Abstract
New miRNAs are evolutionarily important but their functional evolution remains unclear. Here we report that the evolution of a microRNA cluster, mir-972C rewires its downstream regulatory networks in Drosophila. Genomic analysis reveals that mir-972C originated in the common ancestor of Drosophila where it comprises six old miRNAs. It has subsequently recruited six new members in the melanogaster subgroup after evolving for at least 50 million years. Both the young and the old mir-972C members evolved rapidly in seed and non-seed regions. Combining target prediction and cell transfection experiments, we found that the seed and non-seed changes in individual mir-972C members cause extensive target divergence among D. melanogaster, D. simulans, and D. virilis, consistent with the functional evolution of mir-972C reported recently. Intriguingly, the target pool of the cluster as a whole remains relatively conserved. Our results suggest that clustering of young and old miRNAs broadens the target repertoires by acquiring new targets without losing many old ones. This may facilitate the establishment of new miRNAs in existing regulatory networks.
Highlights
Evolved genes constitute at least 10–20% of the genome in every taxonomic group (Khalturin et al, 2009; Kondo et al, 2017), and they play a significant role in the innovations of biological traits (Kaessmann, 2010; Chen et al, 2013)
Small RNA and mRNA testes deep-sequence libraries from D. melanogaster, D. simulans, D. pseudoobscura, and D. virilis (Czech et al, 2008; Rozhkov et al, 2010; Brown et al, 2014; Lyu et al, 2014; Ahmed-Braimah et al, 2017; Zhao et al, 2018) were retrieved from the GEO database (GEO accession IDs are listed in Supplementary Table S1)
We found homologous sequences in all the seven Drosophila genomes surveyed (D. simulans, D. yakuba, D. erecta, D. ananassae, D. pseudoobscura, D. mojavensis, and D. virilis), but failed to detect any homologs in the mosquito or the honey bee genomes
Summary
Evolved genes constitute at least 10–20% of the genome in every taxonomic group (Khalturin et al, 2009; Kondo et al, 2017), and they play a significant role in the innovations of biological traits (Kaessmann, 2010; Chen et al, 2013). Increasing evidence suggests that a large fraction of the new genes are functionally important (Kaessmann, 2010; McLysaght and Hurst, 2016; Kondo et al, 2017; Xia et al, 2021). They are primarily expressed in testes, and are often involved in reproductive functions including male fertility (Gubala et al, 2017; Kondo et al, 2017; Lange et al, 2021), sperm competition (Yeh et al, 2012), courtship (Dai et al, 2008), and pheromone metabolism (Zhang J. et al, 2004). Transcriptomic and protein-protein interaction studies suggest that the targets of some new genes changed dramatically even among closely related species (Chen et al, 2012; Ross et al, 2013), yet the underlying mechanisms are unclear
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