Regulatory features determine the evolutionary fate of laterally acquired genes in plants

Lateral gene transfer (LGT) is widespread in eukaryotes, including in animals and plants where it can fuel adaptive evolution and innovation. However, the factors that influence the integration and long-term retention of transferred genes remain poorly understood. The pangenome of the grass Alloteropsis has a high turnover of laterally acquired genes, and here we combine expression, methylation and genomic data to identify factors promoting their long-term persistence. Most transferred genes appear to be degenerating, showing lower expression levels and/or greater sequence truncation compared to their vertically inherited homologs. These degenerating genes also show significantly higher levels of DNA methylation, potentially indicating transcriptional silencing. The likelihood of a transferred gene being retained will be influenced by how easily it can be expressed in the recipient genome. In Alloteropsis, putatively functional laterally acquired genes had expression levels significantly more similar to their donor xenolog than to their vertically inherited homolog. This pattern suggests that transferred genes may carry cis-regulatory elements encoded on the fragment of DNA that moves between species, facilitating their expression in the new genomic context. Evolutionary novelty may also increase the likelihood that selection retains a transferred gene. However, only a significant difference in expression level, not sequence divergence, between donor and recipient orthologs is associated with successful lateral gene transfer. Overall, our results show that most transferred genes degrade over time. However, those capable of regulating their own expression are more likely to persist and contribute to long-term evolutionary innovation.

Significance Statement Lateral gene transfer (LGT) can introduce novel traits into plant genomes, yet most transferred genes are only transient residents and are degenerating, with reduced expression, truncation, and elevated DNA methylation. However, a minority persist and are more likely to resemble their donor counterparts in expression, suggesting co-transfer of cis-regulatory elements. These findings indicate that regulatory compatibility is key to their long-term survival.