Long-term evolution of the S788 fungal nuclear small subunit rRNA group I introns

Abstract

More than 1000 group I introns have been identified in fungal rDNA. Little is known, however, of the splicing and secondary structure evolution of these ribozymes. Here, we use a combination of comparative and biochemical methods to address the evolution and splicing of a vertically inherited group I intron found at position 788 in the fungal small subunit (S) rRNA. The ancestral state of the S788 intron contains a highly conserved core and an extended P5 domain typical of IC1 introns. In contrast, the more derived introns have lost most of P5, and have an accelerated divergence rate within the core region with three functionally important substitutions that unambiguously separate them from the ancestral pool. Of 14 S788 group I introns that were tested for splicing, five, all of the ancestral type, were able to self-splice and produced intron RNA circles in vitro. The more derived S788 introns did not self-splice, and potentially rely on fungal-specific factors to facilitate splicing. In summary, we demonstrate one possible fate of vertically inherited group I introns, the loss of secondary structure elements, lessened selective constraints in the intron core, and ultimately, dependence on host-mediated splicing.

Occurrence and characteristics of group 1 introns found at three different positions within the 28S ribosomal RNA gene of the dematiaceous Phialophora verrucosa: phylogenetic and secondary structural implications

“…Loss of P5abcd domain in derived S788 introns was correlated with inability to self-splice in vitro in a previous report [19]. Accordingly, we have not confirmed insertion positions of intron-H by RT-PCR.…”

Site-specific reverse splicing of a HEG-containing group I intron in ribosomal RNA

“…Exactly how these differences can contribute to discrepancy in the observed reverse splicing outcome is unclear. Whatever the reasons are, our findings of reverse splicing into a single site that corresponds to the natural intron homing site correlate very well with numerous phylogenetic analyses that support horizontal group I intron transfers almost exclusively into the homologous site (3,21,22,28). We conclude that the observed distribution of rDNA group I introns among fungi and protists could be explained by a combination of two mobility mechanisms: ribozyme-dependent reverse splicing that results in intron integration into a homologous site in a new organism (horizontal intron transfer) and the homing endonuclease-dependent intron mobility mediating efficient unidirectional spread throughout the population.…”

Low Selection Pressure Aids the Evolution of Cooperative Ribozyme Mutations in Cells

“…The spliceosome, for example, appears to share a common ancestor with self-splicing group II intrions (14,15); RNase P evolved into RNA-protein particles with different sets of proteins in bacteria, archaea and eukarya (16); and group I introns appear to follow an evolutionary round of invasion, degeneration, and loss (17). The correlation of sequences for group I intron ribozymes that were vertically inherited over hundreds of millions of years has provided insight into their loss of secondary structure elements and the concomitant loss of splicing activity (18). The comparison of biological sequences, however, cannot recapitulate their evolution because the evolutionary parameters, and evolutionary intermediates, are lost to history.…”