LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss

Abstract

Background: LTR retrotransposons are one of the main causes for plant genome size and structure evolution, along with polyploidy. The characterization of their amplification and subsequent elimination of the genomes is therefore a major goal in plant evolutionary genomics. To address the extent and timing of these forces, we performed a detailed analysis of 41 LTR retrotransposon families in rice.

Results: Using a new method to estimate the insertion date of both truncated and complete copies, we estimated these two forces more accurately than previous studies based on other methods. We show that LTR retrotransposons have undergone bursts of amplification within the past 5 My. These bursts vary both in date and copy number among families, revealing that each family has a particular amplification history. The number of solo LTR varies among families and seems to correlate with LTR size, suggesting that solo LTR formation is a family-dependent process. The deletion rate estimate leads to the prediction that the half-life of LTR retrotransposon sequences evolving neutrally is about 19 My in rice, suggesting that other processes than the formation of small deletions are prevalent in rice DNA removal.

Conclusion: Our work provides insights into the dynamics of LTR retrotransposons in the rice genome. We show that transposable element families have distinct amplification patterns, and that the turn-over of LTR retrotransposons sequences is rapid in the rice genome.

Figure 1

New method to estimate the insertion date of truncated copies. When a burst of amplification occurs, all the copies deriving from one master copy insert approximately at the same time. Upon insertion, all the new copies are identical in sequence as well as the two LTRs of each copy, leading to a null divergence between copies (Div = 0) and between the two LTRs of each copy (Div_LTRs = 0). Over time, all sequences evolve at the same rate, so both the divergence between two copies and the divergence between the two LTRs of one copy are equal at a given time. Hence, if the nucleotide divergence between a truncated copy and a copy with two LTRs ("2 LTRs" copy) is equal to the nucleotide divergence between the two LTRs of the "2 LTRs" copy, the two copies originated from the same burst of amplification and the insertion date estimated for the "2 LTRs" copy can be used as an approximation of the insertion date of the truncated one.

Figure 2

Histogram of the copy number by date of insertion for 10 LTR retrotransposon families. The LTR divergence is an estimate of the insertion date of the copies, each time scale corresponding to a LTR divergence of 0.01 (0.385 My). For complete copies, ("2 LTRs") this divergence corresponds to the divergence between the two LTRs. For truncated copies (Internal Region [IR], LTR, and LTR-Internal region [LTR-IR]), the divergence is derived from the "2 LTRs" copies (see Materials and Methods and Figure 1).

Figure 3

Relationship between divergence and deletion number per nucleotide. The slope corresponding to the maximum likelihood estimate of the deletion rate relative to substitutions (0.094) is represented in red.