Quantitative Approach to Fish Cytogenetics in the Context of Vertebrate Genome Evolution

. 2021 Feb 22 ; 12 (2) : . [epub] 20210222

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33671814

Our novel Python-based tool EVANGELIST allows the visualization of GC and repeats percentages along chromosomes in sequenced genomes and has enabled us to perform quantitative large-scale analyses on the chromosome level in fish and other vertebrates. This is a different approach from the prevailing analyses, i.e., analyses of GC% in the coding sequences that make up not more than 2% in human. We identified GC content (GC%) elevations in microchromosomes in ancient fish lineages similar to avian microchromosomes and a large variability in the relationship between the chromosome size and their GC% across fish lineages. This raises the question as to what extent does the chromosome size drive GC% as posited by the currently accepted explanation based on the recombination rate. We ascribe the differences found across fishes to varying GC% of repetitive sequences. Generally, our results suggest that the GC% of repeats and proportion of repeats are independent of the chromosome size. This leaves an open space for another mechanism driving the GC evolution in vertebrates.

Zobrazit více v PubMed

Gregory T.R. Animal Genome Size Database. [(accessed on 31 January 2021)]; Available online: http://www.genomesize.com.

Levan A., Fredga K., Sandberg A.A. Nomenclature for Centromeric Position on Chromosomes. Hereditas. 1964;52:201–220. doi: 10.1111/j.1601-5223.1964.tb01953.x. DOI

Mark H.F., Mark R., Pan T., Mark Y. Centromere Index Derivation by a Novel and Convenient Approach. Ann. Clin. Lab. Sci. 1993;23:267–274. PubMed

Comings D.E. Mechanisms of Chromosome Banding and Implications for Chromosome Structure. Annu. Rev. Genet. 1978;12:25–46. doi: 10.1146/annurev.ge.12.120178.000325. PubMed DOI

Luo C. Multiple Chromosomal Banding in Grass Carp, Ctenopharyngodon Idellus. Heredity. 1998;81:481–485. doi: 10.1046/j.1365-2540.1998.00323.x. DOI

Medrano L., Bernardi G., Couturier J., Dutrillaux B., Bernardi G. Chromosome Banding and Genome Compartmentalization in Fishes. Chromosoma. 1988;96:178–183. doi: 10.1007/BF00331050. DOI

Mayr B., Kalat M., Ráb P., Lambrou M. Band Karyotypes and Specific Types of Heterochromatins in Several Species of European Percid Fishes (Percidea, Pisces) Genetica. 1987;75:199–205. doi: 10.1007/BF00123574. DOI

Mank J.E., Avise J.C. Phylogenetic Conservation of Chromosome Numbers in Actinopterygiian Fishes. Genetica. 2006;127:321–327. doi: 10.1007/s10709-005-5248-0. PubMed DOI

Gregory T.R., Witt J.D.S. Population Size and Genome Size in Fishes: A Closer Look. Genome. 2008;51:309–313. doi: 10.1139/G08-003. PubMed DOI

Hardie D.C., Hebert P.D.N. The Nucleotypic Effects of Cellular DNA Content in Cartilaginous and Ray-Finned Fishes. Genome. 2003;46:683–706. doi: 10.1139/g03-040. PubMed DOI

Hardie D.C., Hebert P.D. Genome-Size Evolution in Fishes. Can. J. Fish. Aquat. Sci. 2004;61:1636–1646. doi: 10.1139/f04-106. DOI

Melodelima C., Gautier C. The GC-Heterogeneity of Teleost Fishes. BMC Genom. 2008;9:632. doi: 10.1186/1471-2164-9-632. PubMed DOI PMC

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

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

Eyre-Walker A. Recombination and Mammalian Genome Evolution. Proc. R. Soc. Lond. B Biol. Sci. 1993;252:237–243. doi: 10.1098/rspb.1993.0071. PubMed DOI

Fullerton S.M., Bernardo Carvalho A., Clark A.G. Local Rates of Recombination Are Positively Correlated with GC Content in the Human Genome. Mol. Biol. Evol. 2001;18:1139–1142. doi: 10.1093/oxfordjournals.molbev.a003886. PubMed DOI

Montoya-Burgos J.I., Boursot P., Galtier N. Recombination Explains Isochores in Mammalian Genomes. Trends Genet. 2003;19:128–130. doi: 10.1016/S0168-9525(03)00021-0. PubMed DOI

Mugal C.F., Weber C.C., Ellegren H. GC-Biased Gene Conversion Links the Recombination Landscape and Demography to Genomic Base Composition: GC-Biased Gene Conversion Drives Genomic Base Composition across a Wide Range of Species. BioEssays. 2015;37:1317–1326. doi: 10.1002/bies.201500058. PubMed DOI

Stapley J., Feulner P.G.D., Johnston S.E., Santure A.W., Smadja C.M. Variation in Recombination Frequency and Distribution across Eukaryotes: Patterns and Processes. Philos. Trans. R. Soc. B Biol. Sci. 2017;372:20160455. doi: 10.1098/rstb.2016.0455. PubMed DOI PMC

Romiguier J., Ranwez V., Douzery E.J.P., Galtier N. Contrasting GC-Content Dynamics across 33 Mammalian Genomes: Relationship with Life-History Traits and Chromosome Sizes. Genome Res. 2010;20:1001–1009. doi: 10.1101/gr.104372.109. PubMed DOI PMC

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 doi: 10.1186/s12862-019-1469-1. PubMed DOI PMC

Shen W., Wang D., Ye B., Shi M., Ma L., Zhang Y., Zhao Z. GC3-Biased Gene Domains in Mammalian Genomes. Bioinformatics. 2015;31:3081–3084. doi: 10.1093/bioinformatics/btv329. PubMed DOI PMC

Weber C.C., Boussau B., Romiguier J., Jarvis E.D., Ellegren H. Evidence for GC-Biased Gene Conversion as a Driver of between-Lineage Differences in Avian Base Composition. Genome Biol. 2014;15 doi: 10.1186/s13059-014-0549-1. PubMed DOI PMC

Bolívar P., Mugal C.F., Nater A., Ellegren H. Recombination Rate Variation Modulates Gene Sequence Evolution Mainly via GC-Biased Gene Conversion, Not Hill–Robertson Interference, in an Avian System. Mol. Biol. Evol. 2016;33:216–227. doi: 10.1093/molbev/msv214. PubMed DOI PMC

Matsubara K., Kuraku S., Tarui H., Nishimura O., Nishida C., Agata K., Kumazawa Y., Matsuda Y. Intra-Genomic GC Heterogeneity in Sauropsids: Evolutionary Insights from CDNA Mapping and GC3 Profiling in Snake. BMC Genom. 2012;13:604. doi: 10.1186/1471-2164-13-604. PubMed DOI PMC

Figuet E., Ballenghien M., Romiguier J., Galtier N. Biased Gene Conversion and GC-Content Evolution in the Coding Sequences of Reptiles and Vertebrates. Genome Biol. Evol. 2015;7:240–250. doi: 10.1093/gbe/evu277. PubMed DOI PMC

Wang D. GCevobase: An Evolution-Based Database for GC Content in Eukaryotic Genomes. Bioinformatics. 2018;34:2129–2131. doi: 10.1093/bioinformatics/bty068. PubMed DOI

Frenkel S., Kirzhner V., Korol A. Organizational Heterogeneity of Vertebrate Genomes. PLoS ONE. 2012;7:e32076. doi: 10.1371/journal.pone.0032076. 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

Symonová R., Suh A. Nucleotide Composition of Transposable Elements Likely Contributes to AT/GC Compositional Homogeneity of Teleost Fish Genomes. Mob. DNA. 2019;10 doi: 10.1186/s13100-019-0195-y. PubMed DOI PMC

Carducci F., Barucca M., Canapa A., Carotti E., Biscotti M.A. Mobile Elements in Ray-Finned Fish Genomes. Life. 2020;10:221. doi: 10.3390/life10100221. PubMed DOI PMC

Bernardi G. The Vertebrate Genome: Isochores and Evolution. Mol. Biol. Evol. 1993 doi: 10.1093/oxfordjournals.molbev.a039994. 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. Part B Mol. Dev. Evol. 2017;328:607–619. doi: 10.1002/jez.b.22719. PubMed DOI

Matoulek D., Borůvková V., Ocalewicz K., Symonová R. GC and Repeats Profiling along Chromosomes—The Future of Fish Compositional Cytogenomics. Genes. 2021;12:50. doi: 10.3390/genes12010050. PubMed DOI PMC

Bernardi G. Structural and Evolutionary Genomics Natural Selection in Genome Evolution. Elsevier; Amsterdam, The Netherlands: 2005.

Peona V., Weissensteiner M.H., Suh A. How Complete Are “Complete” Genome Assemblies?—An Avian Perspective. Mol. Ecol. Resour. 2018;18:1188–1195. doi: 10.1111/1755-0998.12933. PubMed DOI

Jebb D., Huang Z., Pippel M., Hughes G.M., Lavrichenko K., Devanna P., Winkler S., Jermiin L.S., Skirmuntt E.C., Katzourakis A., et al. Six Reference-Quality Genomes Reveal Evolution of Bat Adaptations. Nature. 2020;583:578–584. doi: 10.1038/s41586-020-2486-3. PubMed DOI PMC

R Core Team . R: A Language and Environment for Statistical Computing. R Core Team; Vienna, Austria: 2013. Version 2.6.2.

Wickham H. Ggplot2: Elegant Graphics for Data Analysis. 2nd ed. Springer International Publishing; Cham, Switzerland: 2016. Use R!

Nelson J.S., Grande T., Wilson M.V.H. Fishes of the World. 5th ed. John Wiley & Sons; Hoboken, NJ, USA: 2016.

Howe K., Clark M.D., Torroja C.F., Torrance J., Berthelot C., Muffato M., Collins J.E., Humphray S., McLaren K., Matthews L., et al. The Zebrafish Reference Genome Sequence and Its Relationship to the Human Genome. Nature. 2013;496:498–503. doi: 10.1038/nature12111. PubMed DOI PMC

Hidalgo O., Pellicer J., Christenhusz M., Schneider H., Leitch A.R., Leitch I.J. Is There an Upper Limit to Genome Size? Trends Plant Sci. 2017;22:567–573. doi: 10.1016/j.tplants.2017.04.005. PubMed DOI

NCBI Genome Browser. [(accessed on 31 January 2021)]; Available online: https://www.ncbi.nlm.nih.gov/genome/browse.

Meyer A., Schartl M. Gene and Genome Duplications in Vertebrates: The One-to-Four (-to-Eight in Fish) Rule and the Evolution of Novel Gene Functions. Curr. Opin. Cell Biol. 1999;11:699–704. doi: 10.1016/S0955-0674(99)00039-3. PubMed DOI

Hannan A.J. Tandem Repeats and Repeatomes: Delving Deeper into the ‘Dark Matter’ of Genomes. EBioMedicine. 2018;31:3–4. doi: 10.1016/j.ebiom.2018.04.004. PubMed DOI PMC

Arkhipova I.R., Yushenova I.A. Giant Transposons in Eukaryotes: Is Bigger Better? Genome Biol. Evol. 2019;11:906–918. doi: 10.1093/gbe/evz041. PubMed DOI PMC

Fontana F., Bruch R.M., Binkowski F.P., Lanfredi M., Chicca M., Beltrami N., Congiu L. Karyotype Characterization of the Lake Sturgeon, Acipenser fulvescens (Rafinesque 1817) by Chromosome Banding and Fluorescent in Situ Hybridization. Genome. 2004;47:742–746. doi: 10.1139/g04-028. PubMed DOI

Symonová R., Havelka M., Amemiya C.T., Howell W.M., Kořínková T., Flajšhans M., Gela D., Ráb P. Molecular Cytogenetic Differentiation of Paralogs of Hox Paralogs in Duplicated and Re-Diploidized Genome of the North American Paddlefish (Polyodon spathula) BMC Genet. 2017;18 doi: 10.1186/s12863-017-0484-8. 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. Part B Mol. Dev. Evol. 2017;328:620–628. doi: 10.1002/jez.b.22720. PubMed DOI

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

Lien S., Koop B.F., Sandve S.R., Miller J.R., Kent M.P., Nome T., Hvidsten T.R., Leong J.S., Minkley D.R., Zimin A., et al. The Atlantic Salmon Genome Provides Insights into Rediploidization. Nature. 2016;533:200–205. doi: 10.1038/nature17164. PubMed DOI PMC

De-Kayne R., Zoller S., Feulner P.G.D. A de Novo Chromosome-level Genome Assembly of Coregonus sp. “Balchen”: One Representative of the Swiss Alpine Whitefish Radiation. Mol. Ecol. Resour. 2020;20:1093–1109. doi: 10.1111/1755-0998.13187. PubMed DOI PMC

Pearse D.E., Barson N.J., Nome T., Gao G., Campbell M.A., Abadía-Cardoso A., Anderson E.C., Rundio D.E., Williams T.H., Naish K.A., et al. Sex-Dependent Dominance Maintains Migration Supergene in Rainbow Trout. Nat. Ecol. Evol. 2019;3:1731–1742. doi: 10.1038/s41559-019-1044-6. PubMed DOI

Christensen K.A., Leong J.S., Sakhrani D., Biagi C.A., Minkley D.R., Withler R.E., Rondeau E.B., Koop B.F., Devlin R.H. Chinook Salmon (Oncorhynchus tshawytscha) Genome and Transcriptome. PLoS ONE. 2018;13:e0195461. doi: 10.1371/journal.pone.0195461. PubMed DOI PMC

Canapa A., Barucca M., Biscotti M.A., Forconi M., Olmo E. Transposons, Genome Size, and Evolutionary Insights in Animals. Cytogenet. Genome Res. 2015;147:217–239. doi: 10.1159/000444429. PubMed DOI

Nowoshilow S., Schloissnig S., Fei J.-F., Dahl A., Pang A.W.C., Pippel M., Winkler S., Hastie A.R., Young G., Roscito J.G., et al. The Axolotl Genome and the Evolution of Key Tissue Formation Regulators. Nature. 2018;554:50–55. doi: 10.1038/nature25458. PubMed DOI

Rodriguez F., Arkhipova I.R. Transposable Elements and Polyploid Evolution in Animals. Curr. Opin. Genet. Dev. 2018;49:115–123. doi: 10.1016/j.gde.2018.04.003. 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 doi: 10.1186/s12864-016-2537-1. PubMed DOI PMC

Yi S., Streelman J.T. Genome Size Is Negatively Correlated with Effective Population Size in Ray-Finned Fish. Trends Genet. 2005;21:643–646. doi: 10.1016/j.tig.2005.09.003. PubMed DOI

Rolland J., Schluter D., Romiguier J. Vulnerability to Fishing and Life History Traits Correlate with the Load of Deleterious Mutations in Teleosts. Mol. Biol. Evol. 2020;37:2192–2196. doi: 10.1093/molbev/msaa067. PubMed DOI PMC

Tollis M., Boissinot S. The Evolutionary Dynamics of Transposable Elements in Eukaryote Genomes. In: Garrido-Ramos M.A., editor. Genome Dynamics. Volume 7. S. KARGER AG; Basel, Switzerland: 2012. pp. 68–91. PubMed

Bourgeois Y., Boissinot S. On the Population Dynamics of Junk: A Review on the Population Genomics of Transposable Elements. Genes. 2019;10:419. doi: 10.3390/genes10060419. PubMed DOI PMC

Kent T.V., Uzunović J., Wright S.I. Coevolution between Transposable Elements and Recombination. Philos. Trans. R. Soc. B Biol. Sci. 2017;372:20160458. doi: 10.1098/rstb.2016.0458. PubMed DOI PMC

Ruggiero R.P., Boissinot S. Variation in Base Composition Underlies Functional and Evolutionary Divergence in Non-LTR Retrotransposons. Mob. DNA. 2020;11 doi: 10.1186/s13100-020-00209-9. PubMed DOI PMC

Paudel R., Fedorova L., Fedorov A. Adapting Biased Gene Conversion Theory to Account for Intensive GC-Content Deterioration in the Human Genome by Novel Mutations. PLoS ONE. 2020;15:e0232167. doi: 10.1371/journal.pone.0232167. PubMed DOI PMC

Nam K., Ellegren H. Recombination Drives Vertebrate Genome Contraction. PLoS Genet. 2012;8:e1002680. doi: 10.1371/journal.pgen.1002680. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...