukaryotic gene finding. Genomics 59: 24–31.Google Scholar
  37. Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.Google Scholar
  38. Schmidt, R. 2002. Plant genome evolution: lessons from comparative genomics at the DNA level. Plant Mol. Biol. 48: 21–37.Google Scholar
  39. Smith, R.F., Wiese, B.A., Wojzynski, M.K., Davison, D.B. and Worley, K.C. 1996. BCM Search Launcher–An Integrated Interface to Molecular Biology Data Base Search and Analysis Services Available on the World Wide Web. Genome Res. 6: 454–462.Google Scholar
  40. Smyth, D.R., Kalitsis, P., Joseph, J.L. and Sentry, J.W. 1989. Plant retrotransposon from Lilium henryi is related to Ty3 of yeast and the gypsy group of Drosophila. Proc. Natl. Acad. Sci. USA 86: 5015–5019.Google Scholar
  41. Soltis, P.S., Soltis, D.E. and Chase, M.W. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402: 402–404.Google Scholar
  42. Song, W.Y., Pi, L.Y., Wang, G.L., Gardner, J., Holsten, T. and Ronald, P.C. 1997. Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9: 1279–1287.Google Scholar
  43. Sonnhammer, E.L.L., von Heijne, G. and Krogh, A. 1998. A hidden Markov model for predicting transmembrane helices in protein sequences. Proceedings of Sixth Conference on Intelligent Systems for Molecular Biology, Menlo Park, CA, USA, AAAI Press, 175–182.Google Scholar
  44. Staden, R. 1996. The Staden Sequence Analysis Package. Mol. Biotechnol. 5: 233–241.Google Scholar
  45. Strong, S.J., Ohta, Y., Litman, G.W. and Amemiya, C.T. 1997. Marked improvement of PAC and BAC cloning is achieved using electroelution of pulsed-field gel-seperated partial digests of genomic DNA. Nucleic Acids Res. 25: 3959–3961.Google Scholar
  46. Sudupak, M.A., Bennetzen, J.L. and Hulbert, S.H. 1993. Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. Genetics 133: 119–125.Google Scholar
  47. Takai, R., Hasegawa, K., Kaku, H., Shibuya, N. and Minami, E. 2001. Isolation and analysis of expression mechanisms of a rice gene, EL5, which shows structural similarity to ATL family from Arabidopsis, in response to N-acetylchitooligosaccharide elicitor. Plant Sci. 160: 577–583.Google Scholar
  48. Tarchini, R., Biddle, P., Wineland, R., Tingey, S. and Rafalski, A. 2000. The complete sequence of 340 kb of DNA around the rice Adh1-Adh2 region reveals interrupted colinearity with maize chromosome 4. Plant Cell 12: 381–391.Google Scholar
  49. Tatusova, T.A. and Madden, T.L. 1999. Blast 2 sequences – a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174: 247–250.Google Scholar
  50. Temnykh, S., DeClerck, G., Lukashova, A., Lipovich, L., Cartinhour, S. and McCouch, S. 2001. Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res. 11: 1441–1452.Google Scholar
  51. The Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.Google Scholar
  52. Wang, G.L., Holsten, T.E., Song, W.Y., Wang, H.P. and Ronald, P.C. 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.Google Scholar
  53. Wang, G.L., Ruan, D.L., Song, W.Y., Sideris, S., Chen, L., Pi, L.Y., Zhang, S., Zhang, Z., Fauquet, C., Gaut, B.S., Whalen, M.C. and Ronald, P.C. 1998. Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell 10: 765–779.Google Scholar
  54. Woo, S.S., Jiang, J., Gill, B., Paterson, A.H. and Wing, R.A. 1994. Construction and characterisation of a bacterial artificial chromosome library of Sorghum bicolor. Nucleic Acids Res. 22: 4922–4931.Google Scholar
  55. Xu, M., Song, J., Cheng, Z., Jiang, J. and Korban, S.S. 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.Google Scholar
  56. Zhang, H.B., Choi, S., Woo, S.S., Li, Z., and Wing, R.A. 1996. Construction and characterisation of two rice bacterial artificial chromosome libraries from the parents of a permanent recombinant inbred mapping population. Mol. Breed. 2: 11–24.Google Scholar
  57. Zhang, H.B., Zhao, X., Ding, X, Paterson, H. and Wing, R. 1995. Preparation of megabase-size DNA from plant nuclei. Plant J. 7: 175–184.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Hans van Leeuwen
    • 1
  • Amparo Monfort
    • 1
    • 2
  • Hong-Bin Zhang
    • 3
  • Pere Puigdomènech
    • 1
  1. 1.Departament de Genètica MolecularInstitut de Biologia Molecular de Barcelona, CID-CSICBarcelonaSpain
  2. 2.Departament de Genètica VegetalIRTA, Ctra. de Cabrils s/nCabrils, BarcelonaSpain
  3. 3.Department of Soil and Crop Sciences and Institute for Plant Genomics and Biotechnology, 2123 TAMUTexas A&M UniversityCollege StationUSA

Personalised recommendations