Internally Symmetrical Stwintrons and Related Canonical Introns in Hypoxylaceae Species

Abstract

Spliceosomal introns are pervasive in eukaryotes. Intron gains and losses have occurred throughout evolution, but the origin of new introns is unclear. Stwintrons are complex intervening sequences where one of the sequence elements (5′-donor, lariat branch point element or 3′-acceptor) necessary for excision of a U2 intron (external intron) is itself interrupted by a second (internal) U2 intron. In Hypoxylaceae, a family of endophytic fungi, we uncovered scores of donor-disrupted stwintrons with striking sequence similarity among themselves and also with canonical introns. Intron–exon structure comparisons suggest that these stwintrons have proliferated within diverging taxa but also give rise to proliferating canonical introns in some genomes. The proliferated (stw)introns have integrated seamlessly at novel gene positions. The recently proliferated (stw)introns appear to originate from a conserved ancestral stwintron characterised by terminal inverted repeats (45–55 nucleotides), a highly symmetrical structure that may allow the formation of a double-stranded intron RNA molecule. No short tandem duplications flank the putatively inserted intervening sequences, which excludes a DNA transposition-based mechanism of proliferation. It is tempting to suggest that this highly symmetrical structure may have a role in intron proliferation by (an)other mechanism(s).

Transposable elements drive intron gain in diverse eukaryotes

“…Some algal Introners appear to be MITE TEs based on observation of target site duplications (TSDs), terminal inverted repeats (TIRs), and biased insertion into nucleosome linker regions ( 12 ). In contrast, fungal Introners lack TSDs and TIRs and are highly biased towards gene regions (insertion into nucleosome linkers was not studied), and have been interpreted as novel RNA-based elements that propagate through reverse-splicing of RNA copies of spliced Introners ( 14, 16 ).…”

“…Introners have only been described in 5 eukaryotic lineages, and even among these cases, the precise molecular mechanisms remain obscure. Some Introner families show clear signatures of DNA TEs (12,15) while others may be novel RNA-propagated elements (14,16).…”

“…Introners have only been described in 5 eukaryotic lineages, and even among these cases, the precise molecular mechanisms remain obscure. Some Introner families show clear signatures of DNA TEs ( 12, 15 ) while others may be novel RNA-propagated elements ( 14, 16 ). More importantly, determining the extent to which introners are a primary source of ongoing intron gain is essential for interpreting the evolution of genome structure and function, and requires a broad survey that spans the eukaryotic tree of life.…”

“…In addition to these ad hoc intron creation mechanisms, the intron-generating transposable elements (TEs) known as Introners represent a mechanism that could explain the high and episodic frequency and genome-wide scale of intron gains observed across eukaryotic lineages. These poorly understood TEs create introns de novo through insertion into exons (12)(13)(14)(15)(16)(17). Introners have only been described in 5 eukaryotic lineages, and even among these cases, the precise molecular mechanisms remain obscure.…”

Transposable elements drive intron gain in diverse eukaryotes

“…In addition to these ad hoc intron creation mechanisms, the intron-generating transposable elements (TEs) known as Introners represent a mechanism that could explain the high and episodic frequency and genome-wide scale of intron gains observed across eukaryotic lineages. These poorly understood TEs create introns de novo through insertion into exons ( 12 – 17 ). Introners have only been described in five eukaryotic lineages, and even among these cases, the precise molecular mechanisms remain obscure.…”