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Pack-MULE transposable elements mediate gene evolution in plants

Abstract

Mutator-like transposable elements (MULEs) are found in many eukaryotic genomes and are especially prevalent in higher plants1,2,3. In maize, rice and Arabidopsis a few MULEs were shown to carry fragments of cellular genes4,5,6. These chimaeric elements are called Pack-MULEs in this study. The abundance of MULEs in rice and the availability of most of the genome sequence permitted a systematic analysis of the prevalence and nature of Pack-MULEs in an entire genome. Here we report that there are over 3,000 Pack-MULEs in rice containing fragments derived from more than 1,000 cellular genes. Pack-MULEs frequently contain fragments from multiple chromosomal loci that are fused to form new open reading frames, some of which are expressed as chimaeric transcripts. About 5% of the Pack-MULEs are represented in collections of complementary DNA. Functional analysis of amino acid sequences and proteomic data indicate that some captured gene fragments might be functional. Comparison of the cellular genes and Pack-MULE counterparts indicates that fragments of genomic DNA have been captured, rearranged and amplified over millions of years. Given the abundance of Pack-MULEs in rice and the widespread occurrence of MULEs in all characterized plant genomes, gene fragment acquisition by Pack-MULEs might represent an important new mechanism for the evolution of genes in higher plants.

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Figure 1: Pack-MULEs in Nipponbare.
Figure 2: Distribution of Pack-MULEs on chromosomes 1 and 10.
Figure 3: Structure and genomic origin of chimaeric Pack-MULEs.

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Acknowledgements

We thank I. K. Jordan and E. K. Kentner for assistance with Ka/Ks analysis, R. Liu for verification of TSD sequences, C. Feschotte for advice, and J. Bennetzen and E. Pritham for critical reading of the manuscript. This study was supported by a grant from the NSF Plant Genome Program to S.R.W. and S.R.E. N.J., X.Z. and S.R.W. were also supported in part by grants from the NIH, and Z.B. and S.R.E. were also supported in part by grants from the NIH, the Howard Hughes Medical Institute, and Alvin Goldfarb.

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Correspondence to Susan R. Wessler.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Methods

Detailed description of methods including identification of MULEs from rice genomic sequence, the PCR amplification of Pack-MULE fragments from Nipponbare genomic DNA, and control experiment for Ka/Ks analysis. (DOC 33 kb)

Supplementary Table 1

TIR sequences of 62 MULE families that were involved in the formation of Pack-MULEs. Sequences in fasta format were also provided. (DOC 137 kb)

Supplementary Table 2

The TSDs of 100 randomly chosen Pack-MULEs from the genome-wide search. (XLS 47 kb)

Supplementary Table 3

The 320 Pack-MULEs on rice chromosome 1. Their position in relevant genomic sequence, the TSD sequences, their size, and a short description of the relevant protein hit for each Pack-MULE. (DOC 218 kb)

Supplementary Table 4

The 156 Pack-MULEs on rice chromosome 10. See Supplementary Table 3. (XLS 100 kb)

Supplementary Table 5

Multi-copy Pack-MULEs and their TSDs on rice chromosomes 1 and 10. (XLS 101 kb)

Supplementary Table 6

Pack-MULEs and their genomic homologs. The 100 randomly chosen Pack-MULEs and the gene structure of their genomic homologs. The size of the acquired fragment and the similarity between Pack-MULE and their genomic counterparts. (XLS 72 kb)

Supplementary Table 7

PCR primers and amplified fragments for 13 Pack-MULEs. The detailed information about primers and PCR conditions used to amplify Pack-MULE fragments (3 Pack-MULEs described in Figure 3, and 10 randomly selected Pack-MULEs from the 100 Pack-MULEs on chromosomes 1 and 10). The expected and observed fragment sizes were also provided. (XLS 64 kb)

Supplementary Table 8

25 Pack-MULEs with cDNA matches from chromosomes 1 and 10. The 34 full cDNA clones that correspond to 25 Pack-MULEs from chromosomes 1 and 10, and their transcription initiation sites inside Pack-MULEs. (XLS 19 kb)

Supplementary Table 9

Pack-MULEs with peptide matches. The genomic position of the relevant Pack-MULEs, the sequence of the peptides involved, and the tissue where each peptide was detected. (XLS 20 kb)

Supplementary Table 10

Ka/Ks analysis for Pack-MULEs and their genomic copies. The gene structure of the genomic copy, the regions involved in the analysis, the Ka and Ks value and the p value of purifying selection test. (XLS 23 kb)

Supplementary Figure 1

Genomic origin of Pack-MULE gene fragments. (DOC 94 kb)

Supplementary Figure 2

Amplification of Pack-MULE fragments using Nipponbare genomic DNA. (DOC 77 kb)

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Jiang, N., Bao, Z., Zhang, X. et al. Pack-MULE transposable elements mediate gene evolution in plants. Nature 431, 569–573 (2004). https://doi.org/10.1038/nature02953

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