Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize

Abstract

We report a whole-genome comparison of gene content in allelic BAC contigs from two maize inbred lines. Genic content polymorphisms involve as many as 10,000 sequences and are mainly generated by DNA insertions. The termini of eight of the nine genic insertions that we analyzed shared the structural hallmarks of helitron rolling-circle transposons1,2,3. DNA segments defined by helitron termini contained multiple gene-derived fragments and had a structure typical of nonautonomous helitron-like transposons. Closely related insertions were found in multiple genomic locations. Some of these produced transcripts containing segments of different genes, supporting the idea that these transposition events have a role in exon shuffling and the evolution of new proteins. We identified putative autonomous helitron elements and found evidence for their transcription. Helitrons in maize seem to continually produce new nonautonomous elements responsible for the duplicative insertion of gene segments into new locations and for the unprecedented genic diversity. The maize genome is in constant flux, as transposable elements continue to change both the genic and nongenic fractions of the genome, profoundly affecting genetic diversity.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Genome analysis of nonshared genic regions in maize.
Figure 2: Sequence features of gene fragment–containing polymorphic insertions in five genomic regions of maize.
Figure 3: Two helitron-like insertions in the bronze1 region4,6 are responsible for the observed genic differences.

References

  1. Kapitonov, V.V. & Jurka, J. Rolling-circle transposons in eukaryotes. Proc. Natl. Acad. Sci. USA 98, 8714–8719 (2001).

    Article  CAS  Google Scholar 

  2. Poulter, R.T., Goodwin, T.J. & Butler, M.I. Vertebrate helentrons and other novel Helitrons . Gene 313, 201–212 (2003).

    Article  CAS  Google Scholar 

  3. Lal, S.K., Giroux, M.J., Brendel, V., Vallejos, C.E. & Hannah, L.C. The maize genome contains a helitron insertion. Plant Cell 15, 381–391 (2003).

    Article  CAS  Google Scholar 

  4. Fu, H. & Dooner, H.K. Intraspecific violation of genetic colinearity and its implications in maize. Proc. Natl. Acad. Sci. USA 99, 9573–9578 (2002).

    Article  CAS  Google Scholar 

  5. Song, R. & Messing, J. Gene expression of a gene family in maize based on noncollinear haplotypes. Proc. Natl. Acad. Sci. USA 100, 9055–9060 (2003).

    Article  CAS  Google Scholar 

  6. Brunner, S., Fengler, K., Morgante, M., Tingey, S. & Rafalski, A. Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17, 343–360 (2005).

    Article  CAS  Google Scholar 

  7. Meyers, B.C., Scalabrin, S. & Morgante, M. Mapping and sequencing complex genomes: let's get physical! Nat. Rev. Genet. 5, 578–588 (2004).

    Article  CAS  Google Scholar 

  8. Gardiner, J. et al. Anchoring 9,371 maize expressed sequence tagged unigenes to the bacterial artificial chromosome contig map by two-dimensional overgo hybridization. Plant Physiol. 134, 1317–1326 (2004).

    Article  Google Scholar 

  9. Bennetzen, J.L., Coleman, C., Liu, R., Ma, J. & Ramakrishna, W. Consistent over-estimation of gene number in complex plant genomes. Curr. Opin. Plant Biol. 7, 732–736 (2004).

    Article  CAS  Google Scholar 

  10. Palmer, L.E. et al. Maize genome sequencing by methylation filtration. Science 302, 2115–2117 (2003).

    Article  Google Scholar 

  11. Messing, J. et al. Sequence composition and genome organization of maize. Proc. Natl Acad. Sci. USA 101, 14349–14354 (2004).

    Article  CAS  Google Scholar 

  12. Ramakrishna, W., Emberton, J., Ogden, M., SanMiguel, P. & Bennetzen, J.L. Structural analysis of the maize rp1 complex reveals numerous sites and unexpected mechanisms of local rearrangement. Plant Cell 14, 3213–3223 (2002).

    Article  CAS  Google Scholar 

  13. Craig, N.L., Craigie, R., Gellert, M. & Lambowitz, A.M. Mobile DNA II (American Society of Microbiology Press, Washington, DC, 2002).

    Book  Google Scholar 

  14. Gupta, S., Gallavotti, A., Stryker, G.A., Schmidt, R.J. & Lal, S.K. A novel class of Helitron-related transposable elements in maize contains portions of multiple pseudogenes. Plant Mol. Biol. 57, 115–127 (2005).

    Article  CAS  Google Scholar 

  15. Feschotte, C. & Wessler, S.R. Treasures in the attic: rolling circle transposons discovered in eukaryotic genomes. Proc. Natl. Acad. Sci. USA 98, 8923–8924 (2001).

    Article  CAS  Google Scholar 

  16. Kynast, R.G. et al. A complete set of maize individual chromosome additions to the oat genome. Plant Physiol. 125, 1216–1227 (2001).

    Article  CAS  Google Scholar 

  17. Okagaki, R.J. et al. Mapping maize sequences to chromosomes using oat-maize chromosome addition materials. Plant Physiol. 125, 1228–1235 (2001).

    Article  CAS  Google Scholar 

  18. Song, R., Llaca, V. & Messing, J. Mosaic organization of orthologous sequences in grass genomes. Genome Res. 12, 1549–1555 (2002).

    Article  CAS  Google Scholar 

  19. Lai, J. et al. Gene loss and movement in the maize genome. Genome Res. 14, 1924–1931 (2004).

    Article  CAS  Google Scholar 

  20. Swigonova, Z., Bennetzen, J.L. & Messing, J. Structure and evolution of the r/b chromosomal regions in rice, maize, and sorghum. Genetics 169, 891–906 (2005).

    Article  CAS  Google Scholar 

  21. Ilic, K., SanMiguel, P.J. & Bennetzen, J.L. A complex history of rearrangement in an orthologous region of the maize, sorghum, and rice genomes. Proc. Natl. Acad. Sci. USA 100, 12265–12270 (2003).

    Article  CAS  Google Scholar 

  22. Hamilton, A.J. & Baulcombe, D.C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950–952 (1999).

    Article  CAS  Google Scholar 

  23. van der Krol, A.R., Mur, L.A., Beld, M., Mol, J.N. & Stuitje, A.R. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2, 291–299 (1990).

    Article  CAS  Google Scholar 

  24. Duvick, D.N. Biotechnology in the 1930s: the development of hybrid maize. Nat. Rev. Genet. 2, 69–74 (2001).

    Article  CAS  Google Scholar 

  25. Birchler, J.A., Auger, D.L. & Riddle, N.C. In search of the molecular basis of heterosis. Plant Cell 15, 2236–2239 (2003).

    Article  CAS  Google Scholar 

  26. Jiang, N., Bao, Z., Zhang, X., Eddy, S.R. & Wessler, S.R. Pack-MULE transposable elements mediate gene evolution in plants. Nature 431, 569–573 (2004).

    Article  CAS  Google Scholar 

  27. Yu, Z., Wright, S.I. & Bureau, T.E. Mutator-like elements in Arabidopsis thaliana. Structure, diversity and evolution. Genetics 156, 2019–2031 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Le, Q.H., Wright, S., Yu, Z. & Bureau, T. Transposon diversity in Arabidopsis thaliana . Proc. Natl. Acad. Sci. USA 97, 7376–7381 (2000).

    Article  CAS  Google Scholar 

  29. Lai, J., Li, Y., Messing, J. & Dooner, H.K. Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc. Natl. Acad. Sci. USA 102, 9068–9073 (2005).

    Article  CAS  Google Scholar 

  30. Meyers, B.C., Tingey, S.V. & Morgante, M. Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res. 11, 1660–1676 (2001).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank F. Salamini and S. Tingey for critical reading of the manuscript and Y. Zhang for writing the script used for the overgo probe comparison in the two physical maps. M.M. is supported by a DuPont Young Professor Grant. This research is partly supported by an Italian Ministry of University and Research, PRIN projects grant to M.M.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michele Morgante.

Ethics declarations

Competing interests

S.B., K.F. and A.R. are employed by DuPont and may be viewed as potentially gaining or losing financially through publication. M.M. owns shares in DuPont.

Supplementary information

Supplementary Fig. 1

Structure of two maize autonomous helitron elements. (PDF 97 kb)

Supplementary Fig. 2

PCR amplification targeting non shared (present in B73 and not in Mo17) genic fragments identified within helitron-like elements. (PDF 139 kb)

Supplementary Fig. 3

Expression analysis by RT-PCR targeting non shared (present in B73 and not in Mo17) genic fragments identified within helitron-like elements. (PDF 499 kb)

Supplementary Table 1

Maize sequences with homology to proteins encoded by autonomous helitron elements. (PDF 106 kb)

Supplementary Table 2

Organization and genomic location of the non-shared genic clusters at loci 9002, 9008 and 9009. (PDF 64 kb)

Supplementary Table 3

Location of primers used for PCR and RT-PCR analysis on genic clusters and structure of non shared genic clusters. (PDF 66 kb)

Supplementary Table 4

Additional maize helitron non autonomous elements identified in the nr section of GenBank. (PDF 97 kb)

Supplementary Table 5

List of PCR primer pairs. (PDF 78 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Morgante, M., Brunner, S., Pea, G. et al. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37, 997–1002 (2005). https://doi.org/10.1038/ng1615

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng1615

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing