On biased distribution of introns in various eukaryotes

Sakurai, Atsushi; Fujimori, Shigeo; Kochiwa, Hiromi; Kitamura-Abe, Sumie; Washio, Takumi; Saito, Rintaro; Carninci, Piero; Hayashizaki, Yoshihide; Tomita, Masaru

doi:10.1016/s0378-1119(02)01035-1

Cited by 63 publications

(57 citation statements)

References 29 publications

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“…With rare exceptions, intron-poor unicellular eukaryotes have been found to have a significant 5Ј bias in intron position, a property not observed in metazoan genes (31,37). Our analyses of T. vaginalis introns are consistent with these findings, because introns are typically found within the first one-third of the gene.…”

Section: Discussionsupporting

confidence: 83%

“…Our analyses of T. vaginalis introns are consistent with these findings, because introns are typically found within the first one-third of the gene. These data support the argument that the paucity of introns in unicellular eukaryotes results from a secondary loss, driven by homologous recombination between the gene and an intronless cDNA derived by reverse transcription of the corresponding mRNA (31,37,38), as opposed to introns simply being less abundant during early eukaryotic evolution.…”

Section: Discussionsupporting

confidence: 82%

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Spliceosomal introns in the deep-branching eukaryote Trichomonas vaginalis

Vaňáčová

Wang

Carlton

et al. 2005

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

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Eukaryotes have evolved elaborate splicing mechanisms to remove introns that would otherwise destroy the protein-coding capacity of genes. Nuclear premRNA splicing requires sequence motifs in the intron and is mediated by a ribonucleoprotein complex, the spliceosome. Here we demonstrate the presence of a splicing apparatus in the protist Trichomonas vaginalis and show that RNA motifs found in yeast and metazoan introns are required for splicing. We also describe the first introns in this deep-branching lineage. The positions of these introns are often conserved in orthologous genes, indicating they were present in a common ancestor of trichomonads, yeast, and metazoa. All examined T. vaginalis introns have a highly conserved 12-nt 3 splice-site motif that encompasses the branch point and is necessary for splicing. This motif is also found in the only described intron in a gene from another deep-branching eukaryote, Giardia intestinalis. These studies demonstrate the conservation of intron splicing signals across large evolutionary distances, reveal unexpected motif conservation in deep-branching lineages that suggest a simplified mechanism of splicing in primitive unicellular eukaryotes, and support the presence of introns in the earliest eukaryote.evolution ͉ gene expression ͉ old introns ͉ splicing S plicing of nuclear premRNA plays a central role in eukaryotic gene expression and contributes to gene regulation and protein diversity (1, 2). Splice-site (SS) motifs, recognized by small nuclear RNAs and protein components of the spliceosome, coordinate multiple steps in splicing (1). Precision is required to generate mRNAs that encode functional proteins, yet the SS motifs that define exon͞intron junctions are short and often weakly conserved. Two types of spliceosomal introns, U2-and U12-dependent, have been described in eukaryotes (reviewed in ref.3). Groups I and II introns, capable of self splicing in vitro and present in some eubacterial genomes, are also found in organellar genomes of unicellular eukaryotes and plants (reviewed in refs. 4 and 5). Most spliceosomal introns are U2-dependent and are bordered at the 5Ј end by a consensus of 6 nt, encompassing the invariant 5Ј GT. The 5Ј splice-site consensus in yeast (Saccharomyces cerevisiae) introns is generally highly conserved, whereas the consensus in mammalian introns is often limited to the 5Ј GT. The 3Ј SS motif of mammalian and yeast U2-dependent introns is shorter and typically limited to the last 3 nt (T͞CAG3Ј) (1,3,6,7). In addition to the 5Ј and 3Ј SS motifs, yeast introns also require a conserved branch-point sequence (TACTAAC), which is only loosely conserved in mammalian U2-dependent introns.Spliceosomal introns are common in animal and plant genes, absent in eubacterial and archaeal genes, and found in several unicellular protists. The prevalence of splicing in protists is unknown, and the properties of protist introns vary considerably. In euglenoids and trypanosomes, both transsplicing and cissplicing U2-dependent introns are present (8). Al...

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Section: Discussionsupporting

confidence: 83%

Section: Discussionsupporting

confidence: 82%

Spliceosomal introns in the deep-branching eukaryote Trichomonas vaginalis

Vaňáčová

Wang

Carlton

et al. 2005

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

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“…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)(4)(5)(6)(7)(8)(9).…”

mentioning

confidence: 99%

“…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)(11)(12)(13)(14)(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.…”

mentioning

confidence: 99%

The pattern of intron loss

Roy

Gilbert

2005

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

121

117

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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...

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“…Although most BrTUA retained four introns as in the case of AtTUA, the length ranged from 65 to 2100 bp and a 128-bp regulatory sequence was observed to be inserted ahead of the first codon in Bra020572. The position of introns also changed significantly; they were distributed in every region of the genes, whereas introns of plant microtubule genes were mostly distributed in the 5'-end (Dibb and Newman, 1989;Sakurai et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

Regulation of bolting and identification of the α-tubulin gene family in Brassica rapa L. ssp pekinensis

Jin

et al. 2016

Genet. Mol. Res.

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ABSTRACT.Microtubules are important components of eukaryotic cells, and they play vital roles in cell morphogenesis, carrying of signaling molecules, transport of materials, and establishing the cell polarity. During bolting of biennial plants, cell division and elongation are involved, and cell elongation inevitably involves the microtubules arrangement and expression of related genes. So we deduce that it is of great significance to figure out the mechanism of bolting and flowering in which TUA genes are involved. In the present study, bioinformatic methods were used to predict and identify the α-tubulin gene family (BrTUAs) in Brassica rapa L. ssp pekinensis (Chinese cabbage) through the alignment of AtTUA gene sequence from Arabidopsis thaliana with the B. rapa genome database (http://brassicadb.org/brad/) using the basic local alignment search tool. The change in the structure and functions of BrTUAs during the process of evolution, cis-acting elements in the promoter sequences of BrTUAs, and the expression of the identified genes was also analyzed. Twelve members of the α-tubulin gene family were identified from Chinese cabbage. The gene length, intron, exon, and promoter regions were determined to have changed significantly during the genome evolution. Only five of the 12 members were encoded completely and were observed to differ in their spatial and temporal expression. The five BrTUA promoter sequences contained different numbers of cis-elements responsive to light and lowtemperature response, cis-elements responsive among which hormonal responses were significantly different. We also report that the BrTUAs were involved in the regulation of the bolting in Chinese cabbage, and propose that this process could be controlled by regulating the expression of BrTUAs.

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On biased distribution of introns in various eukaryotes

Cited by 63 publications

References 29 publications

Spliceosomal introns in the deep-branching eukaryote Trichomonas vaginalis

Spliceosomal introns in the deep-branching eukaryote Trichomonas vaginalis

The pattern of intron loss

Regulation of bolting and identification of the α-tubulin gene family in Brassica rapa L. ssp pekinensis

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