Transposable elements drive intron gain in diverse eukaryotes

Abstract

There is massive variation in intron numbers across eukaryotic genomes, yet the major drivers of intron content during evolution remain elusive. Rapid intron loss and gain in some lineages contrast with long-term evolutionary stasis in others. Episodic intron gain could be explained by recently discovered specialized transposons called Introners, but so far Introners are only known from a handful of species. Here, we performed a systematic search across 3,325 eukaryotic genomes and identified 27,563 Introner-derived introns in 175 genomes (5.2%). Species with Introners span remarkable phylogenetic diversity, from animals to basal protists, representing lineages whose last common ancestor dates to over 1.7 billion years ago. Aquatic organisms were 6.5 times more likely to contain Introners than terrestrial organisms. Introners exhibit mechanistic diversity but most are consistent with DNA transposition, indicating that Introners have evolved convergently hundreds of times from nonautonomous transposable elements. Transposable elements and aquatic taxa are associated with high rates of horizontal gene transfer, suggesting that this combination of factors may explain the punctuated and biased diversity of species containing Introners. More generally, our data suggest that Introners may explain the episodic nature of intron gain across the eukaryotic tree of life. These results illuminate the major source of ongoing intron creation in eukaryotic genomes.

The rubber tree kinome: Genome-wide characterization and insights into coexpression patterns associated with abiotic stress responses

“…We believe that the association of TEs, TDEs and specific PK subfamilies provides deeper insights into the role and maintenance of PKs for stress resilience. In addition to the genetic adaptation of the rubber tree, TEs have increasingly been attracting attention, mainly due to their association with (i) intron gain ( Gozashti et al., 2022 ); (ii) increased heterozygosity in stress-responsive genes ( De Kort et al., 2022 ); (iii) increases in gene expression variation ( Uzunović et al., 2019 ); and (iv) important polymorphisms associated with the genetic effects of complex traits( Vourlaki et al., 2022 ). These facts, together with the association of TDEs and stress responses, enabled the establishment of important PK subfamilies with high potential to be investigated for climate resilience.…”

Introns are derived from transposons

“…Their decline coincides with increases in the number of spliceosomal introns in both the large subunit (LSU) and small subunit (SSU) genes [19]. Introners appear to be a type of spliceosomal intron capable of rapid spread through genomes either by reverse splicing or transposition [5,11–13,20]. Although the link between DNA transposons and group I introns is more tenuous, both use endonucleases that target specific “homing” sites [21].…”

“…The fact that one strain of a species can carry an intron that is absent from another strain indicates that introns were mobile in the past and may still be mobilized, a property shared with mobile genetic elements (MGEs) that will be considered below. Although the origin of introns is enigmatic [5–8], they have been classified according to the way in which they are removed from gene transcripts (Fig 1).…”

The rubber tree kinome: genome-wide characterization and insights into coexpression patterns associated with abiotic stress responses

“…We believe that the association of TEs, TDEs and specific PK subfamilies provides deeper insights into the role and maintenance of PKs for stress resilience. In addition to the genetic adaptation of the rubber tree, TEs have increasingly been attracting attention, mainly due to their association with (i) intron gain (Gozashti et al, 2022); (ii) increased heterozygosity in stress-responsive genes (De Kort et al, 2022); (iii) increases in gene expression variation (Uzunović et al, 2019); and (iv) important polymorphisms associated with the genetic effects of complex traits(Vourlaki et al, 2022). These facts, together with the association of TDEs and stress responses, enabled the establishment of important PK subfamilies with high potential to be investigated for climate resilience.…”