Intron Dynamics in Ribosomal Protein Genes

PLOS ONE, Jan 2007

The role of spliceosomal introns in eukaryotic genomes remains obscure. A large scale analysis of intron presence/absence patterns in many gene families and species is a necessary step to clarify the role of these introns. In this analysis, we used a maximum likelihood method to reconstruct the evolution of 2,961 introns in a dataset of 76 ribosomal protein genes from 22 eukaryotes and validated the results by a maximum parsimony method. Our results show that the trends of intron gain and loss differed across species in a given kingdom but appeared to be consistent within subphyla. Most subphyla in the dataset diverged around 1 billion years ago, when the “Big Bang” radiation occurred. We speculate that spliceosomal introns may play a role in the explosion of many eukaryotes at the Big Bang radiation.

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Intron Dynamics in Ribosomal Protein Genes

Citation: Yoshihama M, Nguyen HD, Kenmochi N ( Intron Dynamics in Ribosomal Protein Genes Maki Yoshihama 0 1 Hung D. Nguyen 0 1 Naoya Kenmochi kenmochi@med 0 1 0 Academic Editor: Oliver Hofmann, South African National Bioinformatics Institute , South Africa 1 Frontier Science Research Center, University of Miyazaki , Kiyotake, Miyazaki , Japan The role of spliceosomal introns in eukaryotic genomes remains obscure. A large scale analysis of intron presence/absence patterns in many gene families and species is a necessary step to clarify the role of these introns. In this analysis, we used a maximum likelihood method to reconstruct the evolution of 2,961 introns in a dataset of 76 ribosomal protein genes from 22 eukaryotes and validated the results by a maximum parsimony method. Our results show that the trends of intron gain and loss differed across species in a given kingdom but appeared to be consistent within subphyla. Most subphyla in the dataset diverged around 1 billion years ago, when the ''Big Bang'' radiation occurred. We speculate that spliceosomal introns may play a role in the explosion of many eukaryotes at the Big Bang radiation. - INTRODUCTION Many spliceosomal introns, which are non-coding DNA sequences, exist in eukaryotic nuclear genes. Their role in the genome, however, remains poorly understood. From the view of eukaryotic evolution, it is very important to know why exon/ intron structures of genes differ across species and what the effects of intron gain and loss are. In order to clarify these issues, we must first reconstruct the process of intron gain and loss during eukaryotic evolution. This task became possible recently with the availability of many completely sequenced genomes. In a representative study, Rogozin et al. [1] compiled a dataset of 684 gene orthologs from eight eukaryotes and used a maximum parsimony method to infer the evolution of introns in this dataset. The results of applying maximum likelihood methods to the same dataset were reported later [24]. Although the number of species in the dataset is not very large and the different methods inferred different patterns of intron gain and loss, it became clear that: (i) from 15% to 25% of present-day introns were already present in the last common ancestor of plantae, metazoa, and fungi, and (ii) many introns were gained after this divergence [14]. We have recently compiled a dataset of ribosomal protein (RP) genes [5]. RP genes offer several advantages for studying intron evolution [68]. First, they exist in all species and, as they are involved in the vital process of translation, they are well conserved throughout evolution [9,10]. Thus, it is fairly easy to compare intron positions in RP genes across a wide range of distantly diverged species. Second, there are a large number of conserved RP gene families. For instance, 79 distinct RPs are found in humans and of these 79, 78 are also found in yeast. Third, introns also exist in RP genes of very deep-branching eukaryotes that harbor very few introns, such as Giardia lamblia [11,12]. With these advantages, we expect that RP genes will become a powerful tool for discovering the roles of spliceosomal introns. RESULTS Compilation of the dataset and phylogenetic analysis We compiled a dataset of 76 RP gene orthologs from 22 eukaryotes. The phylogenetic tree of these 22 species is depicted in Figure 1. These 22 species belong to four kingdoms, metazoa, fungi, protozoa, and plantae, and cover 14 different subphyla. The conserved regions of this dataset included 2,961 introns located at 1,182 different positions. To the best of our knowledge, this is the first time a dataset with this many gene families and species has been used for studying intron evolution. Patterns of intron gain and loss in 22 species We first used our recently developed maximum likelihood (ML) method [4] to infer the process of intron gain and loss (Figure 2A). We also used a maximum parsimony method to validate the result of the ML method, because the ML method may produce unreliable results when the data sample is small (Figure 2B). Since the two results show similar patterns of intron gain and loss in most subphyla of the dataset (the largest differences are in the two plant subphyla), the results from the ML method were used for subsequent analyses. The most significant feature in Figure 2 is that species belonging to a given subphylum show similar trends of intron gain and loss. For example, all three species in insecta (subphylum 3 in Figure 2) show trends toward decreasing introns, whereas all three species in pezizomycotina (subphylum 5) show trends toward increasing introns. There is, however, no consensus trend of intron gain and loss among species of a given kingdom. This fact is most notable in the fungus kingdom. The subphyla pezizomycotina (subphylum 5) and hymenomycetes (subphylum 8) trended toward increasing introns, whereas the three other subphyla [saccharomycotina (subphylum (...truncated)


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Maki Yoshihama, Hung D. Nguyen, Naoya Kenmochi. Intron Dynamics in Ribosomal Protein Genes, PLOS ONE, 2007, Volume 2, Issue 1, DOI: 10.1371/journal.pone.0000141