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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.

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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.

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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.

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Correspondence to Michele Morgante.

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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)

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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

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