Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지

Genomic Distribution of Simple Sequence Repeats in Brassica rapa

  • Hong, Chang Pyo (Department of Horticulture, College of Agriculture and Life Science, Chungnam National University) ;
  • Piao, Zhong Yun (College of Horticulture, Shenyang Agricultural University) ;
  • Kang, Tae Wook (Korean Bioinformation Center (KOBIC), Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Batley, Jacqueline (Primary Industries Research Victoria, Department of Primary Industries, Victorian AgriBioscience Centre) ;
  • Yang, Tae-Jin (Department of Plant Science, College of Agriculture and Life Sciences, Seoul National University) ;
  • Hur, Yoon-Kang (Department of Bioscience, School of Bioscience and Biotechnology, Chungnam National University) ;
  • Bhak, Jong (Korean Bioinformation Center (KOBIC), Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Park, Beom-Seok (Brassica Genomics Team, National Institute of Agricultural Biotechnology, Rural Development Administration) ;
  • Edwards, David (Primary Industries Research Victoria, Department of Primary Industries, Victorian AgriBioscience Centre) ;
  • Lim, Yong Pyo (Department of Horticulture, College of Agriculture and Life Science, Chungnam National University)
  • Received : 2006.12.28
  • Accepted : 2007.03.06
  • Published : 2007.06.30
⟨ Previous Next ⟩

Abstract

Simple Sequence Repeats (SSRs) represent short tandem duplications found within all eukaryotic organisms. To examine the distribution of SSRs in the genome of Brassica rapa ssp. pekinensis, SSRs from different genomic regions representing 17.7 Mb of genomic sequence were surveyed. SSRs appear more abundant in non-coding regions (86.6%) than in coding regions (13.4%). Comparison of SSR densities in different genomic regions demonstrated that SSR density was greatest within the 5'-flanking regions of the predicted genes. The proportion of different repeat motifs varied between genomic regions, with trinucleotide SSRs more prevalent in predicted coding regions, reflecting the codon structure in these regions. SSRs were also preferentially associated with gene-rich regions, with peri-centromeric heterochromatin SSRs mostly associated with retrotransposons. These results indicate that the distribution of SSRs in the genome is non-random. Comparison of SSR abundance between B. rapa and the closely related species Arabidopsis thaliana suggests a greater abundance of SSRs in B. rapa, which may be due to the proposed genome triplication. Our results provide a comprehensive view of SSR genomic distribution and evolution in Brassica for comparison with the sequenced genomes of A. thaliana and Oryza sativa.

Keywords

Acknowledgement

Supported by : Korean Science and Engineering Foundation

References

  1. Abdurakhmonov, I. Y., Abdullaev, A. A., Saha, S., Buriev, Z. T., Arslanov, D., et al. (2005) Simple sequence repeat marker associated with a natural leaf defoliation trait in tetraploid cotton. J. Hered. 96, 644-653 https://doi.org/10.1093/jhered/esi097
  2. Alba, M. M., Santibáñez-Koref, M. F., and Hancock, J. M. (1999) Amino acid reiterations in yeast are overrepresented in particular classes of proteins and show evidence of a slippage-like mutational process. J. Mol. Evol. 49, 789-797 https://doi.org/10.1007/PL00006601
  3. Bachtrog, D., Weiss, S., Zangerl, B., Brem, G., and Schlötterer, C. (1999) Distribution of dinucleotide microsatellites in the Drosophila melanogaster genome. Mol. Biol. Evol. 16, 602-610 https://doi.org/10.1093/oxfordjournals.molbev.a026142
  4. Bevan, M. and Walsh, S. (2005) The Arabidopsis genome: a foundation for plant research. Genome Res. 15, 1632-1642 https://doi.org/10.1101/gr.3723405
  5. Brinkmann, B., Klintschar, M., Neuhuber, F., Huhne, J., and Rolf, B. (1998) Mutation rate in human microsatellites: influence of the structure and length of the tandem repeat. Am. J. Hum. Genet. 62, 1408-1415 https://doi.org/10.1086/301869
  6. Cardle, L., Ramsay, L., Milbourne, D., Macaulay, M., Marshall, D., et al. (2000) Computational and experimental characterization of physically clustered simple sequence repeats in plants. Genetics 156, 847-854
  7. Chung, S. M. and Staub, J. E. (2003) The development and evaluation of consensus chloroplast primer pairs that possess highly variable sequence regions in a diverse array of plant taxa. Theor. Appl. Genet. 107, 757-767 https://doi.org/10.1007/s00122-003-1311-3
  8. Edwards, Y. J., Elgar, G., Clark, M. S., and Bishop, M. J. (1998) The identification and characterization of microsatellites in the compact genome of the Japanese pufferfish, Fugu rubripes: perspectives in functional and comparative genomic analyses. J. Mol. Biol. 278, 843-854 https://doi.org/10.1006/jmbi.1998.1752
  9. Eisen, J. (1999) Mechanistic explanations for variation in microsatellite stability within and between species; in Microsatellites: Evolution and Applications, Goldstein, D. and Schlötterer, C. (eds.), pp. 34-48, Oxford University Press, Oxford
  10. Ellegren, H. (2000) Heterogeneous mutation processes in human microsatellite DNA sequences. Nat. Genet. 24, 400-402 https://doi.org/10.1038/74249
  11. Ellegren, H. (2004) Microsatellites: simple sequence sequences with complex evolution. Nat. Rev. Genet. 5, 435-445
  12. Field, D. and Wills, C. (1996) Long, polymorphic microsatellites in simple organisms. Proc. R. Soc. London Ser. B. 263, 209-251
  13. Flannery, M. L., Mitchell, F. J., Coyne, S., Kavanagh, T. A., Burke, J. I., et al. (2006) Plastid genome characterisation in Brassica and Brassicaceae using a new set of nine SSRs. Theor. Appl. Genet. 113, 1221-1231 https://doi.org/10.1007/s00122-006-0377-0
  14. Fujimori, S., Washio, T., Higo, K., Ohtomo, Y., Murakami, K., et al. (2003) A novel feature of microsatellites in plants: a distribution gradient along the direction of transcription. FEBS Lett. 554, 17-22 https://doi.org/10.1016/S0014-5793(03)01041-X
  15. Goldstein, D. B. and Clark, A. G.. (1995) Microsatellite variation in North American populations of Drosophila melanogaster. Nucleic Acids Res. 23, 3882-3886 https://doi.org/10.1093/nar/23.19.3882
  16. Harr, B. and Schlötterer, C. (2000) Long microsatellite alleles in Drosophila melanogaster have a downward mutation bias and short persistence times, which cause their genome-wide underrepresentation. Genetics 155, 1213-1220
  17. Harr, B., Todorova, J., and Schlötterer, C. (2002) Mismatch repair-driven mutational bias in D. melanogaster. Mol. Cell 10,199-205 https://doi.org/10.1016/S1097-2765(02)00575-0
  18. Hancock, J. M. (1995) The contribution of slippage-like process to genome evolution. J. Mol. Evol. 41, 1038-1047
  19. Hong, C. P., Lee, S. J., Park, J. Y., Plaha, P., Park, Y. S., et al. (2004) Construction of a BAC library of Korean ginseng and initial analysis of BAC-end sequences. Mol. Genet. Genomics 271, 709-716
  20. Hong, C. P., Plaha, P., Koo, D. H., Yang, T. J., Choi, S. R., et al. (2006) A survery of the Brassica rapa Genome by BAC-end sequence analysis and comparison with Arabidopsis thaliana. Mol. Cells 22, 300-307
  21. Johnston, J. S., Pepper, A. E., Hall, A. E., Chen, Z. J., Hodnett, G., et al. (2005) Evolution of genome size in Brassicaceae. Ann. Bot. 95, 229-235 https://doi.org/10.1093/aob/mci016
  22. Katti, M. V., Ranjekar, P. K., and Gupta, V. S. (2001) Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol. Biol. Evol. 18, 1161-1167 https://doi.org/10.1093/oxfordjournals.molbev.a003903
  23. Kruglyak, S., Durrett, R. T., Schug, M. D., and Aquadro, C. F. (1998) Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. Proc. Natl. Acad. Sci. USA 95, 10774-10778
  24. Lagercrantz, U. (1998) Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150, 1217-1228
  25. La Rota, M., Kantety, R. V., Yu, J. K., and Sorrells, M. E. (2005) Nonrandom distribution and frequencies of genomic and EST-derived microsatellite markers in rice, wheat, and barley. BMC Genomics 6, 23
  26. Lawson, M. J. and Zhang, L. (2006) Distinct patterns of SSR distribution in the Arabidopsis thaliana and rice genomes. Genome Biol. 7, R14 https://doi.org/10.1186/gb-2006-7-2-r14
  27. Li, Y. C., Korol, A. B., Fahima, T., Beiles, A., and Nevo, E. (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol. Ecol. 11, 2453-2465 https://doi.org/10.1046/j.1365-294X.2002.01643.x
  28. Li, Y. C., Korol, A. B., Fahima, T., and Nevo, E. (2004) Microsatellites within genes: structure, function, and evolution. Mol. Biol. Evol. 21, 991-1007 https://doi.org/10.1093/molbev/msh073
  29. Lim, K. B., Yang, T. J., Hwang, Y. J., Kim, J. S., Park, J. Y., et al. (2007) Characterization of the centromere and peri-centromere retrotransposons in Brassica rapa and their distribution in related Brassica species. Plant J. 49, 173-183 https://doi.org/10.1111/j.1365-313X.2006.02952.x
  30. Lysak, M. A., Koch, M. A., Pecinka, A., and Schubert, I. (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res. 15, 516-525 https://doi.org/10.1101/gr.3531105
  31. McCouch, S. R., Chen, X., Panaud, O., Temnykh, S., Xu, Y., et al. (1997) Microsatellite marker development, mapping and applications in rice genetics and breeding. Plant Mol. Biol. 35, 89-99 https://doi.org/10.1023/A:1005711431474
  32. Meloni, R., Albanese, V., Ravassard, P., Treilhou, F., and Mallet, J. (1998) A tetranucleotide polymorphic microsatellite, located in the first intron of the tyrosine hydroxylase gene, acts as a transcription regulatory element in vitro. Hum. Mol. Genet. 7, 423-428 https://doi.org/10.1093/hmg/7.3.423
  33. Messing, J., Bharti, A. K., Karlowski, W. M., Gundlach, H., Kim, H. R., et al. (2004) Sequence composition and genome organization of maize. Proc. Natl. Acad. Sci. USA 101, 14349-14354
  34. Metzgar, D., Bytof, J., and Wills, C. (2000) Selection against frameshift mutations limits microsatellite expansion in coding DNA. Genome Res. 10, 72-80
  35. Mortimer, J. C., Batley, J., Love, C. G., Logan, E., and Edwards, D. (2005) Simple sequence repeat (SSR) and GC distribution in the Arabidopsis thaliana genome. J. Plant Biotechnol. 7, 17-25
  36. Morgante, M., Hanafey, M., and Powell, W. (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat. Genet. 30, 194-200 https://doi.org/10.1038/ng822
  37. Nadir, E., Margalit, H., Gallily, T., and Ben-Sasson, S. A. (1996) Microsatellite spreading in the human genome: evolutionary mechanisms and structural implications. Proc. Natl. Acad. Sci. USA 93, 6470-6475
  38. O'Neill, C. M. and Bancroft, I. (2000) Comparative physical mapping of segments of the genome of Brassica oleracea var. alboglabra that are homoeologous to sequenced regions of chromosomes 4 and 5 of Arabidopsis thaliana. Plant J. 23, 233-243 https://doi.org/10.1046/j.1365-313x.2000.00781.x
  39. Park, J. Y., Koo, D. H., Hong, C. P., Lee, S. J., Jeon, J. W., et al. (2005) Physical mapping and microsynteny of Brassica rapa ssp. pekinensis genome corresponding to a 222 kb gene-rich region of Arabidopsis chromosome 4 and partially duplicated on chromosome 5. Mol. Genet. Genomics 274, 579-588 https://doi.org/10.1007/s00438-005-0041-4
  40. Plieske, J. and Struss, D. (2001) Microsatellite markers for genome analysis in Brassica. I. development in Brassica napus and abundance in Brassicaceae species. Theor. Appl. Genet. 102, 689-694 https://doi.org/10.1007/s001220051698
  41. Ramsay, L., Macaulay, M., Cardle, L., Morgante, M., degli Ivanissevich, S., et al. (1999) Intimate association of microsatellite repeats with retrotransposons and other dispersed repetitive elements in barley. Plant J. 17, 415-425 https://doi.org/10.1046/j.1365-313X.1999.00392.x
  42. Rana, D., van den Boogaart, T., O'Neill, C. M., Hynes, L., Bent, E., et al. (2004) Conservation of the microstructure of genome segments in Brassica napus and its diploid relatives. Plant J. 40, 725-733 https://doi.org/10.1111/j.1365-313X.2004.02244.x
  43. Ranum, L. P. and Day, J. W. (2002) Dominantly inherited, noncoding microsatellite expansion disorders. Curr. Opin. Genet. Dev. 12, 266-271 https://doi.org/10.1016/S0959-437X(02)00297-6
  44. Rosenberg, N. A., Pritchard, J. K., Weber, J. L., Cann, H. M., Kidd, K. K., et al. (2002) Genetic structure of human populations. Science 298, 2381-2385 https://doi.org/10.1126/science.1078311
  45. Schlotterer, C. (1998) Are microsatellites really simple sequences? Curr. Biol. 8, R132-R134 https://doi.org/10.1016/S0960-9822(98)70989-3
  46. Schlotterer, C. (2000) Evolutionary dynamics of microsatellite DNA. Chromosoma 109, 365-371 https://doi.org/10.1007/s004120000089
  47. Schlotterer, C., Ritter, R., Harr, B., and Brem, G. (1998) High mutation rate of a long microsatellite allele in Drosophila melanogaster provides evidence for allele-specific mutation rates. Mol. Biol. Evol. 15, 1269-1274 https://doi.org/10.1093/oxfordjournals.molbev.a025855
  48. Schug, M. D., Hutter, C. M., Wetterstrand, K. A., Gaudette, M. S., Mackay, T. F., et al. (1998) The mutation rates of di-, triand tetranucleotide repeats in Drosophila melanogaster. Mol. Biol. Evol. 15, 1751-1760 https://doi.org/10.1093/oxfordjournals.molbev.a025901
  49. Subramanian, S., Mishra, R. K., and Singh, L. (2003) Genomewide analysis of microsatellite repeats in humans: their abundance and density in specific genomic regions. Genome Biol. 4, R13 https://doi.org/10.1186/gb-2003-4-2-r13
  50. Tautz, D. and Schlötterer, C. (1994) Simple sequences. Curr. Opin. Genet. Dev. 4, 832-837 https://doi.org/10.1016/0959-437X(94)90067-1
  51. Temnykh, S., DeClerck, G., Lukashova, A., Lipovich, L., Cartinhour, S., et al. (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 https://doi.org/10.1101/gr.184001
  52. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815 https://doi.org/10.1038/35048692
  53. Toth, G., Gaspari, Z., and Jurka, J. (2000) Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res. 10, 967-981 https://doi.org/10.1101/gr.10.7.967
  54. Toutenhoofd, S. L., Garcia, F., Zacharias, D. A., Wilson, R. A., and Strehler, E. E. (1998) Minimum CAG repeat in the human calmodulin-1 gene 5′ untranslated region is required for full expression. Biochim. Biophys. Acta. 1398, 315-320 https://doi.org/10.1016/S0167-4781(98)00056-6
  55. U, N. (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn. J. Bot. 7, 389-452
  56. Varshney, R. K., Graner, A., and Sorrells M. E. (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol. 23, 48-55 https://doi.org/10.1016/j.tibtech.2004.11.005
  57. Weber, J. L. and Wong, C. (1993) Mutation of human short tandem repeats. Hum. Mol. Genet. 2, 1123-1128 https://doi.org/10.1093/hmg/2.8.1123
  58. Wierdl, M., Dominska, M., and Petes, T. D. (1997) Microsatellite instability in yeast: dependence on the length of the microsatellite. Genetics 146, 769-779
  59. Xu, X., Peng, M., and Fang, Z. (2000) The direction of microsatellite mutations is dependent upon allele length. Nat. Genet. 24, 396-399 https://doi.org/10.1038/74238
  60. Yang, T. J., Kim, J. S., Kwon, S. J., Lim, K. B., Choi, B. S., et al. (2006) Sequence-level analysis of the diploidization process in the triplicated FLOWERING LOCUS C region of Brassica rapa. Plant Cell 18, 1339-1347 https://doi.org/10.1105/tpc.105.040535
  61. Yang, T. J., Kwon, S. J., Choi, B. S., Kim, J. S., Jin, M., et al. (2007) Characterization of terminal-repeat retrotransposon in miniature (TRIM) in Brassica relatives. Theor. Appl. Genet. 114, 627-636 https://doi.org/10.1007/s00122-006-0463-3
  62. Yang, Y. W., Lai, K. N., Tai, P. Y., and Li, W. H. (1999) Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J. Mol. Evol. 48, 597-604 https://doi.org/10.1007/PL00006502
  63. Zhang, L., Yuan, D., Yu, S., Li, Z., Cao, Y., et al. (2004) Preference of simple sequence repeats in coding and non-coding regions of Arabidopsis thaliana. Bioinformatics 20, 1081-1086 https://doi.org/10.1093/bioinformatics/bth043
  64. Zoghbi, H. Y. and Orr, H. T. (2000) Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23, 217-237 https://doi.org/10.1146/annurev.neuro.23.1.217