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Unexpected consequences of a sudden and massive transposon amplification on rice gene expression

Abstract

High-copy-number transposable elements comprise the majority of eukaryotic genomes where they are major contributors to gene and genome evolution1. However, it remains unclear how a host genome can survive a rapid burst of hundreds or thousands of insertions because such bursts are exceedingly rare in nature and therefore difficult to observe in real time2. In a previous study we reported that in a few rice strains the DNA transposon mPing was increasing its copy number by 40 per plant per generation3. Here we exploit the completely sequenced rice genome to determine 1,664 insertion sites using high-throughput sequencing of 24 individual rice plants and assess the impact of insertion on the expression of 710 genes by comparative microarray analysis. We find that the vast majority of transposable element insertions either upregulate or have no detectable effect on gene transcription. This modest impact reflects a surprising avoidance of exon insertions by mPing and a preference for insertion into 5′ flanking sequences of genes. Furthermore, we document the generation of new regulatory networks by a subset of mPing insertions that render adjacent genes stress inducible. As such, this study provides evidence for models first proposed previously4,5,6 for the involvement of transposable elements and other repetitive sequences in genome restructuring and gene regulation.

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Figure 1: Distribution of mPing insertions in strain EG4.
Figure 2: Impact of mPing -containing alleles on host transcription.
Figure 3: Cold inducibility of a transgene in Arabidopsis containing the Ping ORF1 promoter fused to GUS.
Figure 4: Stress-induction of transcription of alleles harbouring mPing.

Accession codes

Primary accessions

Gene Expression Omnibus

Data deposits

Sequence data has been submitted to GEO under accession number GSE15021.

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Acknowledgements

We thank the Rice Genome Resource Center for the use of the rice microarray system and Y. Nagamura and R. Motoyama for technical support; the GenBank project of the National Institute of Agrobiological Science in Japan for providing seeds of Gimbozu landraces (A123 and A157); and X. Zhang and C. Feschotte for critical discussions and reading of the manuscript. S.R.W. is funded by a NSF Plant Genome grant and the University of Georgia Research Foundation and T.Tanisaka by the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Author Contributions K.N. and F.Z. performed 454 sequencing and analysed the data. A.O.R. provided statistical analyses. T.Tsukiyama and Y.O. performed microarray, and K.N. and H.S. analysed the data. C.N.H. performed Arabidopsis transformation. K.N. performed stress treatment and real-time PCR. K.N., F.Z., T.Tanisaka and S.R.W. contributed the experimental design and wrote the paper.

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Correspondence to Takatoshi Tanisaka or Susan R. Wessler.

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Naito, K., Zhang, F., Tsukiyama, T. et al. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461, 1130–1134 (2009). https://doi.org/10.1038/nature08479

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