How to start a LINE: 5' switching rejuvenates LINE retrotransposons in tobacco and related Nicotiana species

Abstract

In contrast to their conserved mammalian counterparts, plant long interspersed nuclear elements (LINEs) are highly variable, splitting into many low-copy families. Curiously, LINE families from the RTE clade retain a stronger sequence conservation and hence reach higher copy numbers. The cause of this RTE-typical property is not yet understood, but would help clarifying why some transposable elements are removed quickly whereas others persist in plant genomes. Here, we bring forward the first detailed study of RTE LINE structure, diversity and evolution in plants. For this, we argue that the Nightshade family is the ideal taxon to follow the evolutionary trajectories of RTE LINEs, given their high abundance, recent activity and partnership to non-autonomous elements. Using bioinformatic, cytogenetic and molecular approaches, we detect 4029 full-length RTE LINEs across the Solanaceae. We finely characterize and manually curate a core group of 458 full-length LINEs in allotetraploid tobacco, show amplification after polyploidization, and trace hybridization events by RTE LINE composition of parental genomes. Finally, we reveal the role of the untranslated regions (UTRs) as causes for the unique RTE LINE amplification and evolution pattern in plants: On one hand, we detect a highly conserved motif at the 3 UTR, suggesting strong selective constraints acting on the RTE terminus. On the other hand, we observed successive rounds of 5 UTR cycling, constantly rejuvenating the promoter sequences. This interplay between exchangeable promoters and conserved LINE bodies and 3 UTR likely allows RTE LINEs to persist and thrive in plant genomes.