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Codon usage vis-a-vis start and stop codon context analysis of three dicot species

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Abstract

To understand the variation in genomic composition and its effect on codon usage, we performed the comparative analysis of codon usage and nucleotide usage in the genes of three dicots, Glycine max, Arabidopsis thaliana and Medicago truncatula. The dicot genes were found to be A/T rich and have predominantly A-ending and/or T-ending codons. GC3s directly mimic the usage pattern of global GC content. Relative synonymous codon usage analysis suggests that the high usage frequency of A/T over G/C mononucleotide containing codons in AT-rich dicot genome is due to compositional constraint as a factor of codon usage bias. Odds ratio analysis identified the dinucleotides TpG, TpC, GpA, CpA and CpT as over-represented, where, CpG and TpA as under-represented dinucleotides. The results of (NcExp−NcObs)/NcExp plot suggests that selection pressure other than mutation played a significant role in influencing the pattern of codon usage in these dicots. PR2 analysis revealed the significant role of selection pressure on codon usage. Analysis of varience on codon usage at start and stop site showed variation in codon selection in these sites. This study provides evidence that the dicot genes were subjected to compositional selection pressure.

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References

  • Adzhubei A. A., Adzhubei I. A., Krasheninnikov I. A. and Neidle S. 1996 Non-random usage of ‘degenerate’ codons is related to protein three-dimensional structure. FEBS Lett. 399, 78–82.

    Article  CAS  PubMed  Google Scholar 

  • Angellotti M. C., Bhuiyan S. B., Chen G. and Wan X. 2007 CodonO: codon usage bias analysis within and across genomes. Nucleic Acids Res. 35, W132–W136.

    Article  PubMed  PubMed Central  Google Scholar 

  • Behura S. K. and Severson D. W. 2012 Comparative analysis of codon usage bias and codon context patterns between dipteran and hymenopteran sequenced genomes. PLoS One 7, e43111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bellgard M., Schibeci D., Trifonov E. and Gojobori T. 2001 Early detection of G + C differences in bacterial species inferred from the comparative analysis of the two completely sequenced Helicobacter pylori strains. J. Mol. Evol. 53, 465–468.

    Article  CAS  PubMed  Google Scholar 

  • Berg O. G. 1996 Selection intensity for codon bias and the effective population size of Escherichia coli. Genetics 142, 1379–1382.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bulmer M. 1991 The selection-mutation-drift theory of synonymous codon usage. Genetics 129, 897–907.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Butt A. M., Nasrullah I. and 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 

  • Chen Y. 2013 A comparison of synonymous codon usage bias patterns in DNA and RNA virus genomes: quantifying the relative importance of mutational pressure and natural selection. Biomed. Res. Int. Article ID 406342 (https://doi.org/10.1155/2013/406342).

  • Clement Y., Fustier M. A., Nabholz B. and Glemin S. 2014 The bimodal distribution of genic GC content is ancestral to monocot species. Genome Biol. Evol. 7, 336–348.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cristina J., Fajardo A., Sonora M., Moratorio G. and Musto H. 2016 A detailed comparative analysis of codon usage bias in Zika virus. Virus Res. 223, 147–152.

    Article  CAS  PubMed  Google Scholar 

  • De Amicis F. and Marchetti S. 2000 Intercodon dinucleotides affect codon choice in plant genes. Nucleic Acids Res. 28, 3339–3345.

    Article  PubMed  PubMed Central  Google Scholar 

  • Doherty A. and McInerney J. O. 2013 Translational selection frequently overcomes genetic drift in shaping synonymous codon usage patterns in vertebrates. Mol. Biol. Evol. 30, 2263–2267.

    Article  CAS  PubMed  Google Scholar 

  • Duret L. and Mouchiroud D. 1999 Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc. Natl. Acad. Sci. USA 96, 4482–4487.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodarzi H., Torabi N., Najafabadi H. S. and Archetti M. 2008 Amino acid and codon usage profiles: adaptive changes in the frequency of amino acids and codons. Gene 407, 30–41.

    Article  CAS  PubMed  Google Scholar 

  • Goodman D. B., Church G. M. and Kosuri S. 2013 Causes and effects of N-terminal codon bias in bacterial genes. Science 342, 475–479.

    Article  CAS  PubMed  Google Scholar 

  • Guo X., Bao J. and Fan L. 2007 Evidence of selectively driven codon usage in rice: implications for GC content evolution of Gramineae genes. FEBS Lett. 581, 1015–1021.

    Article  CAS  PubMed  Google Scholar 

  • Gupta S. K. and Ghosh T. C. 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. K., Bhattacharyya T. K. and Ghosh T. C. 2004 Synonymous codon usage in Lactococcus lactis: mutational bias versus translational selection. J. Biomol. Struct. Dyn. 21, 527–536.

    Article  CAS  PubMed  Google Scholar 

  • Gustafsson C., Govindarajan S. and Minshull J. 2004 Codon bias and heterologous protein expression. Trends Biotechnol. 22, 346–353.

    Article  CAS  PubMed  Google Scholar 

  • Hambuch T. M. and Parsch J. 2005 Patterns of synonymous codon usage in Drosophila melanogaster genes with sex-biased expression. Genetics 170, 1691–1700.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu J., Zhao X., Zhang Z. and Yu J. 2007. Compositional dynamics of guanine and cytosine content in prokaryotic genomes. Res. Microbiol. 158, 363–370.

    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: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J. Mol. Biol. 151, 389–409.

    Article  CAS  PubMed  Google Scholar 

  • Jia X., Liu S., Zheng H., Li B., Qi Q., Wei L. et al. 2015 Non-uniqueness of factors constraint on the codon usage in Bombyx mori. BMC Genomics 16, 356.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kariin S. and Burge C. 1995 Dinucleotide relative abundance extremes: a genomic signature. Trends Genet. 11, 283–290.

    Article  Google Scholar 

  • Karlin S., Mrazek J. and Campbell A. M. 1998 Codon usages in different gene classes of the Escherichia coli genome. Mol. Microbiol. 29, 1341–1355.

    Article  CAS  PubMed  Google Scholar 

  • Kawabe A. and Miyashita N. T. 2003 Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet. Sys. 78, 343–352.

    Article  CAS  Google Scholar 

  • Kudla G., Lipinski L., Caffin F., Helwak A. and Zylicz M. 2006 High guanine and cytosine content increases mRNA levels in mammalian cells. PLoS Biol. 4, e180.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li X., Song H., Kuang Y., Chen S., Tian P., Li C. et al. 2016 Genome-wide analysis of codon usage bias in Epichloe festucae. Int. J. Mol. Sci. 17, 1138.

    Article  CAS  PubMed Central  Google Scholar 

  • Liu Q. and Xue Q. 2005 Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species. J. Genet. 84, 55–62.

    Article  CAS  PubMed  Google Scholar 

  • Mirsafian H., Mat Ripen A., Singh A., Teo P. H., Merican A. F. and Mohamad S. B. 2014 A comparative analysis of synonymous codon usage bias pattern in human albumin superfamily. Sci. World J. 2014, 639682.

    Google Scholar 

  • Morton B. R., Bi I. V., McMullen M. D. and Gaut B. S. 2006 Variation in mutation dynamics across the maize genome as a function of regional and flanking base composition. Genetics 172, 569–577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mudge J., Cannon S. B., Kalo P., Oldroyd G. E., Roe B. A., Town C. D. et al. 2005 Highly syntenic regions in the genomes of soybean, Medicago truncatula, and Arabidopsis thaliana. BMC Plant Biol. 5, 1.

    Article  Google Scholar 

  • Nasrullah I., Butt A. M., Tahir S., Idrees M. and Tong Y. 2015 Genomic analysis of codon usage shows influence of mutation pressure, natural selection, and host features on Marburg virus evolution. BMC Evol. Biol. 15, 1.

    Article  Google Scholar 

  • Plotkin J. B., Dushoff J. and Fraser H. B. 2004 Detecting selection using a single genome sequence of M. tuberculosis and P. falciparum. Nature 428, 942–945.

    Article  CAS  PubMed  Google Scholar 

  • Prat Y., Fromer M., Linial N. and Linial M. 2009 Codon usage is associated with the evolutionary age of genes in metazoan genomes. BMC Evol. Biol. 9, 285.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ressayre A., Glemin S., Montalent P., Serre-Giardi L., Dillmann C. and Joets J. 2015 Introns structure patterns of variation in nucleotide composition in Arabidopsis thaliana and rice protein-coding genes. Genome Biol. Evol. 7, 2913–2928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha E. P. and Danchin A. 2002 Base composition bias might result from competition for metabolic resources. Trends Genet. 18, 291–294.

    Article  CAS  PubMed  Google Scholar 

  • Serres-Giardi L., Belkhir K., David J. and Glemin S. 2012 Patterns and evolution of nucleotide landscapes in seed plants. Plant Cell 24, 1379–1397.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharp P. M. and 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 P. M. and 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 P. M., Emery L. R. and Zeng K. 2010 Forces that influence the evolution of codon bias. Phil. Trans. R. Soc. London Ser. B 365, 1203–1212.

    Article  CAS  Google Scholar 

  • Singer G. A. and Hickey D. A. 2003 Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. Gene 317, 39–47.

    Article  CAS  PubMed  Google Scholar 

  • Subramanian A. and Sarkar R. R. 2015 Comparison of codon usage bias across Leishmania and Trypanosomatids to understand mRNA secondary structure, relative protein abundance and pathway functions. Genomics 106, 232–241.

    Article  CAS  PubMed  Google Scholar 

  • Sueoka N. 1988 Directional mutation pressure and neutral molecular evolution. Proc. Natl. Acad. Sci. USA 85, 2653–2657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sueoka N. 1999 Translation-coupled violation of parity rule 2 in human genes is not the cause of heterogeneity of the DNA G+C content of third codon position. Gene 238, 53–58.

    Article  CAS  PubMed  Google Scholar 

  • Tatarinova T., Elhaik E. and Pellegrini M. 2013 Cross-species analysis of genic GC3 content and DNA methylation patterns. Genome Biol. Evol. 5, 1443–1456.

    Article  CAS  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 

  • Xia X., Xie Z. and Li W. H. 2003 Effects of GC content and mutational pressure on the lengths of exons and coding sequences. J. Mol. Evol. 56, 362–370.

    Article  CAS  PubMed  Google Scholar 

  • Xiang H., Zhang R., Butler III R. R., Liu T., Zhang L., Pombert J.-F. et al. 2015 Comparative analysis of codon usage bias patterns in microsporidian genomes. PLoS One 10, e0129223.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan H., Mudge J., Kim D., Shoemaker R., Cook D. and Young N. 2004 Comparative physical mapping reveals features of microsynteny between Glycine max, Medicago truncatula, and Arabidopsis thaliana. Genome 47, 141–155.

    Article  CAS  PubMed  Google Scholar 

  • Yan H. H., Mudge J., Kim D. J., Larsen D., Shoemaker R. C., Cook D. R. et al. 2003 Estimates of conserved microsynteny among the genomes of Glycine max, Medicago truncatula and Arabidopsis thaliana. Theor. Appl. Genet. 106, 1256–1265.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Zhang W. J., Zhou J., Li Z. F., Wang L., Gu X. and Zhong Y. 2007 Comparative analysis of codon usage patterns among mitochondrion, chloroplast and nuclear genes in Triticum aestivum L. J. Integr. Plant Biol. 49, 246–254.

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu H., Kim D. J., Baek J. M., Choi H. K., Ellis L. C., Kuester H. et al. 2003 Syntenic relationships between Medicago truncatula and Arabidopsis reveal extensive divergence of genome organization. Plant Physiol. 131, 1018–1026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Authors are grateful to the University Grants Commission, New Delhi, India, for providing UGC-BSR Fellowship to carry out this research work. Authors are also grateful to the Assam University, Silchar, Assam, India for providing the research facility.

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Correspondence to Supriyo Chakraborty.

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Corresponding editor: Umesh Varshney

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Paul, P., Malakar, A.K. & Chakraborty, S. Codon usage vis-a-vis start and stop codon context analysis of three dicot species. J Genet 97, 97–107 (2018). https://doi.org/10.1007/s12041-018-0892-1

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