A tendency for exons to correspond to discrete units of protein structure in protein-coding genes of ancient origin would provide clear evidence in favor of the exon theory of genes, which proposes that split genes arose not by insertion of introns into unsplit genes, but from combinations of primordial mini-genes (exons) separated by spacers (introns). Although putative examples of such correspondence have strongly influenced previous debate on the origin of introns, a general correspondence has not been rigorously proved. Objective methods for detecting correspondences were developed and applied to four examples that have been cited previously as evidence of the exon theory of genes. No significant correspondence between exons and units of protein structure was detected, suggesting that the putative correspondence does not exist and that the exon theory of genes is untenable.
The gene encoding the glycolytic enzyme triose-phosphate isomerase (TPI; EC 5.3.1.1) has been central to the long-standing controversy on the origin and evolutionary significance of spliceosomal introns by virtue of its pivotal support for the introns-early view, or exon theory of genes.Putative correlations between intron positions and TPI protein structure have led to the conjecture that the gene was assembled by exon shuffling, and five TPI intron positions are old by the criterion of being conserved between animals and plants. We have sequenced TPI genes from three diverse eukaryotes-the basidiomycete Coprinus cinereus, the nematode Caenorhabditis elegans, and the insect Heliothis virescens and have found introns at seven novel positions that disrupt previously recognized gene/protein structure correlations.The set of 21 TPI introns now known is consistent with a random model of intron insertion. Twelve of the 21 TPI introns appear to be of recent origin since each is present in but a single examined species. These results, together with their implication that as more TPI genes are sequenced more intron positions will be found, render TPI untenable as a paradigm for the introns-early theory and, instead, support the introns-late view that spliceosomal introns have been inserted into preexisting genes during eukaryotic evolution.The surprising discovery of spliceosomal introns in 1977 was soon followed by considerable speculation about their origin, evolution, and significance (1-3). Nearly 20 years later, the issue is very much alive and has long since become polarized into two opposing theories. The introns-early theory, or exon theory of genes, posits the presence of many introns in the common ancestor of all life, followed by massive, often complete, intron loss in many independent lineages (4, 5). Introns are thought to have functioned in the primordial assembly of protein genes by promoting the recombinational shuffling of short exons, each encoding 15-20 amino acid units of protein structure (6-8). The other theory, termed introns-late, posits that spliceosomal introns were not present in the common ancestor of life but, instead, arose and spread within eukaryotic evolution (9-11); therefore, these introns could not have played any role in ancient gene and protein assembly.A major part of the evidence in favor of the introns-early theory has been supplied by the ancient gene encoding the glycolytic enzyme triose-phosphate isomerase (TPI; EC 5.3.1.1; refs. 6-8 and 12). As soon as the first eukaryotic TPI gene was sequenced, a correspondence was noted between exons and secondary structural elements, with all six chicken introns falling at or near the ends of a-helices and (3-strands (13). More TPI intron positions were discovered in 1986 from a plant and a fungus (6). Five introns are located in the same positions in plant and animal TPI genes, indicating that these introns were in place prior to the presumably ancient divergence of these taxa (6). Since these new data did not support a straightf...
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