Elimination of a Retrotransposon for Quenching Genome Instability in Modern Rice

Transposable elements (TEs) constitute the most abundant portions of plant genomes and can dramatically shape host genomes during plant evolution. They also play important roles in crop domestication. However, whether TEs themselves are also selected during crop domestication has remained unknown. Here, we identify an active long terminal repeat (LTR) retrotransposon, HUO, as a potential target of selection during rice domestication and breeding. HUO is a low-copy-number LTR retrotransposon, and is active under natural growth conditions and transmitted through male gametogenesis, preferentially inserting into genomic regions capable of transcription. HUO exists in all wild rice accessions and about half of the archaeological rice grains (1200-7000 years ago) and landraces surveyed, but is absent in almost all modern varieties, indicating its gradual elimination during rice domestication and breeding. Further analyses showed that HUO is subjected to strict gene silencing through the RNA-directed DNA methylation pathway. Our results also suggest that multiple HUO copies may trigger genomic instability through altering genome-wide DNA methylation and small RNA biogenesis and changing global gene expression, resulting in decreased disease resistance and yield, coinciding with its elimination during rice breeding. Together, our study suggests that negative selection of an active retrotransposon might be important for genome stability during crop domestication and breeding.