Gene capture by transposable elements leads to epigenetic conflict
2019
Plant transposable elements (TEs) regularly capture fragments of host genes. When the host employs siRNAs to silence these TEs, siRNAs homologous to the captured regions may target both the TEs and the genes, potentially leading to their silencing. This epigenetic cross-talk establishes an intragenomic conflict: silencing the TEs comes with the potential cost of silencing the genes. If the genes are important, however, natural selection will act to maintain function by moderating the silencing response. Such moderation may advantage the TEs. Here, we examined the potential for these epigenetic conflicts by focusing on three TE families in maize - Helitrons, Pack-MULEs and Sirevirus LTR retrotransposons. We documented 1,508 TEs with fragments captured from 2,019 donor genes and characterized the epigenetic profiles of both. Consistent with epigenetic conflict, donor genes mapped more siRNAs and were more methylated than 9free9 genes that had no evidence of exon capture. However, these patterns differed between syntelog vs. transposed donor genes. Syntelog genes appeared to maintain function, consistent with moderation of the epigenetic response for important genes before reaching a deleterious threshold, while transposed genes bore the signature of silencing and potential pseudogenization. Intriguingly, transposed genes were overrepresented among donor genes, suggesting a link between capture and gene movement. We also investigated the potential for TEs to gain an advantage. TEs with captured fragments were older, mapped fewer siRNAs and had lower levels of methylation than 9free9 TEs without gene fragments, but they showed no obvious evidence of increased copy numbers. Altogether, our results demonstrate that TE capture triggers an epigenetic conflict when genes are important, contrasting the loss of function for genes that are not under strong selective constraint. The evidence for an advantage to TEs is currently less obvious.
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