Footprints of primordial introns on the eukaryotic genome

Roy, Scott William; Lewis, Benjamin P.; Fedorov, Alexei; Gilbert, Walter

doi:10.1016/s0168-9525(01)02375-7

Cited by 24 publications

(18 citation statements)

References 13 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This number rapidly decreases while moving away from the peak of 47 nt. Also, positions of many C. elegans introns differ from the intron positions in other species Roy et al 2001 …”

Section: Comparison Of C Elegans Intronsmentioning

confidence: 99%

Mystery of Intron Gain

Fedorov¹,

Roy²,

Fedorova³

et al. 2003

Genome Res.

Self Cite

View full text Add to dashboard Cite

For nearly 15 years, it has been widely believed that many introns were recently acquired by the genes of multicellular organisms. However, the mechanism of acquisition has yet to be described for a single animal intron. Here, we report a large-scale computational analysis of the human, Drosophila melanogaster, Caenorhabditis elegans, and Arabidopsis thaliana genomes. We divided 147,796 human intron sequences into batches of similar lengths and aligned them with each other. Different types of homologies between introns were found, but none showed evidence of simple intron transposition. Also, 106,902 plant, 39,624 Drosophila, and 6021 C. elegans introns were examined. No single case of homologous introns in nonhomologous genes was detected. Thus, we found no example of transposition of introns in the last 50 million years in humans, in 3 million years in Drosophila and C. elegans, or in 5 million years in Arabidopsis. Either new introns do not arise via transposition of other introns or intron transposition must have occurred so early in evolution that all traces of homology have been lost.[A. Smit and P. Green kindly provided computer programs.]When introns were first discovered in 1977, an immediate question was where do they come from? Very early in the debate, Crick and others suggested that new introns might arise as transposons that either come equipped with or quickly acquire signals sufficient for splicing (Crick 1979). This idea was reinforced by the finding by Dibb and Newman (1989) that introns tend to arise at sites with a consensus sequence of (C/A)AG|R, which they interpreted in terms of sequence-specific targeting of some notyet-characterized insertion machinery. However, small-scale comparisons of intron sequences have turned up no evident transposition events, and there is to date a sole convincing demonstration of the creation of an intron from a transposable element, in plants ( Giroux et al. 1994).Yet, it is becoming increasingly clear that some introns have arisen very recently. There is a growing collection of introns found at positions in one species at which closely related species have no intron (Palmer and Logsdon Jr. 1991;Logsdon Jr. et al. 1995;Rzhetsky et al. 1997;Frugoli et al. 1998;Gotoh 1998;Tarrio et al. 1998;Venkatesh et al. 1999; for an insightful review, see Logsdon Jr. et al. 1998;Lynch and Richardson 2002). Over a longer time scale, only 14% of animal intron positions match with the intron positions of homologous plant genes, indicating that, if gain is a primary mechanism of intron discordance, 60%-80% percent of contemporary animal introns were acquired after the evolutionary divergence of animals and plants (Fedorov et al. 2002).Such new introns should not be hard to find. For instance, the human genome has 31,000 intron-containing genes with 160,000 introns. If 60% of these introns were acquired since the animal-plant divergence then there have been an average of 20-50 cases of intron insertion per million years of human evolution. This estimation is also in accordance w...

show abstract

“…This number rapidly decreases while moving away from the peak of 47 nt. Also, positions of many C. elegans introns differ from the intron positions in other species Roy et al 2001 …”

Section: Comparison Of C Elegans Intronsmentioning

confidence: 99%

Mystery of Intron Gain

Fedorov¹,

Roy²,

Fedorova³

et al. 2003

Genome Res.

Self Cite

View full text Add to dashboard Cite

show abstract

“…The earliest version of the intronsearly theory postulated that, during the course of evolution, introns were completely lost from prokaryotes while being partly retained in eukaryotes. A recently revised version suggests that although intron loss was the main driving force for intron evolution, some modern introns were inserted recently [4,5]. The introns-late theory, on the other hand, holds that all spliceosomal introns were only recently inserted into eukaryotic genes [6,7]; although the introns-late theory allows for some intron losses, it stresses that intron gains played the primary role in forming the modern pattern of introns.…”

Section: Introductionmentioning

confidence: 99%

“…The introns-late theory, on the other hand, holds that all spliceosomal introns were only recently inserted into eukaryotic genes [6,7]; although the introns-late theory allows for some intron losses, it stresses that intron gains played the primary role in forming the modern pattern of introns. The debate between these two theories remains vigorous [4,8].…”

Section: Introductionmentioning

confidence: 99%

Analysis of Ribosomal Protein Gene Structures: Implications for Intron Evolution

Yoshihama¹,

Nakao²,

Nguyen³

et al. 2005

PLoS Genet

View full text Add to dashboard Cite

Many spliceosomal introns exist in the eukaryotic nuclear genome. Despite much research, the evolution of spliceosomal introns remains poorly understood. In this paper, we tried to gain insights into intron evolution from a novel perspective by comparing the gene structures of cytoplasmic ribosomal proteins (CRPs) and mitochondrial ribosomal proteins (MRPs), which are held to be of archaeal and bacterial origin, respectively. We analyzed 25 homologous pairs of CRP and MRP genes that together had a total of 527 intron positions. We found that all 12 of the intron positions shared by CRP and MRP genes resulted from parallel intron gains and none could be considered to be ''conserved,'' i.e., descendants of the same ancestor. This was supported further by the high frequency of proto-splice sites at these shared positions; proto-splice sites are proposed to be sites for intron insertion. Although we could not definitively disprove that spliceosomal introns were already present in the last universal common ancestor, our results lend more support to the idea that introns were gained late. At least, our results show that MRP genes were intronless at the time of endosymbiosis. The parallel intron gains between CRP and MRP genes accounted for 2.3% of total intron positions, which should provide a reliable estimate for future inferences of intron evolution.

show abstract

“…For the first 25 years, the debate was waged in the context of the introns-early͞introns-late question. Proponents of introns-late believe that spliceosomal introns are relatively recent arrivals whose modern restriction to eukaryotes reflects their absence in the common ancestors of prokaryotes and eukaryotes and subsequent origin within eukaryotes (1,12,24,37,(52)(53)(54)(55)(56). Their task was thus to demonstrate that modern intron-exon structures could be explained primarily or solely by intron gain in eukaryotes, without a necessarily major role for intron loss.…”

mentioning

confidence: 99%

Rates of intron loss and gain: Implications for early eukaryotic evolution

Roy

Gilbert

2005

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

192

145

View full text Add to dashboard Cite

We study the intron-exon structures of 684 groups of orthologs from seven diverse eukaryotic genomes and provide maximum likelihood estimates for rates and numbers of intron losses and gains in these same genes for a variety of lineages. Rates of intron loss vary from Ϸ2 ؋ 10 ؊9 to 2 ؋ 10 ؊10 per year. Rates of gain vary from 6 ؋ 10 ؊13 to 4 ؋ 10 ؊12 per possible intron insertion site per year. There is an inverse correspondence between rates of intron loss and gain, leading to a 20-fold variation among lineages in the ratio of the rates of the two processes. The observed rates of intron gain are insufficient to explain the large number of introns estimated to have been present in the plant-animal ancestor, suggesting that introns present in early eukaryotes may have been created by a fundamentally different process than more recently gained introns. genome evolution T he debate over the relative importance of intron loss and gain in shaping the pattern of imperfect conservation of intronexon structures between homologues has been long and hard fought (1-51). For the first 25 years, the debate was waged in the context of the introns-early͞introns-late question. Proponents of introns-late believe that spliceosomal introns are relatively recent arrivals whose modern restriction to eukaryotes reflects their absence in the common ancestors of prokaryotes and eukaryotes and subsequent origin within eukaryotes (1,12,24,37,(52)(53)(54)(55)(56). Their task was thus to demonstrate that modern intron-exon structures could be explained primarily or solely by intron gain in eukaryotes, without a necessarily major role for intron loss. Introns-early adherents believe that introns are primordial structures whose presence in eukaryote-prokaryote ancestors facilitated the construction of early genes (2-11, 15, 22, 23, 25, 33, 35, 40). The presence of large numbers of introns in modern genomes thus does not necessarily require active intron insertion in eukaryotes, although the lack of spliceosomal introns in prokaryotes, as well as the existence of some introns with spotty phylogenetic distributions within eukaryotes, require significant intron loss. In this way was the more fundamental debate about the timing of origin of the first spliceosomal introns, with all its implications for the origins of early genes, the emergence of complex genomes, and the divergence of the three kingdoms of life, projected onto the issue of intron loss and gain. Since that time, both perspectives have been softened, intronsearly by discoveries of introns whose very limited phylogenetic distributions suggest their recent gain (3, 7-12, 20, 22, 33, 42-44) and introns-late by the discovery of introns and spliceosomal components in very deep-branching eukaryotes (57-60). However, the basic disagreements over when spliceosomal introns first appeared in significant numbers and whether eukaryotic evolution has been characterized by generally decreasing, stable, or increasing intron density persist (30-50).In the first characterized case of intron disc...

show abstract

Footprints of primordial introns on the eukaryotic genome

Cited by 24 publications

References 13 publications

Mystery of Intron Gain

Mystery of Intron Gain

Analysis of Ribosomal Protein Gene Structures: Implications for Intron Evolution

Rates of intron loss and gain: Implications for early eukaryotic evolution

Contact Info

Product

Resources

About