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The paleontology of intergene retrotransposons of maize

Nature Genetics volume 20, pages 43–45 (1998)Cite this article

Abstract

Retrotransposons, transposable elements related to animal retroviruses, are found in all eukaryotes investigated and make up the majority of many plant genomes1,2,3,4,5. Their ubiquity points to their importance, especially in their contribution to the large-scale structure of complex genomes. The nature and frequency of retro-element appearance, activation and amplification are poorly understood in all higher eukaryotes. Here we employ a novel approach to determine the insertion dates for 17 of 23 retrotransposons found near the maize adh1 gene, and two others from unlinked sites in the maize genome, by comparison of long terminal repeat (LTR) divergences with the sequence divergence between adh1 in maize and sorghum. All retrotransposons examined have inserted within the last six million years, most in the last three million years. The structure of the adh1 region appears to be standard relative to the other gene-containing regions of the maize genome, thus suggesting that retrotransposon insertions have increased the size of the maize genome from approximately 1200 Mb to 2400 Mb in the last three million years. Furthermore, the results indicate an increased mutation rate in retrotransposons compared with genes.

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Figure 1: Spatial arrangement of maize adh1-F region retrotransposons.
Figure 2: Temporal arrangement of maize adh1-F region retrotransposons.

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References

  1. Flavell, A.J. et al. Ty1-copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucleic Acids Res. 20, 3639–3644 (1992).

    Article  CAS  Google Scholar 

  2. Grandbastien, M.A. Retroelements in higher plants. Trends Genet. 8, 103–108 (1992).

    Article  CAS  Google Scholar 

  3. Voytas, D.F. et al. copia-like retrotransposons are ubiquitous among plants. Proc. Natl Acad. Sci. USA 89, 7124– 7128 (1992).

    Article  CAS  Google Scholar 

  4. Bennetzen, J.L. The contributions of retroelements to plant genome organization, function and evolution. Trends Microbiol. 4, 347– 353 (1996).

    Article  CAS  Google Scholar 

  5. SanMiguel, P. et al. Nested retrotransposons in the intergenic regions of the maize genome. Science 274, 765– 768 (1996).

    Article  CAS  Google Scholar 

  6. Lewin B. Genes VI. 603–604 (Oxford University Press, New York, 1997).

    Google Scholar 

  7. Gaut, B.S., Morton, B.R., McCaig, B.C. & Clegg, M.T. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc. Natl Acad. Sci. USA 93, 10274–10279 (1996).

    Article  CAS  Google Scholar 

  8. Gaut, B.S. & Doebley, J.F. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc. Natl Acad. Sci. USA 94, 6809–6814 ( 1997).

    Article  CAS  Google Scholar 

  9. Johns, M.A., Strommer, J.N. & Freeling, M. Exceptionally high levels of restriction site polymorphism in DNA near the maize Adh1 gene. Genetics 105 , 733–743 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Avramova, Z. et al. Gene identification in a complex chromosomal continuum by local genomic cross-referencing. Plant J. 10, 1163–1168 (1996).

    Article  CAS  Google Scholar 

  11. Dooner, H.K. & Martinezferez, I.M. Recombination occurs uniformly within the bronze gene, a meiotic recombination hotspot in the maize genome. Plant Cell 9, 1633– 1646 (1997).

    Article  CAS  Google Scholar 

  12. Gaut, B.S. & Clegg, M.T. Molecular evolution of the Adh1 locus in the genus Zea. Proc. Natl Acad. Sci. USA. 90, 5095–5099 ( 1993).

    Article  CAS  Google Scholar 

  13. Hu, W.S. & Temin, H.M. Genetic consequences of packaging two RNA genomes in one retroviral particle: pseudodiploidy and high rate of genetic recombination. Proc. Natl Acad. Sci. USA 87 , 1556–1560 (1990).

    Article  CAS  Google Scholar 

  14. Bennetzen, J.L. et al. Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome 37, 565–576 (1994).

    Article  CAS  Google Scholar 

  15. Coulondre, C., Miller, J.H., Farabaugh, P.J. & Gilbert, W. Molecular basis of base substitution hotspots in Escherichia coli. Nature 274, 775–780 (1978).

    Article  CAS  Google Scholar 

  16. Gruenbaum, Y., Navey-Many, T., Cedar, H. & Razin, A. Sequence specificity of methylation in higher plant DNA. Nature 292, 860–862 ( 1981).

    Article  CAS  Google Scholar 

  17. Selker, E.U. & Stevens, J.N. DNA methylation at asymmetric sites is associated with numerous transition mutations. Proc. Natl Acad. Sci. USA 82, 8114–8118 (1985).

    Article  CAS  Google Scholar 

  18. Yoder, J.A. & Bestor, T.H. Genetic analysis of genomic methylation patterns in plants and mammals. Biol. Chem. 377, 605–610 (1996).

    CAS  PubMed  Google Scholar 

  19. Jin, Y.K. & Bennetzen, J.L. Structure and coding properties of Bs1, a maize retrovirus-like transposon. Proc. Natl Acad. Sci. USA 86, 6235–6239 ( 1989).

    Article  CAS  Google Scholar 

  20. White, S.E., Habera, L.F. & Wessler, S.R. Retrotransposons in the flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and expression. Proc. Natl Acad. Sci. USA 91, 11792–11796 (1994).

    Article  CAS  Google Scholar 

  21. Turcich, M.P. et al. PREM-2, a copia-type retroelement in maize is expressed preferentially in early microspores. Sex. Plant Reprod. 9, 65–74 (1996).

    Article  Google Scholar 

  22. Hu, W., Das, O.P. & Messing, J. Zeon-1, a member of a new maize retrotransposon family. Mol. Gen. Genet. 248, 471– 480 (1995).

    Article  CAS  Google Scholar 

  23. Flavell, R.B., Bennett, M.D., Smith, J.B. & Smith, D.B. Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochemical Genetics 12, 257– 269 (1974).

    Article  CAS  Google Scholar 

  24. Devereux, J., Haeberli, P. & Smithies, O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12, 387– 395 (1984).

    Article  CAS  Google Scholar 

  25. Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120 (1980).

    Article  CAS  Google Scholar 

  26. Yang, Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555–556 (1997).

    CAS  PubMed  Google Scholar 

  27. Kumar, S., Tamura, K. & Nei, M. MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput. Appl. Biosci. 10, 189– 191 (1994).

    CAS  PubMed  Google Scholar 

  28. Nei, M. & Gojobori, T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418–426 (1986).

    CAS  PubMed  Google Scholar 

  29. Gaut, B.S. & Weir, B.S. Detecting substitution-rate heterogeneity among regions of a nucleotide sequence. Mol. Biol. Evol. 11, 620–629 (1994).

    CAS  PubMed  Google Scholar 

  30. Sokal, R.R. & Rohlf, F.J. Biometry. (Freeman, New York, 1995).

    Google Scholar 

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Acknowledgements

We thank S. Frank and S. Subramanian for technical assistance and Z. Avramova for useful discussions. This work was supported by grants from the USDA to J.L.B. and B.S.G.

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Authors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, 47907-1392, Indiana, USA

    Phillip SanMiguel, Alexander Tikhonov, Yuko Nakajima & Jeffrey L. Bennetzen

  2. Genetics Program, Purdue University, West Lafayette, 47907-1392, Indiana, USA

    Phillip SanMiguel & Jeffrey L. Bennetzen

  3. Department of Ecology and Evolutionary Biology, University of California, Irvine, 92697-2525 , California, USA

    Brandon S. Gaut

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  1. Phillip SanMiguel
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  5. Jeffrey L. Bennetzen
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Correspondence to Jeffrey L. Bennetzen.

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SanMiguel, P., Gaut, B., Tikhonov, A. et al. The paleontology of intergene retrotransposons of maize. Nat Genet 20, 43–45 (1998). https://doi.org/10.1038/1695

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