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Gene expression, nucleotide composition and codon usage bias of genes associated with human Y chromosome

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Abstract

Analysis of codon usage pattern is important to understand the genetic and evolutionary characteristics of genomes. We have used bioinformatic approaches to analyze the codon usage bias (CUB) of the genes located in human Y chromosome. Codon bias index (CBI) indicated that the overall extent of codon usage bias was low. The relative synonymous codon usage (RSCU) analysis suggested that approximately half of the codons out of 59 synonymous codons were most frequently used, and possessed a T or G at the third codon position. The codon usage pattern was different in different genes as revealed from correspondence analysis (COA). A significant correlation between effective number of codons (ENC) and various GC contents suggests that both mutation pressure and natural selection affect the codon usage pattern of genes located in human Y chromosome. In addition, Y-linked genes have significant difference in GC contents at the second and third codon positions, expression level, and codon usage pattern of some codons like the SPANX genes in X chromosome.

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References

  • Ahn I, Jeong B-J, Bae S-E, Jung J, Son HS (2006) Genomic analysis of influenza A viruses, including avian flu (H5N1) strains. Eur J Epidemiol 21:511–519

    Article  CAS  PubMed  Google Scholar 

  • Akashi H (1997) Codon bias evolution in Drosophila. Population genetics of mutation-selection drift. Gene 205:269–278

    Article  CAS  PubMed  Google Scholar 

  • Ali S, Hasnain SE (2003) Genomics of the human Y-chromosome: 1. Association with male infertility. Gene 321:25–37

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen JL, Hall B (1982) Codon selection in yeast. J Biol Chem 257:3026–3031

    CAS  PubMed  Google Scholar 

  • Bianchi NO, Richard SM, Pavicic W (2006) Y chromosome instability in testicular cancer mutation research/reviews. Mutat Res 612:172–188

    Article  CAS  PubMed  Google Scholar 

  • Bulmer M (1988) Are codon usage patterns in unicellular organisms determined by selection-mutation balance? J Evol Biol 1:15–26

    Article  Google Scholar 

  • Butt AM, Nasrullah I, Tong Y (2014) Genome-wide analysis of codon usage and influencing factors in chikungunya viruses. PLoS One 9:e90905

    Article  PubMed  PubMed Central  Google Scholar 

  • Camiolo S, Farina L, Porceddu A (2012) The relation of codon bias to tissue-specific gene expression in Arabidopsis thaliana. Genetics 192:641–649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Chen H-T, Gu Y-X, Liu Y-S (2013a) Analysis of synonymous codon usage in dengue viruses. J Anim Vet Adv 12:88–98

    Google Scholar 

  • Chen L et al (2013b) Synonymous codon usage patterns in different parasitic platyhelminth mitochondrial genomes. Genet Mol Res 12:587–596

    Article  CAS  PubMed  Google Scholar 

  • Choudhury MN, Chakraborty S (2015) Codon usage pattern in human SPANX genes. Bioinformation 11:454

    Article  PubMed  PubMed Central  Google Scholar 

  • Choudhury MN, Chakraborty S (2016) Which evolutionary forces dictate codon usage in human testis specific genes? Int J Pharm Pharm Sci 8:24–28

    Article  CAS  Google Scholar 

  • Freire-Picos MA, Gonzalez-Siso MI, Rodríguez-Belmonte E, Rodríguez-Torres AM, Ramil E, Cerdan ME (1994) Codon usage in Kluyveromyces lactis and in yeast cytochrome c-encoding genes. Gene 139:43–49

    Article  CAS  PubMed  Google Scholar 

  • Gatherer D, McEwan NR (1997) Small regions of preferential codon usage and their effect on overall codon bias-the case of the plp gene. IUBMB Life 43:107–114

    Article  CAS  Google Scholar 

  • Gouy M, Gautier C (1982) Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 10:7055–7074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta S, Ghosh T (2001) Gene expressivity is the main factor in dictating the codon usage variation among the genes in Pseudomonas aeruginosa. Gene 273:63–70

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Bhattacharyya T, Ghosh TC (2004) Synonymous codon usage in Lactococcus lactis: mutational bias versus translational selection. J Biomol Struct Dyn 21:527–535

    Article  CAS  PubMed  Google Scholar 

  • Gyles C, Boerlin P (2013) Horizontally transferred genetic elements and their role in pathogenesis of bacterial disease Veterinary Pathology Online:0300985813511131

  • Hershberg R, Petrov DA (2008) Selection on codon bias. Annu Rev Genet 42:287–299

    Article  CAS  PubMed  Google Scholar 

  • Ikemura T (1981) Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J Mol Biol 146:1–21

    Article  CAS  PubMed  Google Scholar 

  • Jangravi Z et al (2012) A fresh look at the male-specific region of the human Y chromosome. J Proteome Res 12:6–22

    Article  PubMed  Google Scholar 

  • Jenkins GM, Holmes EC (2003) The extent of codon usage bias in human RNA viruses and its evolutionary origin. Virus Res 92:1–7

    Article  CAS  PubMed  Google Scholar 

  • Jia W, Higgs PG (2008) Codon usage in mitochondrial genomes: distinguishing context-dependent mutation from translational selection. Mol Biol Evol 25:339–351

    Article  CAS  PubMed  Google Scholar 

  • Jia X et al (2015) Non-uniqueness of factors constraint on the codon usage in Bombyx mori. BMC Genom 16:356

    Article  Google Scholar 

  • Jobling MA, Pandya A, Tyler-Smith C (1997) The Y chromosome in forensic analysis and paternity testing. Int J Legal Med 110:118–124

    Article  CAS  PubMed  Google Scholar 

  • Kanaya S, Yamada Y, Kinouchi M, Kudo Y, Ikemura T (2001) Codon usage and tRNA genes in eukaryotes: correlation of codon usage diversity with translation efficiency and with CG-dinucleotide usage as assessed by multivariate analysis. J Mol Evol 53:290–298

    Article  CAS  PubMed  Google Scholar 

  • Kane JF (1995) Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr Opin Biotechnol 6:494–500

    Article  CAS  PubMed  Google Scholar 

  • KLIMAN RM, HEY J (2003) Hill–Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. Genet Res 81:89–90

    Article  CAS  PubMed  Google Scholar 

  • Lin K, Kuang Y, Joseph JS, Kolatkar PR (2002) Conserved codon composition of ribosomal protein coding genes in Escherichia coli, Mycobacterium tuberculosis and Saccharomyces cerevisiae: lessons from supervised machine learning in functional genomics. Nucleic Acids Res 30:2599–2607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lloyd A, Sharp P (1992) Codons: a microcomputer program for codon usage analysis. J Hered 83:239–240

    Article  CAS  PubMed  Google Scholar 

  • Majewski J (2003) Dependence of mutational asymmetry on gene-expression levels in the human genome. Am J Hum Genet 73:688–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirsafian H, Mat Ripen A, Singh A, Teo PH, Merican AF, Mohamad SB (2014) A comparative analysis of synonymous codon usage bias pattern in human albumin superfamily. Sci World J 2014:1–7

    Google Scholar 

  • Moriyama EN, Powell JR (1998) Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. Nucleic Acids Res 26:3188–3193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palidwor GA, Perkins TJ, Xia X (2010) A general model of codon bias due to GC mutational bias. PLoS One 5:e13431

    Article  PubMed  PubMed Central  Google Scholar 

  • Peden JF (1999) Analysis of Codon Usage. University of Nottingham, Nottingham

    Google Scholar 

  • Plotkin JB, Kudla G (2011) Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12:32–42

    Article  CAS  PubMed  Google Scholar 

  • Plotkin JB, Robins H, Levine AJ (2004) Tissue-specific codon usage and the expression of human genes. Proc Natl Acad Sci USA 101:12588–12591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powell JR, Sezzi E, Moriyama EN, Gleason JM, Caccone A (2003) Analysis of a shift in codon usage in Drosophila. J Mol Evol 57:S214–S225

    Article  CAS  PubMed  Google Scholar 

  • Rocha EP (2004) Codon usage bias from tRNA’s point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res 14:2279–2286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roth A, Anisimova M, Cannarozzi GM (2012) Measuring codon usage bias Codon evolution: mechanisms and models New York. Oxford University Press Inc, Oxford, pp 189–217

    Book  Google Scholar 

  • Sauna ZE, Kimchi-Sarfaty C (2011) Understanding the contribution of synonymous mutations to human disease. Nat Rev Genet 12:683–691

    Article  CAS  PubMed  Google Scholar 

  • Sémon M, Lobry JR, Duret L (2006) No evidence for tissue-specific adaptation of synonymous codon usage in humans. Mol Biol Evol 23:523–529

    Article  PubMed  Google Scholar 

  • Shackelton LA, Parrish CR, Holmes EC (2006) Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. J Mol Evol 62:551–563

    Article  CAS  PubMed  Google Scholar 

  • Sharp PM, Li W-H (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24:28–38

    Article  CAS  PubMed  Google Scholar 

  • Sharp PM, Li W-H (1987) The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharp PM, Matassi G (1994) Codon usage and genome evolution. Current Opin Genet Dev 4:851–860

    Article  CAS  Google Scholar 

  • Sharp PM, Tuohy TM, Mosurski KR (1986) Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic acids Res 14:5125–5143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharp PM, Stenico M, Peden JF, Lloyd AT (1993) Codon usage: mutational bias, translational selection, or both? Biochem Soc Trans 21:835

    Article  CAS  PubMed  Google Scholar 

  • Sharp PM, Emery LR, Zeng K (2010) Forces that influence the evolution of codon bias. Philos Trans R Soc B Biol Sci 365:1203–1212

    Article  CAS  Google Scholar 

  • Shen W, Wang D, Ye B, Shi M, Ma L, Zhang Y, Zhao Z (2015) GC3 biased gene domains in mammalian genomes. Bioinformatics 31(19):3081–3084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Supek F, Vlahoviček K (2005) Comparison of codon usage measures and their applicability in prediction of microbial gene expressivity. BMC Bioinf 6:182

    Article  Google Scholar 

  • Suzuki H, Brown CJ, Forney LJ, Top EM (2008) Comparison of correspondence analysis methods for synonymous codon usage in bacteria. DNA Res 15:357–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Syvanen M (2012) Evolutionary implications of horizontal gene transfer. Annu Rev Genet 46:341–358

    Article  CAS  PubMed  Google Scholar 

  • Waldman YY, Tuller T, Shlomi T, Sharan R, Ruppin E (2010) Translation efficiency in humans: tissue specificity, global optimization and differences between developmental stages. Nucleic Acids Res 38:2964–2974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei L et al (2014) Analysis of codon usage bias of mitochondrial genome in Bombyx mori and its relation to evolution. BMC Evol Biol 14:262

    Article  PubMed  PubMed Central  Google Scholar 

  • Wright F (1990) The ‘effective number of codons’ used in a gene. Gene 87:23–29

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Luo X, Cai X (2014) Analysis of codon usage pattern in Taenia saginata based on a transcriptome dataset. Parasites Vectors 7:1–11

    Article  Google Scholar 

  • Zhang Z, Dai W, Dai D (2013a) Synonymous codon usage in TTSuV2: analysis and comparison with TTSuV1. PloS One 8:e81469

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Dai W, Wang Y, Lu C, Fan H (2013b) Analysis of synonymous codon usage patterns in torque teno sus virus 1 (TTSuV1). Arch Virol 158:145–154

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Zheng H, Xu A, Yan D, Jiang Z, Qi Q, Sun J (2016) Analysis of codon usage bias of envelope glycoprotein genes in nuclear polyhedrosis virus (NPV) and its relation to evolution. BMC Genom 17:677

    Article  Google Scholar 

  • Zheng Y et al (2007) Codon usage bias in Chlamydia trachomatis and the effect of codon modification in the MOMP gene on immune responses to vaccination This paper is one of a selection of papers in this Special Issue, entitled International Symposium on Recent Advances in Molecular, Clinical, and Social Medicine, and has undergone the Journal’s usual peer-review process. Biochem Cell Biol 85:218–226

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are thankful to the Department of Biotechnology, Assam University, Silchar for providing the lab facility to carry out this research work.

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Authors and Affiliations

  1. Department of Biotechnology, Assam University, Silchar, 788011, Assam, India

    Monisha Nath Choudhury & Supriyo Chakraborty

  2. Department of Zoology, Moinul Hoque Choudhury Memorial Science College, Algapur, 788150, Hailakandi, Assam, India

    Arif Uddin

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  1. Monisha Nath Choudhury
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Correspondence to Supriyo Chakraborty.

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Choudhury, M.N., Uddin, A. & Chakraborty, S. Gene expression, nucleotide composition and codon usage bias of genes associated with human Y chromosome. Genetica 145, 295–305 (2017). https://doi.org/10.1007/s10709-017-9965-y

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