Cited by 17Chromosomal and Genetic VariationsGenomics and Phylogenetic StudiesRNA Research and Splicing

Intron size minimisation in teleosts

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Jakt, Lars Martin, Dubin, Arseny, Johansen, Steinar Daae·2022·BMC Genomics

Abstract

Background: Spliceosomal introns are parts of primary transcripts that are removed by RNA splicing. Although introns apparently do not contribute to the function of the mature transcript, in vertebrates they comprise the majority of the transcribed region increasing the metabolic cost of transcription. The persistence of long introns across evolutionary time suggests functional roles that can offset this metabolic cost. The teleosts comprise one of the largest vertebrate clades. They have unusually compact and variable genome sizes and provide a suitable system for analysing intron evolution. Results: We have analysed intron lengths in 172 vertebrate genomes and show that teleost intron lengths are relatively short, highly variable and bimodally distributed. Introns that were long in teleosts were also found to be long in mammals and were more likely to be found in regulatory genes and to contain conserved sequences. Our results argue that intron length has decreased in parallel in a non-random manner throughout teleost evolution and represent a deviation from the ancestral state. Conclusion: Our observations indicate an accelerated rate of intron size evolution in the teleosts and that teleost introns can be divided into two classes by their length. Teleost intron sizes have evolved primarily as a side-effect of genome size evolution and small genomes are dominated by short introns (<256 base pairs). However, a non-random subset of introns has resisted this process across the teleosts and these are more likely have functional roles in all vertebrate clades.

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  • Teleost introns fall into two functional classes: compact introns containing primarily sequences necessary for efficient splicing, and long introns disproportionately harboring regulatory elements and conserved sequences maintained across vertebrates.

    “This is consistent with the observation that teleost introns fall into two functional classes: compact introns containing primarily sequences necessary for efficient splicing, and long introns disproportionately harboring regulatory elements and conserved sequences maintained across vertebrates (68).”

    From Convergent genome streamlining accompanies independent miniaturization in the world’s smallest fishes (2026) · cites this paper as [68]

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Research works printed but not linked: 48

  1. [1]Rogozin IB Carmel L Csuros M Koonin EV Origin and evolution of spliceosomal introns Biol Direct 2012 7 1 11 10.1186/1745-6150-7-11 22507701 PMC3488318 · DOI
  2. [2]Irimia M Roy SW Origin of Spliceosomal Introns and Alternative Splicing Cold Spring Harb Perspect Biol 2014 6 6 a016071 10.1101/cshperspect.a016071 24890509 PMC4031966 · DOI
  3. [3]Lee Y Rio DC Mechanisms and Regulation of Alternative Pre-mRNA Splicing Ann Rev Biochem 2015 84 291 323 10.1146/annurev-biochem-060614-034316 25784052 PMC4526142 · DOI · Paper page
  4. [4]Le Hir H Saulière J Wang Z The exon junction complex as a node of post-transcriptional networks Nat Rev Mol Cell Biol 2016 17 1 41 54 10.1038/nrm.2015.7 26670016 · DOI
  5. [5]Sollner-Webb B Novel intron-encoded small nucleolar RNAs Cell 1993 75 3 403 5 10.1016/0092-8674(93)90374-Y 8221882 · DOI
  6. [6]Caffarelli E Fatica A Prislei S De Gregorio E Fragapane P Bozzoni I Processing of the intron-encoded U16 and U18 snoRNAs: the conserved C and D boxes control both the processing reaction and the stability of the mature snoRNA EMBO J 1996 15 5 1121 31 10.1002/j.1460-2075.1996.tb00450.x 8605882 PMC450010 · DOI
  7. [7]Tycowski KT Shu MD Steitz JA A mammalian gene with introns instead of exons generating stable RNA products Nature 1996 379 6564 464 6 10.1038/379464a0 8559254 · DOI
  8. [8]Bortolin ML Kiss T Human U19 intron-encoded snoRNA is processed from a long primary transcript that possesses little potential for protein coding RNA 1998 4 4 445 54 9630250 PMC1369630
  9. [10]Fedorov A Merican AF Gilbert W Large-scale comparison of intron positions among animal, plant, and fungal genes Proc Natl Acad Sci 2002 99 25 16128 33 10.1073/pnas.242624899 12444254 PMC138576 · DOI
  10. [12]Denoeud F Henriet S Mungpakdee S Aury JM Silva CD Brinkmann H Plasticity of Animal Genome Architecture Unmasked by Rapid Evolution of a Pelagic Tunicate Science 2010 330 6009 1381 5 10.1126/science.1194167 21097902 PMC3760481 · DOI · Paper page
  11. [13]Shaul O How introns enhance gene expression Int J Biochem Cell Biol 2017 91 145 55 10.1016/j.biocel.2017.06.016 28673892 · DOI
  12. [14]Carvalho AB Clark AG Intron size and natural selection Nature 1999 401 6751 344 4 10.1038/43827 10517631 · DOI
  13. [15]Castillo-Davis CI Mekhedov SL Hartl DL Koonin EV Kondrashov FA Selection for short introns in highly expressed genes Nat Genet 2002 31 4 415 8 10.1038/ng940 12134150 · DOI
  14. [16]Hara Y Yamaguchi K Onimaru K Kadota M Koyanagi M Keeley SD Shark genomes provide insights into elasmobranch evolution and the origin of vertebrates Nat Ecol Evol 2018 2 11 1761 71 10.1038/s41559-018-0673-5 30297745 · DOI
  15. [17]Pozzoli U Menozzi G Comi GP Cagliani R Bresolin N Sironi M Intron size in mammals: complexity comes to terms with economy Trends Genet 2007 23 1 20 4 10.1016/j.tig.2006.10.003 17070957 · DOI
  16. [18]Nowoshilow S Schloissnig S Fei JF Dahl A Pang AWC Pippel M The axolotl genome and the evolution of key tissue formation regulators Nature 2018 554 7690 50 5 10.1038/nature25458 29364872 · DOI
  17. [19]Meyer A Schloissnig S Franchini P Du K Woltering JM Irisarri I Giant lungfish genome elucidates the conquest of land by vertebrates Nature 2021 590 7845 284 9 10.1038/s41586-021-03198-8 33461212 PMC7875771 · DOI · Paper page
  18. [20]Dubin A, Jørgensen TE, Moum TB, Johansen SD, Jakt LM. Complete loss of the MHC II pathway in an anglerfish, Lophius piscatorius. 2019. https://nordopen.nord.no/nord-xmlui/handle/11250/2658241. PMC6832177 31594494
  19. [22]Yu J Yang Z Kibukawa M Paddock M Passey DA Wong GKS Minimal Introns Are Not “Junk” Genome Res 2002 12 8 1185 9 10.1101/gr.224602 12176926 PMC186636 · DOI
  20. [23]Marais G Nouvellet P Keightley PD Charlesworth B Intron Size and Exon Evolution in Drosophila Genetics 2005 170 1 481 5 10.1534/genetics.104.037333 15781704 PMC1449718 · DOI
  21. [24]Chorev M Carmel L Computational identification of functional introns: high positional conservation of introns that harbor RNA genes Nucleic Acids Res 2013 41 11 5604 13 10.1093/nar/gkt244 23605046 PMC3675471 · DOI
  22. [25]Pai AA Henriques T McCue K Burkholder A Adelman K Burge CB The kinetics of pre-mRNA splicing in the Drosophila genome and the influence of gene architecture eLife 2017 6 e32537 10.7554/eLife.32537 29280736 PMC5762160 · DOI
  23. [26]Moss SP, Joyce DA, Humphries S, Tindall KJ, Lunt DH. Comparative Analysis of Teleost Genome Sequences Reveals an Ancient Intron Size Expansion in the Zebrafish Lineage. Genome Biol Evol. 2011. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3205604/. PMC3205604 21920901
  24. [27]Organ CL Shedlock AM Palaeogenomics of pterosaurs and the evolution of small genome size in flying vertebrates Biol Lett 2009 5 1 47 50 10.1098/rsbl.2008.0491 18940771 PMC2657748 · DOI
  25. [28]Waltari E Edwards SV Evolutionary dynamics of intron size, genome size, and physiological correlates in archosaurs Am Nat 2002 160 5 539 52 10.1086/342079 18707506 · DOI
  26. [29]Eisenberg E Levanon EY Human housekeeping genes are compact Trends Genet 2003 19 7 362 5 10.1016/S0168-9525(03)00140-9 12850439 · DOI
  27. [30]Wieringa B Hofer E Weissmann C A minimal intron length but no specific internal sequence is required for splicing the large rabbit β-globin intron Cell 1984 37 3 915 25 10.1016/0092-8674(84)90426-4 6204770 · DOI
  28. [31]Jaillon O Aury JM Brunet F Petit JL Stange-Thomann N Mauceli E Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype Nature 2004 431 7011 946 57 10.1038/nature03025 15496914 · DOI · Paper page
  29. [32]Gregory TR A Bird’s-Eye View of the C-Value Enigma: Genome Size, Cell Size, and Metabolic Rate in the Class Aves Evolution 2002 56 1 121 30 10.1111/j.0014-3820.2002.tb00854.x 11913657 · DOI
  30. [33]Zhang Q Edwards SV The Evolution of Intron Size in Amniotes: A Role for Powered Flight? Genome Biol Evol 2012 4 10 1033 43 10.1093/gbe/evs070 22930760 PMC3490418 · DOI
  31. [34]Hardie D Hebert P. Genome-size evolution in fishes Can J Fish Aquat Sci 2004 61 1636 46 10.1139/f04-106 · DOI · Paper page
  32. [35]Seoighe C Korir PK Evidence for intron length conservation in a set of mammalian genes associated with embryonic development BMC Bioinformatics 2011 12 Suppl 9 S16 10.1186/1471-2105-12-S9-S16 22151910 PMC3283306 · DOI
  33. [36]Keane PA Seoighe C Intron Length Coevolution across Mammalian Genomes Mol Biol Evol 2016 33 10 2682 91 10.1093/molbev/msw151 27550903 PMC5026260 · DOI
  34. [37]Swinburne IA Miguez DG Landgraf D Silver PA Intron length increases oscillatory periods of gene expression in animal cells Genes Dev 2008 22 17 2342 6 10.1101/gad.1696108 18703678 PMC2532923 · DOI
  35. [38]Glazier DS Genome Size Covaries More Positively with Propagule Size than Adult Size: New Insights into an Old Problem Biology 2021 10 4 270 10.3390/biology10040270 33810583 PMC8067107 · DOI
  36. [39]Mackintosh A Laetsch DR Hayward A Charlesworth B Waterfall M Vila R The determinants of genetic diversity in butterflies Nat Commun 2019 10 1 3466 10.1038/s41467-019-11308-4 31371715 PMC6672018 · DOI
  37. [40]Romiguier J Gayral P Ballenghien M Bernard A Cahais V Chenuil A Comparative population genomics in animals uncovers the determinants of genetic diversity Nature 2014 515 7526 261 3 10.1038/nature13685 25141177 · DOI
  38. [41]Comeron JM Kreitman M The Correlation Between Intron Length and Recombination in Drosophila: Dynamic Equilibrium Between Mutational and Selective Forces Genetics 2000 156 3 1175 90 10.1093/genetics/156.3.1175 11063693 PMC1461334 · DOI
  39. [42]Mount SM Burks C Herts G Stormo GD White O Fields C Splicing signals in Drosophila: intron size, information content, and consensus sequences Nucleic Acids Res 1992 20 16 4255 62 10.1093/nar/20.16.4255 1508718 PMC334133 · DOI
  40. [44]Lefébure T Morvan C Malard F François C Konecny-Dupré L Guéguen L Less effective selection leads to larger genomes Genome Res 2017 27 6 1016 28 10.1101/gr.212589.116 28424354 PMC5453316 · DOI
  41. [45]DeWoody JA Avise JC Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals J Fish Biol 2000 56 3 461 73 10.1111/j.1095-8649.2000.tb00748.x · DOI
  42. [46]Nam K Ellegren H 8 PLoS Genet 2012 5 e1002680 10.1371/journal.pgen.1002680 PMC3342960 22570634 · DOI
  43. [47]Needleman SB Wunsch CD A general method applicable to the search for similarities in the amino acid sequence of two proteins J Mol Biol 1970 48 3 443 53 10.1016/0022-2836(70)90057-4 5420325 · DOI · Paper page
  44. [49]Kimura M A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences J Mol Evol 1980 16 2 111 20 10.1007/BF01731581 7463489 · DOI · Paper page
  45. [50]Paradis E Schliep K ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R Bioinformatics 2019 35 3 526 8 10.1093/bioinformatics/bty633 30016406 · DOI
  46. [51]Sankoff D Minimal Mutation Trees of Sequences SIAM J Appl Math 1975 28 1 35 42 10.1137/0128004 · DOI
  47. [53]Falcon S Gentleman R Using GOstats to test gene lists for GO term association Bioinformatics 2007 23 2 257 8 10.1093/bioinformatics/btl567 17098774 · DOI
  48. [54]Smith TF Waterman MS Identification of common molecular subsequences J Mol Biol 1981 147 1 195 7 10.1016/0022-2836(81)90087-5 7265238 · DOI

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Authors
Jakt, L. M., Dubin, A., & Johansen, S. D.
Affiliations
Nord University (NO)
Corresponding author
Jakt, Lars Martin
Venue
BMC Genomics
Published
2022-09-01
Volume
23
Issue
1
Pages
628-628
ISSN
1471-2164 (ISSN-L)
OpenAlex
W4294025564
Cited by
17
References
4
Citations by year
2026: 3 · 2025: 1 · 2024: 7 · 2023: 6
FWCI
2.51
Type
journal article
Language
en
Open access
Locations
  • BMC Genomics (publishedVersion, cc-by)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Helmholtz Centre for Ocean Research Kiel (GEOMAR) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • NORA - Norwegian Open Research Archives (submittedVersion, cc-by)
Funders
Nord universitet
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 › Molecular Biology › RNA Research and Splicing
Keywords
intron length, teleosts, RNA splicing, genome size evolution, vertebrate genomes, regulatory genes, conserved sequences, parallel evolution, ancestral states
MeSH terms
Animals, Exons, Introns, Mammals, Vertebrates, Genome, Evolution, Molecular

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