Likely Scenarios of Intron Evolution

Csűrös, Miklós

doi:10.1007/11554714_5

Cited by 44 publications

(35 citation statements)

References 25 publications

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“…The next generation of increasingly sophisticated ML reconstructions of intron gain and loss during eukaryotic evolution suggested that the protein-coding genes of ancient eukaryotic ancestors, including the Last Eukaryotic Common Ancestor (LECA), already possessed intron density comparable to that found in modern, moderately intron-rich genomes [85-88,136]. Accordingly, the history of eukaryotic genes, with respect to the dynamics of introns, appears to be to a large extent dominated by losses, perhaps punctuated by a few episodes of major gain [87,88,91,137].…”

Section: Reconstruction Of Evolution Of Exon-intron Structure Of Eukamentioning

confidence: 99%

“…Episodes of substantial intron gain seem to coincide with the emergence of major new groups of organisms with novel biological characteristics such as the Metazoa (Figure 7) [53]. Several previous studies, performed on much smaller data sets and with less robust reconstruction methods, have suggested that at least some eukaryotic ancestral forms could have possessed intron-rich genes [84,85,136], and observations on gene structures in primitive animals such as the sea anemone Nematostella [139] and the flatworm Platynereis [140] were compatible with these inferences. A particularly striking conclusion has been reached in the reconstruction of the evolution of gene architecture in Chromalveolata: although all sequenced genomes in this supergroup of eukaryotes are intron-poor, intron-rich last common ancestors have been inferred for Chromalveolata and particularly Alveolata [141].…”

Section: Reconstruction Of Evolution Of Exon-intron Structure Of Eukamentioning

confidence: 99%

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Origin and evolution of spliceosomal introns

et al. 2012

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Evolution of exon-intron structure of eukaryotic genes has been a matter of long-standing, intensive debate. The introns-early concept, later rebranded ‘introns first’ held that protein-coding genes were interrupted by numerous introns even at the earliest stages of life's evolution and that introns played a major role in the origin of proteins by facilitating recombination of sequences coding for small protein/peptide modules. The introns-late concept held that introns emerged only in eukaryotes and new introns have been accumulating continuously throughout eukaryotic evolution. Analysis of orthologous genes from completely sequenced eukaryotic genomes revealed numerous shared intron positions in orthologous genes from animals and plants and even between animals, plants and protists, suggesting that many ancestral introns have persisted since the last eukaryotic common ancestor (LECA). Reconstructions of intron gain and loss using the growing collection of genomes of diverse eukaryotes and increasingly advanced probabilistic models convincingly show that the LECA and the ancestors of each eukaryotic supergroup had intron-rich genes, with intron densities comparable to those in the most intron-rich modern genomes such as those of vertebrates. The subsequent evolution in most lineages of eukaryotes involved primarily loss of introns, with only a few episodes of substantial intron gain that might have accompanied major evolutionary innovations such as the origin of metazoa. The original invasion of self-splicing Group II introns, presumably originating from the mitochondrial endosymbiont, into the genome of the emerging eukaryote might have been a key factor of eukaryogenesis that in particular triggered the origin of endomembranes and the nucleus. Conversely, splicing errors gave rise to alternative splicing, a major contribution to the biological complexity of multicellular eukaryotes. There is no indication that any prokaryote has ever possessed a spliceosome or introns in protein-coding genes, other than relatively rare mobile self-splicing introns. Thus, the introns-first scenario is not supported by any evidence but exon-intron structure of protein-coding genes appears to have evolved concomitantly with the eukaryotic cell, and introns were a major factor of evolution throughout the history of eukaryotes. This article was reviewed by I. King Jordan, Manuel Irimia (nominated by Anthony Poole), Tobias Mourier (nominated by Anthony Poole), and Fyodor Kondrashov. For the complete reports, see the Reviewers’ Reports section.

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Section: Reconstruction Of Evolution Of Exon-intron Structure Of Eukamentioning

confidence: 99%

Section: Reconstruction Of Evolution Of Exon-intron Structure Of Eukamentioning

confidence: 99%

Origin and evolution of spliceosomal introns

et al. 2012

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“…Avariety of studies have shown that genes from intron-rich species from any major eukaryotic supergroup share a significant number of intron positions with other groups (Fedorov et al 2002;Rogozin et al 2003;Csurös et al 2008Csurös et al , 2011. Different investigators have used different methods of evolutionary inference, ranging from parsimony to maximum likeli-hood, to attempt to reconstruct ancestral intron densities (Rogozin et al 2003;Qiu et al 2004;Csurös 2005Csurös , 2008Nguyen et al 2005;Roy and Gilbert 2005;Carmel et al 2007Carmel et al , 2009). With increasing taxonomic sampling usually yielding increasingly higher estimates for LECA's intron density, the latest reconstructions (Csurös et al 2011) used a Markov chain Monte Carlo approach to investigate 99 genomes from five eukaryotic supergroups, and estimated that LECA had 53% -74% of modern human intron density, or 4.5 -6.3 introns per gene (assuming similar average protein-coding lengths).…”

Section: Reconstruction Of Intron-exon Structures In Lecamentioning

confidence: 99%

Origin of Spliceosomal Introns and Alternative Splicing

Irimia

Roy

2014

Cold Spring Harbor Perspectives in Biology

130

121

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In this work we review the current knowledge on the prehistory, origins, and evolution of spliceosomal introns. First, we briefly outline the major features of the different types of introns, with particular emphasis on the nonspliceosomal self-splicing group II introns, which are widely thought to be the ancestors of spliceosomal introns. Next, we discuss the main scenarios proposed for the origin and proliferation of spliceosomal introns, an event intimately linked to eukaryogenesis. We then summarize the evidence that suggests that the last eukaryotic common ancestor (LECA) had remarkably high intron densities and many associated characteristics resembling modern intron-rich genomes. From this intronrich LECA, the different eukaryotic lineages have taken very distinct evolutionary paths leading to profoundly diverged modern genome structures. Finally, we discuss the origins of alternative splicing and the qualitative differences in alternative splicing forms and functions across lineages. SURPRISES AND MYSTERIES OF INTRONS AND INTRON EVOLUTIONW ith mid-20th century breakthroughs, molecular cell biology finally seemed to obey a relatively simple logic. Genetic information was encoded in DNA genes (Avery et al. 1944;Watson and Crick 1953), which were transcribed into RNA and subsequently translated into functional proteins (Crick 1958). However, a most unexpected finding "interrupted" this logic. The coding information of DNA genes was sometimes broken into pieces separated by sequences whose sole apparent purpose was to generate an extra RNA sequence that then had to be removed to generate intact proteincoding messenger RNAs. The initial findings in viruses (Berget et al. 1977;Chow et al. 1977) were soon extended to many cellular genes. With the advent of large-scale sequencing projects, it became clear that one kind of intron (the spliceosomal introns), as well as the cellular machinery that removes them (the spliceosome), are ubiquitous in eukaryotic genomes. For example, the average human transcript contains 9 introns, totaling several hundred thousand introns across the genome and comprising a quarter of the DNA content of each cell (Lander et al. 2001;Venter et al. 2001). Moreover, functions for some introns began to

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“…Consequently, likelihood methods tend to underestimate the extent of gene losses. The situation is similar to what is encountered in likelihood models of intron evolution and a possible remedy is discussed in (Csűrös 2005). This paper focuses on the core algorithmic problems of likelihood computations in a biologically realistic model of gene content evolution.…”

Section: Resultsmentioning

confidence: 83%

A Probabilistic Model for Gene Content Evolution with Duplication, Loss, and Horizontal Transfer

Csűrös

Miklós

2006

Lecture Notes in Computer Science

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We introduce a Markov model for the evolution of a gene family along a phylogeny. The model includes parameters for the rates of horizontal gene transfer, gene duplication, and gene loss, in addition to branch lengths in the phylogeny. The likelihood for the changes in the size of a gene family across different organisms can be calculated in O(N + hM 2 ) time and O(N + M 2 ) space, where N is the number of organisms, h is the height of the phylogeny, and M is the sum of family sizes. We apply the model to the evolution of gene content in Preoteobacteria using the gene families in the COG (Clusters of Orthologous Groups) database.

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Likely Scenarios of Intron Evolution

Cited by 44 publications

References 25 publications

Origin and evolution of spliceosomal introns

Origin and evolution of spliceosomal introns

Origin of Spliceosomal Introns and Alternative Splicing

A Probabilistic Model for Gene Content Evolution with Duplication, Loss, and Horizontal Transfer

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