The pattern of intron loss

Abstract

We studied intron loss in 684 groups of orthologous genes from seven fully sequenced eukaryotic genomes. We found that introns closer to the 3 ends of genes are preferentially lost, as predicted if introns are lost through gene conversion with a reverse transcriptase product of a spliced mRNA. Adjacent introns tend to be lost in concert, as expected if such events span multiple intron positions. Directly contrary to the expectations of some, introns that do not interrupt codons (phase zero) are more, not less, likely to be lost, an intriguing and previously unappreciated result. Adjacent introns with matching phases are not more likely to be retained, as would be expected if they enjoyed a relative selective advantage. The findings of 3 and phase zero intron loss biases are in direct contradiction to an extremely recent study of fungi intron evolution. All patterns are less pronounced in the lineage leading to Caenorhabditis elegans, suggesting that the process of intron loss may be qualitatively different in nematodes. Our results support a reverse transcriptase-mediated model of intron loss.evolution ͉ genome evolution T wo generalities of the intron-exon structure of eukaryotic genes remain unexplained. First, introns in intron-sparse species or in intron-sparse genes cluster near the 5Ј ends of genes (1, 2). Second, intron positions within codons are doubly biased: introns tend to lie between the third base of one codon and the first base of the subsequent codon (phase zero) rather than between the first and second (phase one) or second and third (phase two) bases of a codon; and adjacent introns tend to be of the same phase (3-9).The 5Ј skew could be due to mutation-biased intron loss, selection-biased intron loss, or biased intron gain. If intron loss proceeds by means of gene conversion of the genomic copy of a gene by the reverse transcriptase product of a spliced transcript (RT-mRNAs) (10-15), the 3Ј bias of RT products (12) could cause a higher rate of loss for 3Ј introns (1, 2). Alternatively, possible preferential retention of 5Ј introns could reflect their greater selective importance, possibly due to a greater concentration of regulatory elements (reviewed in ref. 16). Finally, intron gain could favor 5Ј ends of genes for some unappreciated reason.We analyzed intron losses in 684 groups of orthologous genes from seven eukaryotic species, previously analyzed by Rogozin et al. (17). Fig. 1 shows the most likely phylogeny for the species (18). Results calculated assuming the alternative coelomata grouping (19,20) are similar and provided in Tables 3 and 4 and Figs. 6-9, which are published as supporting information on the PNAS web site. For each lineage, we defined introns known to be ancestral to the lineage (KAL) based on presence in both the sister group of the lineage and an outgroup. For example, introns present in a dipteran (Drosophila melanogaster and Anopheles gambiae) or Caenorhabditis elegans as well as a non-animal are KAL for the lineage leading to Homo sapiens. We found that 3Ј KAL intr...

Extensive Loss of RNA Editing Sites in Rapidly Evolving Silene Mitochondrial Genomes: Selectionvs. Retroprocessing as the Driving Force

“…This pattern is also evident in Silene, but the observed losses of editing sites in S. noctiflora are not highly clustered (after taking into account the ancestrally clustered distribution of editing sites; Figure 4). We found only 21 adjacent pairs of lost editing sites specific to S. noctiflora (counting only sites that were lost by C-to-T substitution), which is not significantly different from the random expectation (P ¼ 0.31) (Roy and Gilbert 2005). This test for clustering of lost editing sites was similarly nonsignificant when the data were analyzed as individual exons (P ¼ 0.40) or as separately transcribed and trans-spliced fragments (P ¼ 0.42) rather than as whole genes.…”

“…To determine whether C-to-T substitutions at RNA editing sites are clustered within the S. noctiflora mitochondrial genome, we employed the method previously described by Roy and Gilbert (2005) for analyzing spatial patterns of intron loss. We calculated the probability distribution for the expected number of pairs of adjacent losses (i.e., C-to-T substitutions) given the number of lost and retained sites in each gene and the assumption that each loss occurs as an independent event.…”

TheFLOWERING LOCUS T-Like Gene Family in Barley (Hordeum vulgare)

“…Reverse transcription of spliced mRNAs followed by homologous recombination of the cDNA with the genomic copy of the gene has been suggested as a mechanism for precise intron loss (Roy and Gilbert 2006), and this process has been shown to occur in unicellular eukaryotes (Bon et al 2003;Mourier and Jeffares 2003;Sverdlov et al 2004;Roy and Gilbert 2005). The loss of the intron was found in several barley cultivars, wild barley accessions, and wheat, suggesting that it may be a general feature of temperate grasses.…”

Nucleotide sequence composition adjacent to intronic splice sites improves splicing efficiency via its effect on pre-mRNA local folding in fungi

“…In fission yeast, 1500-2000 introns were lost during evolution while ∼1800 introns demonstrated a high degree of conservation (Roy and Gilbert 2005;Carmel et al 2007;Rhind et al 2011;Cohen et al 2012). In order to compare conserved and nonconserved genes in S. pombe, we looked at 1718 conserved and 3029 nonconserved introns found in four diverse fission yeasts reported by Zhu and Niu (2013) (S. cryophilus, S. octosporus, S. pombe, and S. japonicus); we selected 1718 conserved and 1718 nonconserved introns and analyzed their folding preference by generating Z-score profiles (see explanation in the Supplemental Methods).…”