Teleost genomic repeat landscapes in light of diversification rates and ecology.
Diversification
Genome dynamics
Genome size
Repetitive DNA
Short tandem repeats
Transposable elements
Journal
Mobile DNA
ISSN: 1759-8753
Titre abrégé: Mob DNA
Pays: England
ID NLM: 101519891
Informations de publication
Date de publication:
03 Oct 2023
03 Oct 2023
Historique:
received:
28
04
2023
accepted:
20
09
2023
medline:
4
10
2023
pubmed:
4
10
2023
entrez:
3
10
2023
Statut:
epublish
Résumé
Repetitive DNA make up a considerable fraction of most eukaryotic genomes. In fish, transposable element (TE) activity has coincided with rapid species diversification. Here, we annotated the repetitive content in 100 genome assemblies, covering the major branches of the diverse lineage of teleost fish. We investigated if TE content correlates with family level net diversification rates and found support for a weak negative correlation. Further, we demonstrated that TE proportion correlates with genome size, but not to the proportion of short tandem repeats (STRs), which implies independent evolutionary paths. Marine and freshwater fish had large differences in STR content, with the most extreme propagation detected in the genomes of codfish species and Atlantic herring. Such a high density of STRs is likely to increase the mutational load, which we propose could be counterbalanced by high fecundity as seen in codfishes and herring.
Identifiants
pubmed: 37789366
doi: 10.1186/s13100-023-00302-9
pii: 10.1186/s13100-023-00302-9
pmc: PMC10546739
doi:
Types de publication
Journal Article
Langues
eng
Pagination
14Subventions
Organisme : Wellcome Trust
ID : 222378
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 222378
Pays : United Kingdom
Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Levinson G, Gutman GA. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol. 1987;4:203–21.
pubmed: 3328815
Smith GP. Evolution of repeated DNA sequences by unequal crossover. Science. 1976;191:528–35.
pubmed: 1251186
doi: 10.1126/science.1251186
Ellegren H. Microsatellites: simple sequences with complex evolution. Nat Rev Genet. 2004;5:435–45.
pubmed: 15153996
doi: 10.1038/nrg1348
Pasquesi GIM, et al. Squamate reptiles challenge paradigms of genomic repeat element evolution set by birds and mammals. Nat Commun. 2018;9:2774.
pubmed: 30018307
pmcid: 6050309
doi: 10.1038/s41467-018-05279-1
Kapitonov VV, Jurka J. A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet. 2008;9:411–2.
pubmed: 18421312
doi: 10.1038/nrg2165-c1
Tørresen, et al. Tandem repeats lead to sequence assembly errors and impose multi-level challenges for genome and protein databases. Nucleic Acids Res. 2019;47:10994–1006.
pubmed: 31584084
pmcid: 6868369
doi: 10.1093/nar/gkz841
Chalopin D, Naville M, Plard F, Galiana D, Volff J-N. Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates. Genome Biol Evol. 2015;7:567–80.
pubmed: 25577199
pmcid: 4350176
doi: 10.1093/gbe/evv005
Canapa A, Barucca M, Biscotti MA, Forconi M, Olmo E. Transposons, genome size, and evolutionary insights in animals. Cytogenet Genome Res. 2015;147:217–39.
pubmed: 26967166
doi: 10.1159/000444429
Kapusta A, Suh A, Feschotte C. Dynamics of genome size evolution in birds and mammals. Proc Natl Acad Sci U S A. 2017;114:E1460–9.
pubmed: 28179571
pmcid: 5338432
doi: 10.1073/pnas.1616702114
Carducci F, Barucca M, Canapa A, Carotti E, Biscotti MA. Mobile elements in ray-finned fish genomes. Life (Basel). 2020;10:221.
pubmed: 32992841
Gao B, et al. The contribution of transposable elements to size variations between four teleost genomes. Mob DNA. 2016;7:4.
pubmed: 26862351
pmcid: 4746887
doi: 10.1186/s13100-016-0059-7
Yuan Z, et al. Comparative genome analysis of 52 fish species suggests differential associations of repetitive elements with their living aquatic environments. BMC Genomics. 2018;19:141.
pubmed: 29439662
pmcid: 5811955
doi: 10.1186/s12864-018-4516-1
Tenaillon MI, Hollister JD, Gaut BS. A triptych of the evolution of plant transposable elements. Trends Plant Sci. 2010;15:471–8.
pubmed: 20541961
doi: 10.1016/j.tplants.2010.05.003
Hancock JM. Genome size and the accumulation of simple sequence repeats: implications of new data from genome sequencing projects. Genetica. 2002;115:93–103.
pubmed: 12188051
doi: 10.1023/A:1016028332006
Hancock JM. Simple sequences and the expanding genome. BioEssays. 1996;18:421–5.
pubmed: 8639165
doi: 10.1002/bies.950180512
Mayer C, Leese F, Tollrian R. Genome-wide analysis of tandem repeats in Daphnia pulex - a comparative approach. BMC Genomics. 2010;11:277.
pubmed: 20433735
pmcid: 3152781
doi: 10.1186/1471-2164-11-277
Morgante M, Hanafey M, Powell W. Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet. 2002;30:194–200.
pubmed: 11799393
doi: 10.1038/ng822
Hardie DC, Hebert PDN. Genome-size evolution in fishes. Can J Fish Aquat Sci. 2004;61:1636–46.
doi: 10.1139/f04-106
Almojil D, et al. The structural, functional and evolutionary impact of transposable elements in eukaryotes. Genes (Basel). 2021;12:918.
pubmed: 34203645
doi: 10.3390/genes12060918
McClintock B. The significance of responses of the genome to challenge. Science. 1984;226:792–801.
pubmed: 15739260
doi: 10.1126/science.15739260
Schrader L, et al. Transposable element islands facilitate adaptation to novel environments in an invasive species. Nat Commun. 2014;5:5495.
pubmed: 25510865
doi: 10.1038/ncomms6495
Rebollo R, Horard B, Hubert B, Vieira C. Jumping genes and epigenetics: towards new species. Gene. 2010;454:1–7.
pubmed: 20102733
doi: 10.1016/j.gene.2010.01.003
Ricci M, Peona V, Guichard E, Taccioli C, Boattini A. Transposable elements activity is positively related to rate of speciation in mammals. J Mol Evol. 2018;86:303–10.
pubmed: 29855654
pmcid: 6028844
doi: 10.1007/s00239-018-9847-7
de Boer JG, Yazawa R, Davidson WS, Koop BF. Bursts and horizontal evolution of DNA transposons in the speciation of pseudotetraploid salmonids. BMC Genomics. 2007;8:422.
pubmed: 18021408
pmcid: 2198921
doi: 10.1186/1471-2164-8-422
Brawand D, et al. The genomic substrate for adaptive radiation in African cichlid fish. Nature. 2014;513:375–81.
pubmed: 25186727
pmcid: 4353498
doi: 10.1038/nature13726
Salzburger W. Understanding explosive diversification through cichlid fish genomics. Nat Rev Genet. 2018;19:705–17.
pubmed: 30111830
doi: 10.1038/s41576-018-0043-9
Gemayel R, et al. Variable Glutamine-Rich repeats modulate transcription factor activity. Mol Cell. 2015;59:615–27.
pubmed: 26257283
pmcid: 4543046
doi: 10.1016/j.molcel.2015.07.003
Gymrek M, et al. Abundant contribution of short tandem repeats to gene expression variation in humans. Nat Genet. 2016;48:22–9.
pubmed: 26642241
doi: 10.1038/ng.3461
Press MO, McCoy RC, Hall AN, Akey JM, Queitsch C. Massive variation of short tandem repeats with functional consequences across strains of. Genome Res. 2018;28:1169–78.
pubmed: 29970452
pmcid: 6071631
doi: 10.1101/gr.231753.117
Reinar WB, Olsson Lalun V, Reitan T, Jakobsen KS, Butenko MA. Length variation in short tandem repeats affects gene expression in natural populations of Arabidopsis thaliana. Plant Cell. 2021;33(7):2221–34.
Adams RH, et al. Microsatellite landscape evolutionary dynamics across 450 million years of vertebrate genome evolution. Genome. 2016;59:295–310.
pubmed: 27064176
doi: 10.1139/gen-2015-0124
Tørresen OK, et al. An improved genome assembly uncovers prolific tandem repeats in Atlantic cod. BMC Genomics. 2017;18:95.
pubmed: 28100185
pmcid: 5241972
doi: 10.1186/s12864-016-3448-x
Tørresen OK, et al. Genomic architecture of haddock (Melanogrammus aeglefinus) shows expansions of innate immune genes and short tandem repeats. BMC Genomics. 2018;19:240.
pubmed: 29636006
pmcid: 5894186
doi: 10.1186/s12864-018-4616-y
Willems T, et al. The landscape of human STR variation. Genome Res. 2014;24:1894–904.
pubmed: 25135957
pmcid: 4216929
doi: 10.1101/gr.177774.114
Reinar WB, et al. Adaptive protein evolution through length variation of short tandem repeats in Arabidopsis. Sci Adv. 2023;9(12):eadd6960.
Simon M, Hancock JM. Tandem and cryptic amino acid repeats accumulate in disordered regions of proteins. Genome Biol. 2009;10:R59.
pubmed: 19486509
pmcid: 2718493
doi: 10.1186/gb-2009-10-6-r59
Huntley MA, Clark AG. Evolutionary analysis of amino acid repeats across the genomes of 12 Drosophila species. Mol Biol Evol. 2007;24:2598–609.
pubmed: 17602168
doi: 10.1093/molbev/msm129
Quilez J, et al. Polymorphic tandem repeats within gene promoters act as modifiers of gene expression and DNA methylation in humans. Nucleic Acids Res. 2016;44:3750–62.
pubmed: 27060133
pmcid: 4857002
doi: 10.1093/nar/gkw219
Vinces MD, Legendre M, Caldara M, Hagihara M, Verstrepen KJ. Unstable tandem repeats in promoters confer transcriptional evolvability. Science. 2009;324:1213–6.
pubmed: 19478187
pmcid: 3132887
doi: 10.1126/science.1170097
Hefferon TW, Groman JD, Yurk CE, Cutting GR. A variable dinucleotide repeat in the CFTR gene contributes to phenotype diversity by forming RNA secondary structures that alter splicing. Proc Natl Acad Sci U S A. 2004;101:3504–9.
pubmed: 14993601
pmcid: 373492
doi: 10.1073/pnas.0400182101
Malmstrøm M, et al. Evolution of the immune system influences speciation rates in teleost fishes. Nat Genet. 2016;48:1204–10.
pubmed: 27548311
doi: 10.1038/ng.3645
Malmstrøm M, Matschiner M, Tørresen OK, Jakobsen KS, Jentoft S. Whole genome sequencing data and de novo draft assemblies for 66 teleost species. Scientific Data. 2017;4:160132.
pubmed: 28094797
pmcid: 5240625
doi: 10.1038/sdata.2016.132
Musilova Z, et al. Vision using multiple distinct rod opsins in deep-sea fishes. Science. 2019;364:588–92.
pubmed: 31073066
pmcid: 6628886
doi: 10.1126/science.aav4632
Froese R, Pauly D. 06/2018. FishBase. www.fishbase.org .
Balon EK. 1990. Epigenesis of an epigeneticist: the development of some alternative concepts on the early ontogeny and evolution of fishes. 1. 1. https://journal.lib.uoguelph.ca/index.php/gir/article/view/64 (Accessed 17 Sept 2019).
Scholl JP, Wiens JJ. Diversification rates and species richness across the Tree of Life. Proc. Biol. Sci. 2016;283. https://doi.org/10.1098/rspb.2016.1334 .
Kolm N, Ahnesjo I. Do egg size and parental care coevolve in fishes? J Fish Biol. 2005;66:1499–515.
doi: 10.1111/j.0022-1112.2005.00777.x
Duarte CM, Alcaraz M. To produce many small or few large eggs: a size-independent reproductive tactic of fish. Oecologia. 1989;80:401–4.
pubmed: 28312069
doi: 10.1007/BF00379043
Graur D. An upper limit on the functional fraction of the human genome. Genome Biol Evol. 2017;9:1880–5.
pubmed: 28854598
pmcid: 5570035
doi: 10.1093/gbe/evx121
Nei M. 2013. Mutation-Driven Evolution. OUP Oxford.
Barneche DR, Robertson DR, White CR, Marshall DJ. Fish reproductive-energy output increases disproportionately with body size. Science. 2018;360:642–5.
pubmed: 29748282
doi: 10.1126/science.aao6868
Brunet TDP, Doolittle WF. Multilevel selection theory and the evolutionary functions of transposable elements. Genome Biol Evol. 2015;7:2445–57.
pubmed: 26253318
pmcid: 4558868
doi: 10.1093/gbe/evv152
Doolittle WF, Brunet TDP. On causal roles and selected effects: our genome is mostly junk. BMC Biol. 2017;15:116.
pubmed: 29207982
pmcid: 5718017
doi: 10.1186/s12915-017-0460-9
Doolittle WF, Sapienza C. Selfish genes, the phenotype paradigm and genome evolution. Nature. 1980;284:601–3.
pubmed: 6245369
doi: 10.1038/284601a0
Santos ME, et al. The evolution of cichlid fish egg-spots is linked with a cis-regulatory change. Nat Commun. 2014;5:5149.
pubmed: 25296686
doi: 10.1038/ncomms6149
Simpson JT, Pop M. The theory and practice of genome sequence assembly. Annu Rev Genomics Hum Genet. 2015;16:153–72.
pubmed: 25939056
doi: 10.1146/annurev-genom-090314-050032
Treangen TJ, Salzberg SL. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet. 2011;13:36–46.
pubmed: 22124482
pmcid: 3324860
doi: 10.1038/nrg3117
Smit A, Hubley R. 2008–2015. RepeatModeler Open-1.0. http://www.repeatmasker.org .
Ellinghaus D, Kurtz S, Willhoeft U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics. 2008;9:18.
pubmed: 18194517
pmcid: 2253517
doi: 10.1186/1471-2105-9-18
Wheeler TJ, Eddy SR. nhmmer: DNA homology search with profile HMMs. Bioinformatics. 2013;29:2487–9.
pubmed: 23842809
pmcid: 3777106
doi: 10.1093/bioinformatics/btt403
Llorens C, et al. The Gypsy Database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res. 2011;39:D70–4.
pubmed: 21036865
doi: 10.1093/nar/gkq1061
Hubley R, et al. The Dfam database of repetitive DNA families. Nucleic Acids Res. 2016;44:D81–9.
pubmed: 26612867
doi: 10.1093/nar/gkv1272
Goubert C, Modolo L, Vieira C, ValienteMoro C, Mavingui P, Boulesteix M. De Novo Assembly and Annotation of the Asian Tiger Mosquito (Aedes albopictus) Repeatome with dnaPipeTE from Raw Genomic Reads and Comparative Analysis with the Yellow Fever Mosquito (Aedes aegypti). 2015. Genome Biol. Evol. 7:1192-1205
Betancur-R R et al. The tree of life and a new classification of bony fishes. PLoS Curr Tree of Life. 2013. Edition 1.
Magallón S, Sanderson MJ. Absolute diversification rates in angiosperm clades. Evolution. 2001;55:1762–80.
pubmed: 11681732
Rabosky DL, et al. An inverse latitudinal gradient in speciation rate for marine fishes. Nature. 2018;559:392.
pubmed: 29973726
doi: 10.1038/s41586-018-0273-1
Orme, D et al. CAPER: comparative analyses of phylogenetics and evolution in R. 2018. R package version 1.0.1.
Manni M, Berkeley MR, Seppey M, Simão F, Zdobnov E. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol. 2021;38:4647–54.
pubmed: 34320186
pmcid: 8476166
doi: 10.1093/molbev/msab199