Tracking the origin of two genetic components associated with transposable element bursts in domesticated rice

Abstract

Transposable elements (TEs) shape genome evolution through periodic bursts of amplification. In this study prior knowledge of the mPing/Ping/Pong TE family is exploited to track their copy numbers and distribution in genome sequences from 3,000 accessions of domesticated Oryza sativa (rice) and the wild progenitor Oryza rufipogon. We find that mPing bursts are restricted to recent domestication and is likely due to the accumulation of two TE components, Ping16A and Ping16A_Stow, that appear to be critical for mPing hyperactivity. Ping16A is a variant of the autonomous element with reduced activity as shown in a yeast transposition assay. Transposition of Ping16A into a Stowaway element generated Ping16A_Stow, the only Ping locus shared by all bursting accessions, and shown here to correlate with high mPing copies. Finally, we show that sustained activity of the mPing/Ping family in domesticated rice produced the components necessary for mPing bursts, not the loss of epigenetic regulation.

Benchmarking Transposable Element Annotation Methods for Creation of a Streamlined, Comprehensive Pipeline

“…We have benchmarked commonly applied programs for metrics including sensitivity, specificity, accuracy, and precision (Figure 1) and have implemented the optimal set of programs in a comprehensive pipeline called the Extensive de-novo TE Annotator (EDTA). To evaluate each program, we used a high-quality, manually curated library developed for the model species Oryza sativa (rice), which has a long history of TE discovery and annotation [23,34–42]. The reference library contains abundant class I and class II elements, making it optimal for testing currently available annotation programs.…”

Genomic diversity generated by a transposable element burst in a rice recombinant inbred population

“…This was of particular interest because, although all Ping elements are identical, one Ping locus has been implicated in initiating the bursts (9,15). Specifically, PingA_Stow on chromosome (called PingA in this study) was shown previously to be the only Ping shared by the four bursting accessions (9) and found preferentially in the genomes of rice accessions with higher than background mPing copies (15). Taken together, these correlative data suggest that the PingA locus differs from the other Ping loci, perhaps by catalyzing more transposition.…”

“…MITEs are the most abundant TE associated with the genes of higher plants where they populate noncoding regions (introns, 5' and 3' flanking sequences) and are a major contributor to allelic diversity (13,14). While most characterized rice accessions have 0 to 1 Ping and 1-50 mPings (15), the four accessions have 7-10 Pings, ~230-500 mPings, and up to ~40 new mPing insertions per plant/generation (7)(8)(9).…”

“…All available evidence indicates that bursts of both P elements and the Ping/mPing family occurred during the past century (9,17,18), however significant increases in mPing copy number is likely restricted to a few related accessions as no bursts were detected in over 3,000 sequenced rice accessions (15,19). This likely reflects the fact that unlike D. melanogaster, which is a wild species and an outcrosser, rice is a domesticated crop that propagates by selfor sib-pollination.…”

“…A close examination of the RILs with transposed Pings identified from 21 to 96 new mPing insertions including 4 to 60 heterozygous insertions that are likely to be new and provide evidence of recent activity (SupplementaryTable 3).In addition, of the 17 new Ping insertion sites, 14 are into euchromatic loci and 3 into heterochromatin (SupplementaryTable 3). Among this latter class (which is more likely to silence Ping), new mPing insertions vary from 63 (21 are heterozygous) to 67(15) to 111(15), again inconsistent with the loss of Ping…”