Advances in Vertebrate (Cyto)Genomics Shed New Light on Fish Compositional Genome Evolution
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36833171
PubMed Central
PMC9956151
DOI
10.3390/genes14020244
PII: genes14020244
Knihovny.cz E-zdroje
- Klíčová slova
- AT/GC evolution, GC content, GC landscape pipeline, compositional cytogenomics, genome evolution,
- MeSH
- DNA MeSH
- genomika MeSH
- komplementární DNA MeSH
- molekulární evoluce MeSH
- obratlovci * genetika MeSH
- ryby * genetika MeSH
- savci genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA MeSH
- komplementární DNA MeSH
Cytogenetic and compositional studies considered fish genomes rather poor in guanine-cytosine content (GC%) because of a putative "sharp increase in genic GC% during the evolution of higher vertebrates". However, the available genomic data have not been exploited to confirm this viewpoint. In contrast, further misunderstandings in GC%, mostly of fish genomes, originated from a misapprehension of the current flood of data. Utilizing public databases, we calculated the GC% in animal genomes of three different, technically well-established fractions: DNA (entire genome), cDNA (complementary DNA), and cds (exons). Our results across chordates help set borders of GC% values that are still incorrect in literature and show: (i) fish in their immense diversity possess comparably GC-rich (or even GC-richer) genomes as higher vertebrates, and fish exons are GC-enriched among vertebrates; (ii) animal genomes generally show a GC-enrichment from the DNA, over cDNA, to the cds level (i.e., not only the higher vertebrates); (iii) fish and invertebrates show a broad(er) inter-quartile range in GC%, while avian and mammalian genomes are more constrained in their GC%. These results indicate no sharp increase in the GC% of genes during the transition to higher vertebrates, as stated and numerously repeated before. We present our results in 2D and 3D space to explore the compositional genome landscape and prepared an online platform to explore the AT/GC compositional genome evolution.
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Costantini M., Cammarano R., Bernardi G. The Evolution of Isochore Patterns in Vertebrate Genomes. BMC Genom. 2009;10:146. doi: 10.1186/1471-2164-10-146. PubMed DOI PMC
Bernardi G. The Neoselectionist Theory of Genome Evolution. Proc. Natl. Acad. Sci. USA. 2007;104:8385–8390. doi: 10.1073/pnas.0701652104. PubMed DOI PMC
Bernardi G. The Vertebrate Genome: Isochores and Evolution. Mol. Biol. Evol. 1993;10:186–204. doi: 10.1093/oxfordjournals.molbev.a039994. PubMed DOI
Li X.-Q. Comparative Analysis of the Base Compositions of the Pre-MRNA 3′ Cleaved-Off Region and the MRNA 3′ Untranslated Region Relative to the Genomic Base Composition in Animals and Plants. PLoS ONE. 2014;9:e99928. doi: 10.1371/journal.pone.0099928. PubMed DOI PMC
Li X.-Q., Du D. Variation, Evolution, and Correlation Analysis of C+G Content and Genome or Chromosome Size in Different Kingdoms and Phyla. PLoS ONE. 2014;9:e88339. doi: 10.1371/journal.pone.0088339. PubMed DOI PMC
Wu Y., Yuan H., Tan S., Chen J.-Q., Tian D., Yang H. Increased Complexity of Gene Structure and Base Composition in Vertebrates. J. Genet. Genom. 2011;38:297–305. doi: 10.1016/j.jgg.2011.06.004. PubMed DOI
Zhu L., Zhang Y., Zhang W., Yang S., Chen J.-Q., Tian D. Patterns of Exon-Intron Architecture Variation of Genes in Eukaryotic Genomes. BMC Genom. 2009;10:47. doi: 10.1186/1471-2164-10-47. PubMed DOI PMC
Majtánová Z., Symonová R., Arias-Rodriguez L., Sallan L., Ráb P. “Holostei versus Halecostomi” Problem: Insight from Cytogenetics of Ancient Nonteleost Actinopterygian Fish, Bowfin Amia Calva: Molecular cytogenetics of Amia Calva. J. Exp. Zool. Mol. Dev. Evol. 2017;328:620–628. doi: 10.1002/jez.b.22720. PubMed DOI
Symonová R., Majtánová Z., Arias-Rodriguez L., Mořkovský L., Kořínková T., Cavin L., Pokorná M.J., Doležálková M., Flajšhans M., Normandeau E., et al. Genome Compositional Organization in Gars Shows More Similarities to Mammals than to Other Ray-Finned Fish: Cytogenomics of gars. J. Exp. Zool. Mol. Dev. Evol. 2017;328:607–619. doi: 10.1002/jez.b.22719. PubMed DOI
NCBI. [(accessed on 20 December 2022)]; Available online: https://www.ncbi.nlm.nih.gov/
Cunningham F., Allen J.E., Allen J., Alvarez-Jarreta J., Amode M.R., Armean I.M., Austine-Orimoloye O., Azov A.G., Barnes I., Bennett R., et al. Ensembl 2022. Nucleic Acids Res. 2022;50:D988–D995. doi: 10.1093/nar/gkab1049. PubMed DOI PMC
Galtier N. Fine-Scale Quantification of GC-Biased Gene Conversion Intensity in Mammals. Peer Community J. 2021;1:e17. doi: 10.24072/pcjournal.22. DOI
Costantini M., Auletta F., Bernardi G. Isochore Patterns and Gene Distributions in Fish Genomes. Genomics. 2007;90:364–371. doi: 10.1016/j.ygeno.2007.05.006. PubMed DOI
Borůvková V., Howell W.M., Matoulek D., Symonová R. Quantitative Approach to Fish Cytogenetics in the Context of Vertebrate Genome Evolution. Genes. 2021;12:312. doi: 10.3390/genes12020312. PubMed DOI PMC
Symonová R., Suh A. Nucleotide Composition of Transposable Elements Likely Contributes to AT/GC Compositional Homogeneity of Teleost Fish Genomes. Mob. DNA. 2019;10:49. doi: 10.1186/s13100-019-0195-y. PubMed DOI PMC
Matoulek D., Borůvková V., Ocalewicz K., Symonová R. GC and Repeats Profiling along Chromosomes—The Future of Fish Compositional Cytogenomics. Genes. 2020;12:50. doi: 10.3390/genes12010050. PubMed DOI PMC
Graur D. Slaying (Yet Again) the Brain-Eating Zombie Called the “Isochore Theory”: A Segmentation Algorithm Used to “Confirm” the Existence of Isochores Creates “Isochores” Where None Exist. Int. J. Mol. Sci. 2022;23:6558. doi: 10.3390/ijms23126558. PubMed DOI PMC
Šmarda P., Bureš P., Horová L., Leitch I.J., Mucina L., Pacini E., Tichý L., Grulich V., Rotreklová O. Ecological and Evolutionary Significance of Genomic GC Content Diversity in Monocots. Proc. Natl. Acad. Sci. USA. 2014;111:E4096–E4102. doi: 10.1073/pnas.1321152111. PubMed DOI PMC
Trávníček P., Čertner M., Ponert J., Chumová Z., Jersáková J., Suda J. Diversity in Genome Size and GC Content Shows Adaptive Potential in Orchids and Is Closely Linked to Partial Endoreplication, Plant Life-history Traits and Climatic Conditions. New Phytol. 2019;224:1642–1656. doi: 10.1111/nph.15996. PubMed DOI
Bowers J.E., Tang H., Burke J.M., Paterson A.H. GC Content of Plant Genes Is Linked to Past Gene Duplications. PLoS ONE. 2022;17:e0261748. doi: 10.1371/journal.pone.0261748. PubMed DOI PMC
Leppek K., Das R., Barna M. Functional 5′ UTR MRNA Structures in Eukaryotic Translation Regulation and How to Find Them. Nat. Rev. Mol. Cell Biol. 2018;19:158–174. doi: 10.1038/nrm.2017.103. PubMed DOI PMC
Litterman A.J., Kageyama R., Le Tonqueze O., Zhao W., Gagnon J.D., Goodarzi H., Erle D.J., Ansel K.M. A Massively Parallel 3′ UTR Reporter Assay Reveals Relationships between Nucleotide Content, Sequence Conservation, and MRNA Destabilization. Genome Res. 2019;29:896–906. doi: 10.1101/gr.242552.118. PubMed DOI PMC
Gozashti L., Roy S.W., Thornlow B., Kramer A., Ares M., Corbett-Detig R. Transposable Elements Drive Intron Gain in Diverse Eukaryotes. Proc. Natl. Acad. Sci. USA. 2022;119:e2209766119. doi: 10.1073/pnas.2209766119. PubMed DOI PMC
Kratochwil C.F., Kautt A.F., Nater A., Härer A., Liang Y., Henning F., Meyer A. An Intronic Transposon Insertion Associates with a Trans-Species Color Polymorphism in Midas Cichlid Fishes. Nat. Commun. 2022;13:296. doi: 10.1038/s41467-021-27685-8. PubMed DOI PMC
Bourque G., Burns K.H., Gehring M., Gorbunova V., Seluanov A., Hammell M., Imbeault M., Izsvák Z., Levin H.L., Macfarlan T.S., et al. Ten Things You Should Know about Transposable Elements. Genome Biol. 2018;19:199. doi: 10.1186/s13059-018-1577-z. PubMed DOI PMC
Furuno M., Kasukawa T., Saito R., Adachi J., Suzuki H., Baldarelli R., Hayashizaki Y., Okazaki Y. CDS Annotation in Full-Length CDNA Sequence. Genome Res. 2003;13:1478–1487. doi: 10.1101/gr.1060303. PubMed DOI PMC
Smith J.J., Kuraku S., Holt C., Sauka-Spengler T., Jiang N., Campbell M.S., Yandell M.D., Manousaki T., Meyer A., Bloom O.E., et al. Sequencing of the Sea Lamprey (Petromyzon Marinus) Genome Provides Insights into Vertebrate Evolution. Nat. Genet. 2013;45:415–421. doi: 10.1038/ng.2568. PubMed DOI PMC
Smith J.J., Timoshevskaya N., Ye C., Holt C., Keinath M.C., Parker H.J., Cook M.E., Hess J.E., Narum S.R., Lamanna F., et al. The Sea Lamprey Germline Genome Provides Insights into Programmed Genome Rearrangement and Vertebrate Evolution. Nat. Genet. 2018;50:270–277. doi: 10.1038/s41588-017-0036-1. PubMed DOI PMC
Miyashita T., Coates M.I., Farrar R., Larson P., Manning P.L., Wogelius R.A., Edwards N.P., Anné J., Bergmann U., Palmer A.R., et al. Hagfish from the Cretaceous Tethys Sea and a Reconciliation of the Morphological–Molecular Conflict in Early Vertebrate Phylogeny. Proc. Natl. Acad. Sci. USA. 2019;116:2146–2151. doi: 10.1073/pnas.1814794116. PubMed DOI PMC
Randhawa S.S., Pawar R. Fish Genomes: Sequencing Trends, Taxonomy and Influence of Taxonomy on Genome Attributes. J. Appl. Ichthyol. 2021;37:553–562. doi: 10.1111/jai.14227. DOI
Lu G., Luo M. Genomes of Major Fishes in World Fisheries and Aquaculture: Status, Application and Perspective. Aquac. Fish. 2020;5:163–173. doi: 10.1016/j.aaf.2020.05.004. DOI
Amit M., Donyo M., Hollander D., Goren A., Kim E., Gelfman S., Lev-Maor G., Burstein D., Schwartz S., Postolsky B., et al. Differential GC Content between Exons and Introns Establishes Distinct Strategies of Splice-Site Recognition. Cell Rep. 2012;1:543–556. doi: 10.1016/j.celrep.2012.03.013. PubMed DOI
Boissinot S. On the Base Composition of Transposable Elements. Int. J. Mol. Sci. 2022;23:4755. doi: 10.3390/ijms23094755. PubMed DOI PMC
Marx V. Long Road to Long-Read Assembly. Nat. Methods. 2021;18:125–129. doi: 10.1038/s41592-021-01057-y. PubMed DOI
Peona V., Weissensteiner M.H., Suh A. How Complete Are “Complete” Genome Assemblies?-An Avian Perspective. Mol. Ecol. Res. 2018;18:1188–1195. doi: 10.1111/1755-0998.12933. PubMed DOI
Nurk S., Koren S., Rhie A., Rautiainen M., Bzikadze A.V., Mikheenko A., Vollger M.R., Altemose N., Uralsky L., Gershman A., et al. The Complete Sequence of a Human Genome. Science. 2022;376:44–53. doi: 10.1126/science.abj6987. PubMed DOI PMC
Rhie A., McCarthy S.A., Fedrigo O., Damas J., Formenti G., Koren S., Uliano-Silva M., Chow W., Fungtammasan A., Kim J., et al. Towards Complete and Error-Free Genome Assemblies of All Vertebrate Species. Nature. 2021;592:737–746. doi: 10.1038/s41586-021-03451-0. PubMed DOI PMC
Hon T., Mars K., Young G., Tsai Y.-C., Karalius J.W., Landolin J.M., Maurer N., Kudrna D., Hardigan M.A., Steiner C.C., et al. Highly Accurate Long-Read HiFi Sequencing Data for Five Complex Genomes. Sci. Data. 2020;7:399. doi: 10.1038/s41597-020-00743-4. PubMed DOI PMC
Francis W.R., Wörheide G. Similar Ratios of Introns to Intergenic Sequence across Animal Genomes. Genome Biol. Evol. 2017;9:1582–1598. doi: 10.1093/gbe/evx103. PubMed DOI PMC
Hertel K.J. Combinatorial Control of Exon Recognition. J. Biol. Chem. 2008;283:1211–1215. doi: 10.1074/jbc.R700035200. PubMed DOI
Georgakopoulos-Soares I., Parada G.E., Hemberg M. Secondary Structures in RNA Synthesis, Splicing and Translation. Comput. Struct. Biotechnol. J. 2022;20:2871–2884. doi: 10.1016/j.csbj.2022.05.041. PubMed DOI PMC
Jakt L.M., Dubin A., Johansen S.D. Intron Size Minimisation in Teleosts. BMC Genom. 2022;23:628. doi: 10.1186/s12864-022-08760-w. PubMed DOI PMC
Moss S.P., Joyce D.A., Humphries S., Tindall K.J., Lunt D.H. Comparative Analysis of Teleost Genome Sequences Reveals an Ancient Intron Size Expansion in the Zebrafish Lineage. Genome Biol. Evol. 2011;3:1187–1196. doi: 10.1093/gbe/evr090. PubMed DOI PMC
Cruveiller S., Jabbari K., Clay O., Bernardi G. Compositional Gene Landscapes in Vertebrates. Genome Res. 2004;14:886–892. doi: 10.1101/gr.2246704. PubMed DOI PMC
Elhaik E., Landan G., Graur D. Can GC Content at Third-Codon Positions Be Used as a Proxy for Isochore Composition? Mol. Biol. Evol. 2009;26:1829–1833. doi: 10.1093/molbev/msp100. PubMed DOI
Huttener R., Thorrez L., in’t Veld T., Granvik M., Snoeck L., Van Lommel L., Schuit F. GC Content of Vertebrate Exome Landscapes Reveal Areas of Accelerated Protein Evolution. BMC Evol. Biol. 2019;19:144. doi: 10.1186/s12862-019-1469-1. PubMed DOI PMC
Braasch I., Gehrke A.R., Smith J.J., Kawasaki K., Manousaki T., Pasquier J., Amores A., Desvignes T., Batzel P., Catchen J., et al. The Spotted Gar Genome Illuminates Vertebrate Evolution and Facilitates Human-Teleost Comparisons. Nat. Genet. 2016;48:427–437. doi: 10.1038/ng.3526. PubMed DOI PMC
Symonová R. How (Not) to Read Fish Genomics Data—The Importance of Cytogenomics Knowledge in the Current Flood of Sequenced Genomes. J. Appl. Ichthyol. 2022:1–4. doi: 10.1111/jai.14365. DOI
Carotti E., Carducci F., Canapa A., Barucca M., Greco S., Gerdol M., Biscotti M.A. Transposable Elements and Teleost Migratory Behaviour. Int. J. Mol. Sci. 2021;22:602. doi: 10.3390/ijms22020602. PubMed DOI PMC
Gaffaroglu M., Majtánová Z., Symonová R., Pelikánová Š., Unal S., Lajbner Z., Ráb P. Present and Future Salmonid Cytogenetics. Genes. 2020;11:1462. doi: 10.3390/genes11121462. PubMed DOI PMC
Tarallo A., Angelini C., Sanges R., Yagi M., Agnisola C., D’Onofrio G. On the Genome Base Composition of Teleosts: The Effect of Environment and Lifestyle. BMC Genom. 2016;17:173. doi: 10.1186/s12864-016-2537-1. PubMed DOI PMC
Abandoning the Isochore Theory Can Help Explain Genome Compositional Organization in Fish