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Cited by 28Chromosomal and Genetic VariationsGenomics and Phylogenetic StudiesGenome Rearrangement Algorithms

Comparative Analysis of Teleost Genome Sequences Reveals an Ancient Intron Size Expansion in the Zebrafish Lineage

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Moss, Stephen P., Joyce, Domino A., Humphries, Stuart, Tindall, Katherine J., Lunt, David H.·2011·Genome Biology and Evolution
DOI 10.1093/gbe/evr090PMC PMC3205604
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Abstract

We have developed a bioinformatics pipeline for the comparative evolutionary analysis of Ensembl genomes and have used it to analyze the introns of the five available teleost fish genomes. We show our pipeline to be a powerful tool for revealing variation between genomes that may otherwise be overlooked with simple summary statistics. We identify that the zebrafish, Danio rerio, has an unusual distribution of intron sizes, with a greater number of larger introns in general and a notable peak in the frequency of introns of approximately 500 to 2,000 bp compared with the monotonically decreasing frequency distributions of the other fish. We determine that 47% of D. rerio introns are composed of repetitive sequences, although the remainder, over 331 Mb, is not. Because repetitive elements may be the origin of the majority of all noncoding DNA, it is likely that the remaining D. rerio intronic sequence has an ancient repetitive origin and has since accumulated so many mutations that it can no longer be recognized as such. To study such an ancient expansion of repeats in the Danio, lineage will require further comparative analysis of fish genomes incorporating a broader distribution of teleost lineages.

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  • Changes in intron lengths have been shown to be a significant part of genomic truncations and expansions, such as severe intron shortening in Paedocypris or intron expansion in zebrafish.

    “Changes in the intron lengths have been shown to be a significant part of genomic truncations and expansions, such as a severe intron shortening in another miniature fish species, Paedocypris35, or an intron expansion in zebrafish36.”

    From Hybrid genome assembly and annotation of Danionella translucida (2019) · cites this paper as [36]

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Research works printed but not linked: 52

  1. Adams MD Rudner DZ Rio DC Biochemistry and regulation of pre-mRNA splicing Curr Opin Cell Biol. 1996 8 331 339 8743883
  2. Aparicio S Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes Science 2002 297 1301 1310 12142439
  3. Benson G Tandem repeats finder: a program to analyze DNA sequences Nucleic Acids Res. 1999 27 573 580 9862982 PMC148217
  4. Bergman CM Quesneville H Discovering and detecting transposable elements in genome sequences Brief Bioinform. 2007 8 382 392 17932080
  5. Bosco G Campbell P Leiva-Neto JT Markow TA Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species Genetics 2007 177 1277 1290 18039867 PMC2147996
  6. Boulesteix M Weiss M Biémont C Differences in genome size between closely related species: the Drosophila melanogaster species subgroup Mol Biol Evol. 2006 23 162 167 16151184
  7. Burnette JM Miyamoto-Sato E Schaub MA Conklin J Lopez AJ Subdivision of large introns in Drosophila by recursive splicing at nonexonic elements Genetics 2005 170 661 674 15802507 PMC1450422
  8. Castillo-Davis CI Mekhedov SL Hartl DL Koonin EV Kondrashov FA Selection for short introns in highly expressed genes Nat Genet. 2002 31 415 418 12134150
  9. Chamary J-V Hurst LD Similar rates but different modes of sequence evolution in introns and at exonic silent sites in rodents: evidence for selectively driven codon usage Mol Biol Evol. 2004 21 1014 1023 15014158
  10. Coghlan A Wolfe KH Origins of recently gained introns in Caenorhabditis Proc Natl Acad Sci U S A. 2004 101 11362 11367 15243155 PMC509176
  11. Deutsch M Long M Intron-exon structures of eukaryotic model organisms Nucleic Acids Res. 1999 27 3219 3228 10454621 PMC148551
  12. Flicek P Ensembl 2011 Nucleic Acids Res. 2010 39 D800 D806 21045057 PMC3013672
  13. Frischmeyer PA Dietz HC Nonsense-mediated mRNA decay in health and disease Hum Mol Genet. 1999 8 1893 1900 10469842
  14. Gaffney DJ Keightley PD Genomic selective constraints in murid noncoding DNA PLoS Genet. 2006 2 e204 17166057 PMC1657059
  15. Gazave E Marqués-Bonet T Fernando O Charlesworth B Navarro A Patterns and rates of intron divergence between humans and chimpanzees Genome Biol. 2007 8 R21 17309804 PMC1852421
  16. Haffter P The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio Development 1996 123 1 36 9007226
  17. Hankeln T Friedl H Ebersberger I Martin J Schmidt ER A variable intron distribution in globin genes of Chironomus: evidence for recent intron gain Gene 1997 205 151 160 9461389
  18. Hatton AR Subramaniam V Lopez AJ Generation of alternative Ultrabithorax isoforms and stepwise removal of a large intron by resplicing at exon–exon junctions Mol Cell. 1998 2 787 796 9885566
  19. Hawkins JS Kim H Nason JD Wing RA Wendel JF Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium Genome Res. 2006 16 1252 1261 16954538 PMC1581434
  20. Hughes AL Yeager M Comparative evolutionary rates of introns and exons in murine rodents J Mol Evol. 1997 45 125 130 9236271
  21. Jaillon O Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype Nature 2004 431 946 957 15496914
  22. Jeffares DC Penkett CJ Bähler J Rapidly regulated genes are intron poor Trends Genet. 2008 24 375 378 18586348
  23. Jurka J Repbase Update, a database of eukaryotic repetitive elements Cytogenet Genome Res. 2005 110 462 467 16093699
  24. Kim E Magen A Ast G Different levels of alternative splicing among eukaryotes Nucleic Acids Res. 2007 35 125 131 17158149 PMC1802581
  25. Kimura T Large-scale isolation of ESTs from medaka embryos and its application to medaka developmental genetics Mech Dev. 2004 121 915 932 15210196
  26. Lander ES Initial sequencing and analysis of the human genome Nature 2001 409 860 921 11237011
  27. Li W Tucker AE Sung W Thomas WK Lynch M Extensive, recent intron gains in Daphnia populations Science 2009 326 1260 1262 19965475 PMC3878872
  28. Lin C-F Mount SM Jarmołowski A Makałowski W Evolutionary dynamics of U12-type spliceosomal introns BMC Evol Biol. 2010 10 47 20163699 PMC2831892
  29. López-Bigas N Audit B Ouzounis C Parra G Guigó R Are splicing mutations the most frequent cause of hereditary disease? FEBS Lett. 2005 579 1900 1903 15792793
  30. Majewski J Ott J Distribution and characterization of regulatory elements in the human genome Genome Res. 2002 12 1827 1836 12466286 PMC187578
  31. Marais G Nouvellet P Keightley PD Charlesworth B Intron size and exon evolution in Drosophila Genetics 2005 170 481 485 15781704 PMC1449718
  32. Mills RE Bennett EA Iskow RC Devine SE Which transposable elements are active in the human genome? Trends Genet. 2007 23 183 191 17331616
  33. Mironov AA Fickett JW Gelfand MS Frequent alternative splicing of human genes Genome Res. 1999 9 1288 1293 10613851 PMC310997
  34. Morgulis A Gertz EM Schäffer AA Agarwala R WindowMasker: window-based masker for sequenced genomes Bioinformatics 2006 22 134 141 16287941
  35. Neafsey DE Palumbi SR Genome size evolution in pufferfish: a comparative analysis of diodontid and tetraodontid pufferfish genomes Genome Res. 2003 13 821 830 12727902 PMC430906
  36. Roest Crollius H Weissenbach J Fish genomics and biology Genome Res. 2005 15 1675 1682 16339365
  37. Rogers J How were introns inserted into nuclear genes? Trends Genet. 1989 5 213 216 2551082
  38. Roy SW Gilbert W The evolution of spliceosomal introns: patterns, puzzles and progress Nat Rev Genet. 2006 7 211 221 16485020
  39. Schwartz SH Large-scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes Genome Res. 2008 18 88 103 18032728 PMC2134773
  40. Sela N Kim E Ast G The role of transposable elements in the evolution of non-mammalian vertebrates and invertebrates Genome Biol. 2010 11 R59 20525173 PMC2911107
  41. Sharp PA On the origin of RNA splicing and introns Cell 1985 42 397 400 2411416
  42. Sharpton TJ Neafsey DE Galagan JE Taylor JW Mechanisms of intron gain and loss in Cryptococcus Genome Biol. 2008 9 R24 18234113 PMC2395259
  43. Shepard S McCreary M Fedorov A The peculiarities of large intron splicing in animals PloS One. 2009 4 e7853 19924226 PMC2773006
  44. Smit AF Interspersed repeats and other mementos of transposable elements in mammalian genomes Curr Opin Genet Dev. 1999 9 657 663 10607616
  45. Stabenau A The Ensembl core software libraries Genome Res. 2004 14 929 933 15123588 PMC479122
  46. Stajich JE Dietrich FS Roy SW Comparative genomic analysis of fungal genomes reveals intron-rich ancestors Genome Biol 2007 8 R223 PMC2246297 17949488
  47. Stajich JE The Bioperl toolkit: Perl modules for the life sciences Genome Res 2002 12 1611 1618 12368254 PMC187536
  48. Stein LD The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics PLoS Biol. 2003 1 E45 14624247 PMC261899
  49. Venter JC The sequence of the human genome Science 2001 291 1304 1351 11181995
  50. Yandell M Large-scale trends in the evolution of gene structures within 11 animal genomes PLoS Comput Biol. 2006 2 e15 16518452 PMC1386723
  51. Zhu L Patterns of exon-intron architecture variation of genes in eukaryotic genomes BMC Genomics. 2009 10 47 19166620 PMC2636830
  52. Zhuang YA Goldstein AM Weiner AM UACUAAC is the preferred branch site for mammalian mRNA splicing Proc Natl Acad Sci U S A. 1989 86 2752 2756 2704744 PMC286996

Cited by

Sorted by citations

Authors
Moss, S. P., Joyce, D. A., Humphries, S., Tindall, K. J., & Lunt, D. H.
Affiliations
University of Hull (GB)
Corresponding author
Lunt, David H.
ORCID
Venue
Genome Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2011-01-01
Volume
3
Pages
1187-1196
ISSN
1759-6653 (ISSN-L)
DOI
10.1093/gbe/evr090
PMC
PMC3205604
OpenAlex
W2159406349
Cited by
28
References
3
Citations by year
2026: 1 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 1 · 2020: 1 · 2019: 2 · 2018: 4 · 2017: 4 · 2016: 1 · 2015: 3 · 2014: 3 · 2013: 2 · 2012: 2
FWCI
2.51
Type
journal article
Language
en
Open access
Licence
Locations
  • Genome Biology and Evolution (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Lincoln Repository (University of Lincoln) (acceptedVersion)
  • Repository@Hull (Worktribe) (University of Hull) (acceptedVersion, other-oa)
  • Figshare (submittedVersion, cc-by)
Funders
  • University of Hull
  • Natural Environment Research Council
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
Keywords
intron size, teleost genomes, zebrafish, comparative genomics, repetitive DNA, non-coding DNA, genome evolution, bioinformatics pipeline
MeSH terms
Animals, Introns, Zebrafish, Genome, Evolution, Molecular

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