New Maximum Likelihood Estimators for Eukaryotic Intron Evolution

Nguyen, Hung D.; Yoshihama, Maki; Kenmochi, Naoya

doi:10.1371/journal.pcbi.0010079

Cited by 78 publications

(102 citation statements)

References 28 publications

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“…In contrast, our estimate was derived from observed data and therefore should be more reliable. It is known that spliceosomal introns existed in quite high density in the last common ancestor of the three eukaryotic kingdoms: animals, fungi, and plants [11,12,26]. However, the evolution of spliceosomal introns at the earliest stage of eukaryotic evolution remains unclear.…”

Section: Discussionmentioning

confidence: 99%

“…We recently proposed a maximum likelihood approach for inferring the evolution of introns [26]; however, we believe that maximum parsimony is the best choice for the current dataset because maximum likelihood uses only patterns of intron position in the conserved regions of the multiple sequence alignment, and our dataset is not large enough to make valid statistical inferences using this method.…”

Section: Parsimony Analysis Of Crp-mrp Shared Positionsmentioning

confidence: 99%

“…(The ninth position shared between RPS23-2 and MRPS12-2 genes could not be classified because the costs of each scenario were equal.) However, considering that A. thaliana has a very high rate of intron gain [12,14,26], the possibility that this intron position was also the result of parallel gain is high. Taking all of the results together, we concluded that all 12 intron positions (including the three misaligned positions) shared between CRP and MRP were the result of parallel gains.…”

Section: Parsimony Analysis Of Crp-mrp Shared Positionsmentioning

confidence: 99%

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Analysis of Ribosomal Protein Gene Structures: Implications for Intron Evolution

Yoshihama¹,

Nakao²,

Nguyen³

et al. 2005

PLoS Genet

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Parsimony Analysis Of Crp-mrp Shared Positionsmentioning

confidence: 99%

Section: Parsimony Analysis Of Crp-mrp Shared Positionsmentioning

confidence: 99%

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Analysis of Ribosomal Protein Gene Structures: Implications for Intron Evolution

Yoshihama¹,

Nakao²,

Nguyen³

et al. 2005

PLoS Genet

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“…Past studies concluded that the early, eukaryotic ancestors were relatively rich in introns and that their genes contained relatively high intron densities (Rogozin et al 2003;Nguyen et al 2005;Raible et al 2005;Roy and Gilbert 2005a,b;Sverdlov et al 2005;Carmel et al 2007). This observation, combined with our finding that splicing signals are degenerate, may suggest that the genome of the ancestral eukaryote was more similar to the mammalian genome than previously anticipated and opens up the possibility that alternative splicing existed early in eukaryotic evolution.…”

Section: Splicing In the Eukaryotic Ancestormentioning

confidence: 99%

Large-scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes

Schwartz

Silva²,

Burstein³

et al. 2007

Genome Res.

168

174

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Introns are among the hallmarks of eukaryotic genes. Splicing of introns is directed by three main splicing signals: the 5Ј splice site (5Јss), the branch site (BS), and the polypyrimdine tract/3Јsplice site (PPT-3Јss). To study the evolution of these splicing signals, we have conducted a systematic comparative analysis of these signals in over 1.2 million introns from 22 eukaryotes. Our analyses suggest that all these signals have dramatically evolved: The PPT is weak among most fungi, intermediate in plants and protozoans, and strongest in metazoans. Within metazoans it shows a gradual strengthening from Caenorhabditis elegans to human. The 5Јss and the BS were found to be degenerate among most organisms, but highly conserved among some fungi. A maximum parsimony-based algorithm for reconstructing ancestral position-specific scoring matrices suggested that the ancestral 5Јss and BS were degenerate, as in metazoans. To shed light on the evolutionary variation in splicing signals, we have analyzed the evolutionary changes in the factors that bind these signals. Our analysis reveals coevolution of splicing signals and their corresponding splicing factors: The strength of the PPT is correlated to changes in key residues in its corresponding splicing factor U2AF2; limited correlation was found between changes in the 5Јss and U1 snRNA that binds it; but not between the BS and U2 snRNA. Thus, although the basic ability of eukaryotes to splice introns has remained conserved throughout evolution, the splicing signals and their corresponding splicing factors have considerably evolved, uniquely shaping the splicing mechanisms of different organisms.[Supplemental material is available online at www.genome.org.]Splicing of pre-mRNA is a key step in eukaryotic gene expression, contributing to gene regulation, protein diversity, and phenotypic complexity. Introns are removed from the pre-mRNA by the spliceosome, which is composed of five snRNPs (small nuclear ribonucleoprotein) (U1, U2, U4, U5, and U6), each containing a small RNA bound by proteins. High-precision recognition of introns is required for correct splicing. This recognition is achieved by the binding of splicing factors to signals of varying specificity that are located both in the intron and its flanking exons (Hastings and Krainer 2001;Black 2003;. In vertebrates, three signals are known to direct splicing: The 5Ј splice site (5Јss) at the 5Ј end of the intron, the polypyrimdine tract/3Ј splice site (PPT-3Јss) at the 3Ј end of the intron, and a branch site (BS) upstream of the PPT-3Јss (Hastings and Krainer 2001;Black 2003). Spliceosome assembly is initiated by the binding of specific splicing factors to these signals: the U1 snRNP to the 5Јss, the protein SF1 to the BS, the U2 snRNP auxiliary factor U2AF large subunit (U2AF2; also known as U2AF65) to the PPT, and the U2AF small subunit (U2AF1; also known as U2AF35) to the 3Јss. In an ensuing reaction, U2 snRNP associates with the pre-mRNA through a base-pairing interaction between U2 snRNA (small nuclear RNA)...

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“…While Qiu et al (2004) concluded that intron gains were overwhelmingly dominant in eukaryotic evolution, the other studies detected both gains and losses but disagreed on their relative contributions. Analyzing the same set of orthologous genes from eight species (Rogozin et al 2003), some found an overall excess of gains (Nguyen et al 2005), others reported a substantial excess of losses Gilbert 2005a,b,c, 2006), and yet others did not offer conclusive statements on the relative contributions of gains and losses (Rogozin et al 2003;Csuros 2005). Each of these studies used a different set of assumptions and simplifications, and employed a different inference technique, making it hard to decide between the conflicting scenarios of intron evolution (Rogozin et al 2005b).…”

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confidence: 99%

Three distinct modes of intron dynamics in the evolution of eukaryotes

Carmel

Wolf²,

Rogozin³

et al. 2007

Genome Res.

158

204

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Several contrasting scenarios have been proposed for the origin and evolution of spliceosomal introns, a hallmark of eukaryotic genes. A comprehensive probabilistic model to obtain a definitive reconstruction of intron evolution was developed and applied to 391 sets of conserved genes from 19 eukaryotic species. It is inferred that a relatively high intron density was reached early, i.e., the last common ancestor of eukaryotes contained >2.15 introns/kilobase, and the last common ancestor of multicellular life forms harbored ∼3.4 introns/kilobase, a greater intron density than in most of the extant fungi and in some animals. The rates of intron gain and intron loss appear to have been dropping during the last ∼1.3 billion years, with the decline in the gain rate being much steeper. Eukaryotic lineages exhibit three distinct modes of evolution of the intron-exon structure. The primary, balanced mode, apparently, operates in all lineages. In this mode, intron gain and loss are strongly and positively correlated, in contrast to previous reports on inverse correlation between these processes. The second mode involves an elevated rate of intron loss and is prevalent in several lineages, such as fungi and insects. The third mode, characterized by elevated rate of intron gain, is seen only in deep branches of the tree, indicating that bursts of intron invasion occurred at key points in eukaryotic evolution, such as the origin of animals. Intron dynamics could depend on multiple mechanisms, and in the balanced mode, gain and loss of introns might share common mechanistic features.

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New Maximum Likelihood Estimators for Eukaryotic Intron Evolution

Cited by 78 publications

References 28 publications

Analysis of Ribosomal Protein Gene Structures: Implications for Intron Evolution

Analysis of Ribosomal Protein Gene Structures: Implications for Intron Evolution

Large-scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes

Three distinct modes of intron dynamics in the evolution of eukaryotes

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