Plant Molecular Biology

, Volume 48, Issue 5–6, pp 539–547 | Cite as

Insertion-deletion polymorphisms in 3′ regions of maize genes occur frequently and can be used as highly informative genetic markers

  • Dinakar Bhattramakki
  • Maureen Dolan
  • Mike Hanafey
  • Robin Wineland
  • Dave Vaske
  • James C. RegisterIII
  • Scott V. Tingey
  • Antoni Rafalski

Abstract

Single-nucleotide polymorphisms (SNPs) are the most frequent variations in the genome of any organism. SNP discovery approaches such as resequencing or data mining enable the identification of insertion deletion (indel) polymorphisms. These indels can be treated as biallelic markers and can be utilized for genetic mapping and diagnostics. In this study 655 indels have been identified by resequencing 502 maize (Zea mays) loci across 8 maize inbreds (selected for their high allelic variation). Of these 502 loci, 433 were polymorphic, with indels identified in 215 loci. Of the 655 indels identified, single-nucleotide indels accounted for more than half (54.8%) followed by two- and three-nucleotide indels. A high frequency of 6-base (3.4%) and 8-base (2.3%) indels were also observed. When analysis is restricted to the B73 and Mo17 genotypes, 53% of the loci analyzed contained indels, with 42% having an amplicon size difference. Three novel miniature inverted-repeat transposable element (MITE)-like sequences were identified as insertions near genes. The utility of indels as genetic markers was demonstrated by using indel polymorphisms to map 22 loci in a B73 × Mo17 recombinant inbred population. This paper clearly demonstrates that the resequencing of 3′ EST sequence and the discovery and mapping of indel markers will position corresponding expressed genes on the genetic map.

genetic mapping indel insertion-deletion polymorphism MITE molecular marker SNP 

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References

  1. Avramova, Z., Tikhonov, A.P., Chen, M. and Bennetzen, J.L. 1998. Matrix attachment regions and structural collinearity in the genomes of two grass species. Nucl. Acids Res. 26: 761-767.Google Scholar
  2. Buckner, B., Miguel, P.S., Janick-Buckner, D. and Bennetzen, J.L. 1996. The y1 gene of maize codes for phytoene synthase. Genetics 143: 479-488.Google Scholar
  3. Bureau, T.E. and Wessler, S.R. 1992. Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4: 1283-1294.Google Scholar
  4. Bureau, T.E. and Wessler, S.R. 1994. Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses. Proc. Natl. Acad. Sci. USA 91: 1411-1415.Google Scholar
  5. Cardle, L., Ramsay, L., Milbourne, D., Macaulay, M., Marshall, D. and Waugh, R. 2000. Computational and experimental characterization of physically clustered simple sequence repeats in plants. Genetics 156: 847-854.Google Scholar
  6. Casa, A.M., Brouwer, C., Nagel, A., Wang, L., Zhang, Q., Kresovich, S. and Wessler, S.R. 2000. The MITE family heartbreaker (Hbr): molecular markers in maize. Proc. Natl. Acad. Sci. USA 97: 10083-10089.Google Scholar
  7. Coe, E.H. Jr., Neuffer, M.G. and Hoisington, D.A. 1988. The genetics of corn. In: G.F. Sprague and J.W. Dudley (Eds) Corn and Corn Improvement, American Society of Agronomy, Madison, WI, pp. 81-258.Google Scholar
  8. Ewing, B. and Green, P. 1998. Base calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8: 186-194.Google Scholar
  9. Ewing, B., Hillier, L., Wendl, M.C. and Green, P. 1998. Base calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8: 175-185.Google Scholar
  10. Gardiner, J.M., Coe, E.H., Melia-Hancock, S., Hoisington, D.A. and Chao, S. 1993. Development of a core RFLP map in maize using an immortalized F2 population. Genetics 134: 917-980.Google Scholar
  11. Gordon, D., Abajian, C. and Green, P. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8: 195-202.Google Scholar
  12. Isaksson, A., Landegren, U., Syvanen, A.C., Bork, P., Stein, C., Ortigao, F. and Brookes, A.J. 2000. Discovery, scoring and utilization of human single nucleotide polymorphisms: a multidisciplinary problem. Eur. J. Hum. Genet. 8: 154-156.Google Scholar
  13. Jones, C.J., Edwards, K.J., Castaglione, S., Winfield, M.O., Sala, F., van de Wiel, C., Bredemeijer, G., Vosman, B., Matthes, M., Daly, A., Brettschneider, R., Bettini, P., Buiatti, M., Maestri, E., Malcevschi, A., Marmiroli, N., Aert, R., Volckaert, G., Rueda, J., Linacero, R., Vazquez, A. and Karp, A. 1997. Reproducibility testing of RAPD, AFLP and SSR markers in plants by a network of European laboratories. Mol. Breed. 3: 381-390.Google Scholar
  14. Landegren, U., Nilsson, M. and Kwok, P.Y. 1998. Reading bits of genetic information: methods for single-nucleotide polymorphism analysis. Genome Res. 8: 769-776.Google Scholar
  15. Lander, E.S., Green, P., Abrahamson, J., Barlow, A., Daly, M.J., Lincoln, S.E. and Newburg, L. 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 174-181.Google Scholar
  16. mdb/mdb3/+Panel+of+Stocks/235384.Google Scholar
  17. Levinson, G. and Gutman, G.A. 1987. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol. Biol. Evol. 4: 203-221.Google Scholar
  18. Li, W.-H. 1997. Molecular Evolution. Sinauer Associates, Inc., Sunderland, MA.Google Scholar
  19. Marshall, D.R. and Allard, R.W. 1970. Isozyme polymorphisms in natural populations of Avena fatua and Avena barbata. Heredity 25: 373-382.Google Scholar
  20. Morgante, M. and Olivieri, A.M. 1993. PCR-amplified microsatellites as markers in plant genetics. Plant J. 3: 175-182.Google Scholar
  21. Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. USA 70: 3321-3323.Google Scholar
  22. Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.Google Scholar
  23. Powell, W., Morgante, M., Andre, C., Hanafey, M., Vogel, J., Tingey, S. and Rafalski, A. 1996. The comparison of RFLP, RAPD, AFLP and SSR (microsatellite) markers for germplasm analysis. Mol. Breed. 2: 225-238.Google Scholar
  24. software/other/primer3.html.Google Scholar
  25. Senior, L., Murphy, J.P., Goodman, M.M. and Stuber, C.W. 1998. Utility of SSRs for determining genetic similarities and relationships in maize using an agarose gel system. Crop Sci. 38: 1088-1098.Google Scholar
  26. Senior, M.L. and Heun, M. 1993. Mapping maize microsatellites and polymerase chain reaction confirmation of the targeted repeats using a CT primer. Genome 36: 884-889.Google Scholar
  27. Smith, J.S.C., Chin, E., Shu, H., Smith, O.S., Wall, S.J., Senior, L., Mitchell, S., Kresovich, S. and Ziegle, J. 1997. An evaluation of the utility of SSR loci as molecular markers in maize (Zea mays L): comparisons with data from RFLPs and pedigree. Theor. Appl. Genet. 95: 163-173.Google Scholar
  28. Taramino, G. and Tingey, S. 1996. Simple sequence repeats for germplasm analysis and mapping in maize. Genome 39: 277-287.Google Scholar
  29. 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
  30. Tikhonov, A.P., San Miguel, P.J., Nakajima, Y., Gorenstein, N.D., Bennetzen, J.L. and Avramova, Z. 1999. Collinearity and its exceptions in orhologous adh regions of maize and sorghum. Proc. Natl. Acad. Sci. USA 96: 7409-7414.Google Scholar
  31. Wang, D.G., Fan, J.B., Siao, C.J., Berno, A., Young, P., Sapolsky, R., Ghandour, G., Perkins, N., Winchester, E., Spencer, J., Kruglyak, L., Stein, L., Hsie, L., Topaloglou, T., Hubbell, E., Robinson, E., Mittmann, M., Morris, M.S., Shen, N., Kilburn, D., Rioux, J., Nusbaum, C., Rozen, S., Hudson, T.J. and Lander, E.S. 1998. Large-scale identification, mapping, and genotyping of single-nucleotide polymorphisms in the human genome. Science 280: 1077-1082.Google Scholar
  32. Weber, D. and Helentjaris, T. 1989. Mapping RFLP loci in maize using B-A translocations. Genetics 121: 583-590.Google Scholar
  33. Weber, S.R., Bureau, T.E. and White, S.E. 1995. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr. Opin. Genet. Dev. 5: 814-821.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Dinakar Bhattramakki
    • 1
  • Maureen Dolan
    • 2
  • Mike Hanafey
    • 2
  • Robin Wineland
    • 1
  • Dave Vaske
    • 1
  • James C. RegisterIII
    • 1
  • Scott V. Tingey
    • 2
  • Antoni Rafalski
    • 2
  1. 1.Pioneer Hi-Bred International Inc.JohnstonUSA
  2. 2.DuPont Agriculture and Nutrition, Molecular GeneticsNewarkUSA

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