LAUSR

Significance Rice (Oryza sativa) has a unique combination of attributes that made it an ideal host to track the natural behavior of very active transposable elements (TEs) over generations. In this study, we have exploited its small genome and propagation by self or sibling pollination to identify and characterize two strain pairs, EG4/HEG4 and A119/A123, undergoing bursts of the nonautonomous miniature inverted repeat transposable element mPing. Comparative sequence analyses of these strains have advanced our understanding of (i) factors that contribute to sustaining a TE burst for decades, (ii) features that distinguish a natural TE burst from bursts in cell culture or mutant backgrounds, and (iii) the extent to which TEs can rapidly diversify the genome of an inbred organism. To understand the success strategies of transposable elements (TEs) that attain high copy numbers, we analyzed two pairs of rice (Oryza sativa) strains, EG4/HEG4 and A119/A123, undergoing decades of rapid amplification (bursts) of the class 2 autonomous Ping element and the nonautonomous miniature inverted repeat transposable element (MITE) mPing. Comparative analyses of whole-genome sequences of the two strain pairs validated that each pair has been maintained for decades as inbreds since divergence from their respective last common ancestor. Strains EG4 and HEG4 differ by fewer than 160 SNPs and a total of 264 new mPing insertions. Similarly, strains A119 and A123 exhibited about half as many SNPs (277) as new mPing insertions (518). Examination of all other potentially active TEs in these genomes revealed only a single new insertion out of ∼40,000 loci surveyed. The virtual absence of any new TE insertions in these strains outside the mPing bursts demonstrates that the Ping/mPing family gradually attains high copy numbers by maintaining activity and evading host detection for dozens of generations. Evasion is possible because host recognition of mPing sequences appears to have no impact on initiation or maintenance of the burst. Ping is actively transcribed, and both Ping and mPing can transpose despite methylation of terminal sequences. This finding suggests that an important feature of MITE success is that host recognition does not lead to the silencing of the source of transposase.