A Genomic and Transcriptomic Analysis of Factors Driving lincRNA Diversification: Lessons from Plants

Transcriptomic analyses from across eukaryotes have led to the conclusion that most of the genome is transcribed at some point in the developmental trajectory of an organism. One class of these transcripts is termed long noncoding RNAs (lncRNAs). Recently, attention has focused on understanding the evolutionary dynamics of lncRNAs, particularly their conservation within genomes. Here we take an explicitly phylogenetic approach to uncover factors influencing lncRNA emergence and persistence, both of which can affect the diversification of lncRNA populations among species. For the first time in any group of organisms, we infer phylogeny for conserved lncRNAs and use gene tree / species tree reconciliation to examine their rates of duplication, tempo of evolution, and origins. Our analyses center on >12,000 intergenic lncRNAs (lincRNAs) in the plant family Brassicaceae, a model system for evolutionary inference. We find that Brassicaceae lincRNA populations are diversifying at a rate 4-5x faster than mammalian lincRNAs over similar evolutionary timeframes. Emergence of lincRNA loci appears to be linked to local duplication events, but surprisingly, not whole genome duplication events (WGD) or the activity of transposable elements. Interestingly, WGD events impact lincRNA diversification by accelerating loss of lincRNA loci. Compared to species-specific lincRNAs, evolutionarily conserved lincRNAs are more likely to be stress-responsive, contain miRNA binding motifs, and originate from a protein-coding locus, highlighting potential functional pathways for these lincRNAs. In sum, we provide insight into the processes influencing lincRNA diversification in eukaryotes, as well as inferring and refining lincRNA datasets across the Brassicaceae.