A new Drosophila spliceosomal intron position is common in plants

Abstract

The 25-year-old debate about the origin of introns between proponents of ''introns early'' and ''introns late'' has yielded significant advances, yet important questions remain to be ascertained. One question concerns the density of introns in the last common ancestor of the three multicellular kingdoms. Approaches to this issue thus far have relied on counts of the numbers of identical intron positions across present-day taxa on the assumption that the introns at those sites are orthologous. However, dismissing parallel intron gain for those sites may be unwarranted, because various factors can potentially constrain the site of intron insertion. Demonstrating parallel intron gain is severely handicapped, because intron sequences often evolve exceedingly fast and intron phylogenetic distributions are usually ambiguous, such that alternative loss and gain scenarios cannot be clearly distinguished. We have identified an intron position that was gained independently in animals and plants in the xanthine dehydrogenase gene. The extremely disjointed phylogenetic distribution of the intron argues strongly for separate gain rather than recurrent loss. If the observed phylogenetic pattern had resulted from recurrent loss, all observational support previously gathered for the introns-late theory of intron origins based on the phylogenetic distribution of introns would be invalidated.S pliceosomal introns are one of the hallmarks of eukaryotic genomes, which are distinctively elusive at providing unmixed clues about their evolutionary origins. Yet, after 25 years of contention (see ref. 1 and references therein), the dispute about the origins of introns between ''introns-early'' (IE, alternatively known as the exon theory of genes) and ''introns-late'' (IL) advocates seems to be approaching a synthesis. It is now almost certain that, if the progenote had introns, those could be type II self-splicing introns but never spliceosomal introns (1, 2). Because of the presumably severe constraints imposed on intronic recombination by the role that self-splicing introns play in their own removal, the IE advocates claim that exon shuffling as a factor for the assemblage of primordial genes seems unlikely. However, recent findings in the deeply diverging, putative basal eukaryote Giardia strongly indicate that spliceosomal introns originated in the eukaryotic stem before the diversification of protists, considerably earlier than suggested initially by IL advocates (i.e., around the time of origin of multicellularity; ref.3). The IL notion that spliceosomal introns as well as the spliceosoma evolved through subfunctionalization of one or more self-splicing group II introns (2, 4, 5) has gained credit. Once released from the constraints of self-splicing, spliceosomal introns may have been instrumental in creating a profusion of new eukaryotic genes by exon shuffling (6). IE supporters now admit that intron insertion is an important process in the evolution of eukaryotic genes, although they persist in asserting that deletion of ancest...

Alternative splicing: A missing piece in the puzzle of intron gain

“…Homoplastic gains represent 5-20% of shared intron positions (8,9,27,28). Although the potential for homoplastic gain decreases with the divergence in the sample, closely related sequences are prone to it by virtue of their high similarity (provided gains do not occur at random) (29). Studies of closely related species that use distantly related outgroups (e.g., 15,17,21,22) have enhanced likelihood of parallel gain.…”

The pattern of intron loss

“…This result suggests that intron loss may occur through qualitatively different mechanisms in nematodes. Kent and Zahler (41) offer the interesting observation that the 5Ј and 3Ј boundaries of unique introns between C. elegans and Caenorhabditis briggsae show greater similarity to each other than do the boundaries of control introns, and suggested that introns may be lost by nonhomologous recombination between intron boundaries [although their result could also be explained by preferential intron insertion into sites with a consensus sequence of AG͉GT (17,(27)(28)(29)(30)(31)(32)(33)(34)]. Comparative analyses of multiple nematode genomes should help to better understand these deviations.…”

“…First, the biases could be echoes of gene formation through combination of exons or groups of exons (3-7, 9, 23-26) mediated by ancient phase zero introns (23). Second, intron insertion might be phase-biased (5,8,16,(27)(28)(29)(30)(31)(32)(33)(34), perhaps due to preferential insertion into sites which themselves happen to be phase-biased (although, see ref. 7).…”

Identification of One Intron Loss and Phylogenetic Evolution of Dfak Gene in the Drosophila melanogaster Species Group

“…Intron-exon structure relationship and intron evolution in genes have been a debating focus of evolutionary biology (Tarrio, Rodriguez-Trelles & Ayala, 2003). Recently, intron loss and its evolutionary significance have been noted in Drosophila.…”