Contribution of the intron retained in the Nxf1 gene transcript to the phylogeny of the order Chiroptera

Abstract

This work is devoted to the possibilities of using a specific intron-containing block of the Nxf1 gene in phylogenetic studies.

Our attention was drawn to the conservative intron of the Nxf1 (nuclear export factor) gene. This intron is a part of an evolutionarily conserved block formed with flanking 110 bp and 37 bp exons, similar in representatives of various taxonomic groups. This evolutionary conservative block in our previous works was designated “cassette intron”. The Nxf1 genes are found in all representatives of Opisthokonta, and may be a convenient object for phylogenetic studies.

The Nxf1 gene sequences of seventeen representatives of the order Chiroptera obtained from publicly available databases (ensembl, ncbi). Alignment algorithm: MUSCLE. Programs: MEGA-X version 10.1.7, IQTree, Mesquite, MrBayes, and FigTree.v1.4.4. Estimation methods: Maximum Likelihood and Bayes Inference.

The use of Nxf1 gene sequences that include only exons or only introns leads to unequal loss of accuracy in establishing evolutionary relationships in comparison with the model based on the complete gene sequence. Sequences involving all exons plus a cassette intron give the same result as the complete Nxf1 gene sequence.

The obtained results indicate the importance of the cassette intron in the evolution of the Nxf1 gene of Chiroptera.

Keywords

nuclear export factor (nxf) / intron-containing transcripts / phylogenetics / evolutionary conservative sequences / bats / Chiroptera

References

[1] Herold A, Suyama M, Rodrigues JP, et al. TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol Cell Biol. 2000;20(23):8996–9008. DOI: 10.1128/MCB.20.23.8996-9008.2000

[2] Herold A., Suyama M., Rodrigues J.P., et al. TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture // Mol Cell Biol. 2000. Vol. 20, No. 23. P. 8996–9008. DOI: 10.1128/MCB.20.23.8996-9008.2000

[3] Herold A, Teixeira L, Izaurralde E. Genome-wide analysis of nuclear mRNA export pathways in Drosophila. EMBO J. 2003;22(10):2472–2483. DOI: 10.1093/emboj/cdg233

[4] Herold A., Teixeira L., Izaurralde E. Genome-wide analysis of nuclear mRNA export pathways in Drosophila // EMBO J. 2003. Vol. 22, No. 10. P. 2472–2483. DOI: 10.1093/emboj/cdg233

[5] Delaleau M, Borden KLB. Multiple Export Mechanisms for mRNAs. Cells. 2015;4(3):452–473. DOI: 10.3390/cells4030452

[6] Delaleau M., Borden K.L.B. Multiple Export Mechanisms for mRNAs // Cells. 2015. Vol. 4, No. 3. P. 452–473. DOI: 10.3390/cells4030452

[7] Herold A, Klymenko T, Izaurralde E. NXF1/p15 heterodimers are essential for mRNA nuclear export in Drosophila. RNA. 2001;7(12):1768–1780.

[8] Herold A., Klymenko T., Izaurralde E. NXF1/p15 heterodimers are essential for mRNA nuclear export in Drosophila // RNA. 2001. Vol. 7, No. 12. P. 1768–1780.

[9] Ivankova N, Tretyakova I, Lyozin GT, et al. Alternative transcripts expressed by small bristles, the Drosophila melanogaster nxf1 gene. Gene. 2010;458(1–2):11–19. DOI: 10.1016/j.gene.2010.02.013

[10] Ivankova N., Tretyakova I., Lyozin G.T., et al. Alternative transcripts expressed by small bristles, the Drosophila melanogaster nxf1 gene // Gene. 2010. Vol. 458, No. 1–2. P. 11–19. DOI: 10.1016/j.gene.2010.02.013

[11] Sasaki M, Takeda E, Takano K, et al. Molecular cloning and functional characterization of mouse Nxf family gene products. Genomics. 2005;85(5):641–653. DOI: 10.1016/j.ygeno.2005.01.003

[12] Sasaki M., Takeda E., Takano K., et al. Molecular cloning and functional characterization of mouse Nxf family gene products // Genomics. 2005. Vol. 85, No. 5. P. 641–653. DOI: 10.1016/j.ygeno.2005.01.003

[13] Mamon L, Ginanova V, Kliver S, et al. Organ-specific transcripts as a source of gene multifunctionality: lessons learned from the Drosophila melanogaster sbr (Dm nxf1) gene. Biol Commun. 2019;64(2). DOI: 10.21638/spbu03.2019.206

[14] Mamon L., Ginanova V., Kliver S., et al. Organ-specific transcripts as a source of gene multifunctionality: lessons learned from the Drosophila melanogaster sbr (Dm nxf1) gene // Biol Commun. 2019. Vol. 64, No. 2. P. DOI: 10.21638/spbu03.2019.206

[15] Kim E, Magen A, Ast G. Different levels of alternative splicing among eukaryotes. Nucleic Acids Res. 2007;35(1):125–131. DOI: 10.1093/nar/gkl924

[16] Kim E., Magen A., Ast G. Different levels of alternative splicing among eukaryotes // Nucleic Acids Res. 2007. Vol. 35, No. 1. P. 125–131. DOI: 10.1093/nar/gkl924

[17] Mamon LA, Kliver SF, Prosovskaya AO, et al. The intron-containing transcript: an evolutionarily conserved characteristic of genes orthologous to nxf1 (Nuclear eXport Factor 1). Ecological genetics. 2013;11(3):3–13. (In Russ.) DOI: 10.17816/ecogen1133-13

[18] Мамон Л.А., Кливер С.Ф., Просовская А.О., и др. Интрон-содержащий транскрипт — эволюционно-консервативная особенность генов-ортологов nxf1 (nuclear export factor) // Экологическая генетика. 2013. Т. 11, № 3. С. 3–13. DOI: 10.17816/ecogen1133-13

[19] Sugnet CW, Kent WJ, Ares M Jr, Haussler D. Transcriptome and genome conservation of alternative splicing events in humans and mice. Pac Symp Biocomput. 2004:66–77. DOI: 10.1142/9789812704856_0007

[20] Sugnet C.W., Kent W.J., Ares M. Jr, Haussler D. Transcriptome and genome conservation of alternative splicing events in humans and mice // Pac Symp Biocomput. 2004. P. 66–77. DOI: 10.1142/9789812704856_0007

[21] Schmitz U, Pinello N, Jia F, et al. Intron retention enhances gene regulatory complexity in vertebrates. Genome Biol. 2017;18:216. DOI: 10.1186/s13059-017-1339-3

[22] Schmitz U., Pinello N., Jia F., et al. Intron retention enhances gene regulatory complexity in vertebrates // Genome Biol. 2017. Vol. 18. ID216. DOI: 10.1186/s13059-017-1339-3

[23] Pimentel H, Parra M, Gee SL, et al. A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis. Nucleic Acids Res. 2016;44(2):838–851. DOI: 10.1093/nar/gkv1168

[24] Pimentel H., Parra M., Gee S.L., et al. A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis // Nucleic Acids Res. 2016. Vol. 44, No. 2. P. 838–851. DOI: 10.1093/nar/gkv1168

[25] Li Y, Bor Y-c, Misawa Y, et al. An intron with a constitutive transport element is retained in a Tap messenger RNA. Nature. 2006;443:234–237. DOI: 10.1038/nature05107

[26] Li Y., Bor Y.-c., Misawa Y., et al. An intron with a constitutive transport element is retained in a Tap messenger RNA // Nature. 2006. Vol. 443. P. 234–237. DOI: 10.1038/nature05107

[27] Li Y, Bor Y-c, Fitzgerald MP, et al. An NXF1 mRNA with a retained intron is expressed in hippocampal and neocortical neurons and is translated into a protein that functions as an Nxf1 cofactor. Mol Biol Cell. 2016;27(24):3791–3946. DOI: 10.1091/mbc.E16-07-0515

[28] Li Y., Bor Y.-c., Fitzgerald M.P., et al. An NXF1 mRNA with a retained intron is expressed in hippocampal and neocortical neurons and is translated into a protein that functions as an Nxf1 cofactor // Mol Biol Cell. 2016. Vol. 27, No. 24. P. 3791–3946. DOI: 10.1091/mbc.E16-07-0515

[29] Galante PAF, Sakabe NJ, Kirschbaum-Slager N, de Souza SJ. Detection and evaluation of intron retention events in the human transcriptome. RNA. 2004;10(5):757–765. DOI: 10.1261/rna.5123504

[30] Galante P.A.F., Sakabe N.J., Kirschbaum-Slager N., de Souza S.J. Detection and evaluation of intron retention events in the human transcriptome // RNA. 2004. Vol. 10, No. 5. P. 757–765. DOI: 10.1261/rna.5123504

[31] Michael IP, Kurlender L, Memari N, et al. Intron retention: a common splicing event within the human kallikrein gene family. Clin Chem. 2005;51(3):506–515. DOI: 10.1373/clinchem.2004.042341

[32] Michael I.P., Kurlender L., Memari N., et al. Intron retention: a common splicing event within the human kallikrein gene family // Clin Chem. 2005. Vol. 51, No. 3. P. 506–515. DOI: 10.1373/clinchem.2004.042341

[33] Chen M-Y, Liang D, Zhang P. Phylogenomic Resolution of the Phylogeny of Laurasiatherian Mammals: Exploring Phylogenetic Signals within Coding and Noncoding Sequences. Genome Biol EVol. 2017;9(8):1998–2012. DOI: 10.1093/gbe/evx147

[34] Chen M.-Y., Liang D., Zhang P. Phylogenomic Resolution of the Phylogeny of Laurasiatherian Mammals: Exploring Phylogenetic Signals within Coding and Noncoding Sequences // Genome Biol EVol. 2017. Vol. 9, No. 8. P. 1998–2012. DOI: 10.1093/gbe/evx147

[35] Jarvis ED, Mirarab S, Aberer AJ, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346(6215):1320–1331. DOI: 10.1126/science.1253451

[36] Jarvis E.D., Mirarab S., Aberer A.J., et al. Whole-genome analyses resolve early branches in the tree of life of modern birds // Science. 2014. Vol. 346, No. 6215. P. 1320–1331. DOI: 10.1126/science.1253451

[37] Yu L, Luan P-T, Jin W, et al. Phylogenetic utility of nuclear introns in interfamilial relationships of Caniformia (order Carnivora). Syst Biol. 2011;60(2):175–187. DOI: 10.1093/sysbio/syq090

[38] Yu L., Luan P.-T., Jin W., et al. Phylogenetic utility of nuclear introns in interfamilial relationships of Caniformia (order Carnivora) // Syst Biol. 2011. Vol. 60, No. 2. P. 175–187. DOI: 10.1093/sysbio/syq090

[39] Creer S. Choosing and using introns in molecular phylogenetics. Evol Bioinform. 2007;3:99–108. DOI: 10.1177/117693430700300011

[40] Creer S. Choosing and using introns in molecular phylogenetics // Evol Bioinform. 2007. Vol. 3. P. 99–108. DOI: 10.1177/117693430700300011

[41] Foley NM, Thong VD, Soisook P, et al. How and why overcome the impediments to resolution: lessons from rhinolophid and hipposiderid bats. Mol Biol EVol. 2015;32(2):313–333. DOI: 10.1093/molbev/msu329

[42] Foley N.M., Thong V.D., Soisook P., et al. How and why overcome the impediments to resolution: lessons from rhinolophid and hipposiderid bats // Mol Biol EVol. 2015. Vol. 32, No. 2. P. 313–333. DOI: 10.1093/molbev/msu329

[43] Aibara S, Katahira J, Valkov E, Stewart M. The principal mRNA nuclear export factor NXF1: NXT1 forms a symmetric binding platform that facilitates export of retroviral CTE-RNA. Nucleic Acids Res. 2015;43(3):1883–1893. DOI: 10.1093/nar/gkv032

[44] Aibara S., Katahira J., Valkov E., Stewart M. The principal mRNA nuclear export factor NXF1: NXT1 forms a symmetric binding platform that facilitates export of retroviral CTE-RNA // Nucleic Acids Res. 2015. Vol. 43, No. 3. P. 1883–1893. DOI: 10.1093/nar/gkv032

[45] Wendt L, Brandt J, Bodmer BS, et al. The Ebola Virus Nucleoprotein Recruits the Nuclear RNA Export Factor NXF1 into Inclusion Bodies to Facilitate Viral Protein Expression. Cells. 2020;9(1):187. DOI: 10.3390/cells9010187

[46] Wendt L., Brandt J., Bodmer B.S., et al. The Ebola Virus Nucleoprotein Recruits the Nuclear RNA Export Factor NXF1 into Inclusion Bodies to Facilitate Viral Protein Expression // Cells. 2020. Vol. 9, No. 1. ID 187. DOI: 10.3390/cells9010187

[47] Kumar S, Stecher G, Li M, et al. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol EVol. 2018;35(6):1547–1549. DOI: 10.1093/molbev/msy096

[48] Kumar S., Stecher G., Li M., et al. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms // Mol Biol EVol. 2018. Vol. 35, No. 6. P. 1547–1549. DOI: 10.1093/molbev/msy096

[49] Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–1797. DOI: 10.1093/nar/gkh340

[50] Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput // Nucleic Acids Res. 2004. Vol. 32, No. 5. P. 1792–1797. DOI: 10.1093/nar/gkh340

[51] Michener CD, Sokal RR. A quantitative approach to a problem in classification. Evolution. 1957;11(2):130–162. DOI: 10.1111/j.1558-5646.1957.tb02884.x

[52] Michener C.D., Sokal R.R. A quantitative approach to a problem in classification // Evolution. 1957. Vol. 11, No. 2. P. 130–162. DOI: 10.1111/j.1558-5646.1957.tb02884.x

[53] mesquiteproject.org [Internet]. Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis. Version 3.70. 2021. Available from: http://www.mesquiteproject.org

[54] mesquiteproject.org [Internet]. Maddison W.P., Maddison D.R. Mesquite: a modular system for evolutionary analysis. Version 3.70. 2021. Доступ по ссылке: http://www.mesquiteproject.org

[55] Huelsenbeck JP, Ronquist F. MrBayes 3: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17(8):754–755. DOI: 10.1093/bioinformatics/17.8.754

[56] Huelsenbeck JP, Ronquist F. MrBayes 3: Bayesian inference of phylogenetic trees // Bioinformatics. 2001. Vol. 17, No. 8. P. 754–755. DOI: 10.1093/bioinformatics/17.8.754

[57] FigTree [Internet]. Molecular evolution, phylogenetics and epidemiology. 2022. Available from: http://tree.bio.ed.ac.uk/software/figtree/. Accessed June 20, 2022.

[58] FigTree [Internet]. Molecular evolution, phylogenetics and epidemiology. 2022. Доступ по ссылке: http://tree.bio.ed.ac.uk/software/figtree/

[59] Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44(W1): W232–W235. DOI: 10.1093/nar/gkw256

[60] Trifinopoulos J., Nguyen L.-T., von Haeseler A., Minh B.Q. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis // Nucleic Acids Res. 2016. Vol. 44, No. W1. P. W232–W235. DOI: 10.1093/nar/gkw256

[61] Kalyaanamoorthy S, Minh BQ, Wong TKF, et al. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–589. DOI: 10.1038/nmeth.4285

[62] Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., et al. ModelFinder: fast model selection for accurate phylogenetic estimates // Nat Methods. 2017. Vol. 14. P. 587–589. DOI: 10.1038/nmeth.4285

[63] Akaike H. A new look at the statistical model identification. IEEE Transactions on Automatic Control. 1974;19(6):716–723. DOI: 10.1109/TAC.1974.1100705

[64] Akaike H. A new look at the statistical model identification // IEEE Transactions on Automatic Control. 1974. Vol. 19, No. 6. P. 716–723. DOI: 10.1109/TAC.1974.1100705

[65] Schwarz G. Estimating the dimension of a model. Ann Stat. 1978;6(2):461–464. DOI: 10.1214/aos/1176344136

[66] Schwarz G. Estimating the dimension of a model // Ann Stat. 1978. Vol. 6, No. 2. P. 461–464. DOI: 10.1214/aos/1176344136

[67] Kimura M. Estimation of evolutionary distances between homologous nucleotide sequences. PNAS. 1981;78(1):454–458. DOI: 10.1073/pnas.78.1.454

[68] Kimura M. Estimation of evolutionary distances between homologous nucleotide sequences // PNAS. 1981. Vol. 78, No. 1. P. 454–458. DOI: 10.1073/pnas.78.1.454

[69] Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol EVol. 1980;16:111–120. DOI: 10.1007/BF01731581

[70] Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences // J Mol EVol. 1980. Vol. 16. P. 111–120. DOI: 10.1007/BF01731581

[71] Guindon S, Dufayard J-F, Lefort V, et al. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Syst Biol. 2010;59(3):307–321. DOI: 10.1093/sysbio/syq010

[72] Guindon S., Dufayard J.-F., Lefort V., et al. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 // Syst Biol. 2010. Vol. 59, No. 3. P. 307–321. DOI: 10.1093/sysbio/syq010

[73] Minh BQ, Nguyen MAT, von Haeseler A. Ultrafast Approximation for Phylogenetic Bootstrap. Mol Biol EVol. 2013;30(5):1188–1195. DOI: 10.1093/molbev/mst024

[74] Minh B.Q., Nguyen M.A.T., von Haeseler A. Ultrafast Approximation for Phylogenetic Bootstrap // Mol Biol EVol. 2013. Vol. 30, No. 5. P. 1188–1195. DOI: 10.1093/molbev/mst024

[75] Hoang DT, Chernomor O, von Haeseler A, et al. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol Biol EVol. 2018;35(2):518–522. DOI: 10.1093/molbev/msx281

[76] Hoang D.T., Chernomor O., von Haeseler A., et al. UFBoot2: Improving the Ultrafast Bootstrap Approximation // Mol Biol EVol. 2018. Vol. 35, No. 2. P. 518–522. DOI: 10.1093/molbev/msx281

[77] Rodríguez F, Oliver JL, Marín A, Medina JR. The general stochastic model of nucleotide substitution. J Theor Biol. 1990;142(4): 485–501. DOI: 10.1016/s0022–5193(05)80104-3

[78] Rodríguez F., Oliver J.L., Marín A., Medina J.R. The general stochastic model of nucleotide substitution // J Theor Biol. 1990. Vol. 142, No. 4. P. 485–501. DOI: 10.1016/s0022-5193(05)80104-3

[79] Lanave C, Preparata G, Sacone C, Serio G. A new method for calculating evolutionary substitution rates. J Mol EVol. 1984;20:86–93. DOI: 10.1007/BF02101990

[80] Lanave C., Preparata G., Sacone C., Serio G. A new method for calculating evolutionary substitution rates // J Mol EVol. 1984. Vol. 20. P. 86–93. DOI: 10.1007/BF02101990

[81] Gu X, Fu YX, Li WH. Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites. Mol Biol EVol. 1995;12(4):546–557. DOI: 10.1093/oxfordjournals.molbev.a040235

[82] Gu X., Fu Y.X., Li W.H. Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites // Mol Biol EVol. 1995. Vol. 12, No. 4. P. 546–557. DOI: 10.1093/oxfordjournals.molbev.a040235

[83] Lemoine F, Domelevo Entfellner J-B, Wilkinson E, et al. Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature. 2018;556:452–456. DOI: 10.1038/s41586-018-0043-0

[84] Lemoine F., Domelevo Entfellner J.-B., Wilkinson E., et al. Renewing Felsenstein’s phylogenetic bootstrap in the era of big data // Nature. 2018. Vol. 556. P. 452–456. DOI: 10.1038/s41586-018-0043-0

[85] Tsagkogeorga G, Parker J, Stupka E, et al. Phylogenomic analyses elucidate the evolutionary relationships of bats. Curr Biol. 2013;23(22):2262–2267. DOI: 10.1016/j.cub.2013.09.014

[86] Tsagkogeorga G., Parker J., Stupka E., et al. Phylogenomic analyses elucidate the evolutionary relationships of bats // Curr Biol. 2013. Vol. 23, No. 22. P. 2262–2267. DOI: 10.1016/j.cub.2013.09.014

[87] Lei M, Dong D. Phylogenomic analyses of bat subordinal relationships based on transcriptome data. Sci Rep. 2016;6:27726. DOI: 10.1038/srep27726

[88] Lei M., Dong D. Phylogenomic analyses of bat subordinal relationships based on transcriptome data // Sci Rep. 2016. Vol. 6. ID27726. DOI: 10.1038/srep27726

[89] Farkašová H, Hron T, Pačes J, et al. Discovery of an endogenous Deltaretrovirus in the genome of long-fingered bats (Chiroptera: Miniopteridae). PNAS. 2017;114(12):3145–3150. DOI: 10.1073/pnas.1621224114

[90] Farkašová H., Hron T., Pačes J., et al. Discovery of an endogenous Deltaretrovirus in the genome of long-fingered bats (Chiroptera: Miniopteridae) // PNAS. 2017. Vol. 114, No. 12. P. 3145–3150. DOI: 10.1073/pnas.1621224114

[91] Miller-Butterworth CM, Murphy WJ, O’Brien SJ, et al. A Family Matter: Conclusive Resolution of the Taxonomic Position of the Long-Fingered Bats, Miniopterus. Mol Biol EVol. 2007;24(7):1553–1561. DOI: 10.1093/molbev/msm076

[92] Miller-Butterworth C.M., Murphy W.J., O’Brien S.J., et al. A Family Matter: Conclusive Resolution of the Taxonomic Position of the Long-Fingered Bats, Miniopterus // Mol Biol EVol. 2007. Vol. 24, No. 7. P. 1553–1561. DOI: 10.1093/molbev/msm076

[93] Agnarsson I, Zambrana-Torrelio CM, Flores-Saldana NP, May-Collado LJ. A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS Curr. 2011;3: RRN1212. DOI: 10.1371/currents.RRN1212

[94] Agnarsson I., Zambrana-Torrelio C.M., Flores-Saldana N.P., May-Collado L.J. A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia) // PLoS Curr. 2011. Vol. 3. ID RRN1212. DOI: 10.1371/currents.RRN1212

[95] Roehrs ZP, Lack JB, Van Den Bussche RA. Tribal phylogenetic relationships within Vespertilioninae (Chiroptera: Vespertilionidae) based on mitochondrial and nuclear sequence data. J Mammal. 2010;91(5):1073–1092. DOI: 10.1644/09-MAMM-A-325.1

[96] Roehrs Z.P., Lack J.B., Van Den Bussche R.A. Tribal phylogenetic relationships within Vespertilioninae (Chiroptera: Vespertilionidae) based on mitochondrial and nuclear sequence data // J Mammal. 2010. Vol. 91, No. 5. P. 1073–1092. DOI: 10.1644/09-MAMM-A-325.1

[97] Zhang Q, Edwards SV. The evolution of intron size in amniotes: a role for powered flight? Genome Biol EVol. 2012;4(10):1033–1043. DOI: 10.1093/gbe/evs070

[98] Zhang Q., Edwards S.V. The evolution of intron size in amniotes: a role for powered flight? // Genome Biol EVol. 2012. Vol. 4, No. 10. P. 1033–1043. DOI: 10.1093/gbe/evs070

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Bondaruk D.D., Golubkova E.V., Mamon L.A.