ReviewGenome evolution and the evolution of exon-shuffling — a review☆
Introduction
Shortly after the discovery of split genes, it was realized that the existence of introns may have dramatic consequences on protein evolution (Gilbert, 1978). It was pointed out that recombination within introns could assort exons independently, and middle repetitious sequences in introns may create hotspots for recombination to shuffle the exonic sequences.
The presence of introns in most eukaryotic protein-coding genes and their absence from prokaryotes was explained by two types of hypotheses. The ‘introns early’ hypotheses assumed that introns and RNA splicing are the relics of the RNA world and the ‘genes in pieces’ organization of the eukaryotic genome is the original, ancestral form (Darnell, 1978, Darnell and Doolittle, 1986, Doolittle, 1978, Gilbert, 1986). According to this view, eukaryotes retained introns and the genetic plasticity of the primitive ancestors of all cells. On the other hand, bacteria gained increased efficiency by eliminating their introns. Supporters of the introns-early hypotheses assume that the introns of all protein-coding genes reflect the assembly of these genes from pieces; that exons do indeed correspond to building blocks (α-helices, β-sheets, etc.) from which all the genes were assembled by intronic recombination (Gilbert and Glynias, 1993).
In contrast with this, the ‘introns late’ theories suggest that the prokaryotic genes resemble the ancestral ones and that the introns were inserted later in genes of eukaryotes (Cavalier-Smith, 1985, Cech, 1985, Crick, 1979, Orgel and Crick, 1980, Sharp, 1985). In fact, it is now obvious that the exon–intron structure of eukaryotic protein-coding genes is not static: introns are continually inserted into (as well as removed from) genes. The actual mechanisms of insertion, propagation of some self-splicing introns have been analyzed in detail and the mechanisms responsible for the insertion of spliceosomal introns are also becoming clear (Belfort, 1991, Belfort, 1993, Dujon, 1989, Grivell, 1994, Lambowitz and Belfort, 1989, Lambowitz, 1993, Morl and Schmelzer, 1990, Mueller et al., 1993, Patthy, 1995, Perlman and Butow, 1989).
Since introns themselves are subject to evolution, it is clear that exon-shuffling has been evolving parallel with the evolution of introns. We have argued previously that the introns suitable for exon-shuffling appeared at a relatively late stage of evolution; therefore, exon-shuffling could not play a major role in the construction of ancient proteins (Patthy, 1987, Patthy, 1991a, Patthy, 1991b). The self-splicing introns of the RNA world that could be present at the time the first proteins were formed are practically unsuitable for exon-shuffling by intronic recombination: such self-splicing introns encode an essential function, therefore their sequence is not tolerant to intronic recombination (Patthy, 1987, Patthy, 1991a, Patthy, 1991b, Patthy, 1994). Exon-shuffling could become significant only with the appearance of spliceosomal introns: these introns play a negligible role in their own excision, therefore intronic recombination is less likely to produce recombinant introns that are deficient in splicing. Furthermore, the nonessential parts of spliceosomal introns could accommodate large segments of middle repetitious sequences, further increasing the chances of intronic recombination. Since spliceosomal introns evolved relatively recently from group II self-splicing introns (Cavalier-Smith, 1991, Cech, 1986, Copertino and Hallick, 1993, Jacquier, 1990, Saldanha et al., 1993, Sharp, 1994) and are restricted in their evolutionary distribution (Cavalier-Smith, 1991, Logsdon, 1991, Palmer and Logsdon, 1991) exon-shuffling could play a major role only in the construction of ‘younger’ proteins (Patthy, 1987, Patthy, 1991a, Patthy, 1991b, Patthy, 1994, Patthy, 1995, Patthy, 1996).
In the present review I wish to emphasize that the significance of exon-shuffling increased parallel with the evolution of less compact genomes. The basis of this correlation is that the number and size of introns and the proportion of repetitive sequences in introns increases parallel with the decrease of genome compactness, therefore the chances of exon-shuffling by intronic recombination also increase. Analysis of the evolutionary distribution of proteins that were clearly assembled from modules by intronic recombination suggests that exon-shuffling became significant at the time of the appearance of the first multicellular animals, and that the rise of exon-shuffling could in fact contribute to the explosive nature of metazoan radiation.
Section snippets
Introns and evolution of genome compactness
In the past few years, the complete sequences of the genomes of several Eubacteria (Escherichia coli, Bacillus subtilis, Haemophilus influenzae, Borrelia burgdorferi, Mycoplasma pneumoniae, Mycoplasma genitalium, etc.), Archaea (Methanococcus jannaschii, Archaeoglobus fulgidus, etc.), a unicellular eukaryote (Saccharomyces cerevisiae), and a multicellular animal (Caenorhabditis elegans) have been determined, and significant progress has also been made on the genome of a protozoan parasite (
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Presented at the Symposium on Evolutionary Genomics, Puntarenas, Costa Rica, 11–15 January 1999.