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Expression levels and codon usage patterns in nuclear genes of the filarial nematode Wucheraria bancrofti and the blood fluke Schistosoma haematobium

Published online by Cambridge University Press:  06 April 2016

G.A. Mazumder ,
A. Uddin  and
S. Chakraborty
G.A. Mazumder
Affiliation:
Department of Biotechnology, Assam University, Silchar-788011, Assam, India
A. Uddin
Affiliation:
Department of Biotechnology, Assam University, Silchar-788011, Assam, India
S. Chakraborty*
Affiliation:
Department of Biotechnology, Assam University, Silchar-788011, Assam, India
*
*E-mail: supriyoch_2008@rediffmail.com
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Abstract

Synonymous codons are used with different frequencies, a phenomenon known as codon bias, which exists in many genomes and is mainly resolute by mutation and selection. To elucidate the genetic characteristics and evolutionary relationship of Wucheraria bancrofti and Schistosoma haematobium we examined the pattern of synonymous codon usage in nuclear genes of both the species. The mean overall GC contents of W. bancrofti and S. haematobium were 43.41 and 36.37%, respectively, which suggests that genes in both the species were AT rich. The value of the High Effective Number of Codons in both species suggests that codon usage bias was weak. Both species had a wide range of P3 distribution in the neutrality plot, with a significant correlation between P12 and P3. The codons were closer to the axes in correspondence analysis, suggesting that mutation pressure influenced the codon usage pattern in these species. We have identified the more frequently used codons in these species, most codons ending with an A or T. The nucleotides A/T and C/G were not proportionally used at the third position of codons, which reveals that natural selection might influence the codon usage patterns. The regression equation of P12 on P3 suggests that natural selection might have played a major role, while mutational pressure played a minor role in codon usage pattern in both species. These results form the basis of exploring the evolutionary mechanisms and the heterologous expression of medically important proteins of W. bancrofti and S. haematobium.

Type
Research Papers
Information
Journal of Helminthology , Volume 91 , Issue 1 , January 2017 , pp. 72 - 79
Copyright
Copyright © Cambridge University Press 2016 

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References

Akashi, H. (1997) Codon bias evolution in Drosophila. Population genetics of mutation-selection drift. Gene 205, 269–278.CrossRefGoogle ScholarPubMed
Akashi, H. (2001) Gene expression and molecular evolution. Current Opinion in Genetics and Development 11, 660–666.CrossRefGoogle ScholarPubMed
Bockarie, M.J., Taylor, M.J. & Gyapong, J.O. (2009) Current practices in the management of lymphatic filariasis. Expert Review of Anti-infective Therapy 7, 595–605.CrossRefGoogle Scholar
Bulmer, M. (1987) Coevolution of codon usage and transfer RNA abundance. Nature 325, 728–730.CrossRefGoogle ScholarPubMed
Bulmer, M. (1988) Are codon usage patterns in unicellular organisms determined by selection–mutation balance? Journal of Evolutionary Biology 1, 15–26.CrossRefGoogle Scholar
Butt, A.M., Nasrullah, I. & Tong, Y. (2014) Genome-wide analysis of codon usage and influencing factors in chikungunya viruses. PLoS ONE 9, e90905.CrossRefGoogle ScholarPubMed
Chen, H.-T., Gu, Y.-X. & Liu, Y.S. (2013) Analysis of synonymous codon usage in dengue viruses. Journal of Animal and Veterinary Advances 12, 88–98.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 Research International 2013, 8.CrossRefGoogle Scholar
Cioli, D. & Pica-Mattoccia, L. (2003) Praziquantel. Parasitology Research 90, S3–S9.CrossRefGoogle ScholarPubMed
Eberhard, M.L., Hightower, A.W., Addiss, D.G. & Lammie, P.J. (1997) Clearance of Wuchereria bancrofti antigen after treatment with diethylcarbamazine or ivermectin. American Journal of Tropical Medicine and Hygiene 57, 483–486.CrossRefGoogle ScholarPubMed
Fadiel, A., Lithwick, S., Wanas, M.Q. & Cuticchia, A.J. (2001) Influence of intercodon and base frequencies on codon usage in filarial parasites. Genomics 74, 197–210.CrossRefGoogle ScholarPubMed
Fennoy, S.L. & Bailey-Serres, J. (1993) Synonymous codon usage in Zea mays L. nuclear genes is varied by levels of C- and G-ending codons. Nucleic Acids Research 21, 5294–5300.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Gustafsson, C., Govindarajan, S. & Minshull, J. (2004) Codon bias and heterologous protein expression. Trends in Biotechnology 22, 346–353.CrossRefGoogle ScholarPubMed
Hershberg, R. & Petrov, D.A. (2008) Selection on codon bias. Annual Review of Genetics 42, 287–299.CrossRefGoogle ScholarPubMed
Hou, Z. & Yang, N. (2001) Analysis of factors shaping S. pneumoniae codon usage. Yi Chuan Xue Bao (Acta Genetica Sinica) 29, 747–752.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. Journal of Molecular Biology 151, 389–409.CrossRefGoogle Scholar
Ikemura, T. (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Molecular Biology and Evolution 2, 13–34.Google ScholarPubMed
Jenkins, G.M. & Holmes, E.C. (2003) The extent of codon usage bias in human RNA viruses and its evolutionary origin. Virus Research 92, 1–7.CrossRefGoogle ScholarPubMed
Jia, W. & Higgs, P.G. (2008) Codon usage in mitochondrial genomes: distinguishing context-dependent mutation from translational selection. Molecular Biology and Evolution 25, 339–351.CrossRefGoogle ScholarPubMed
Jia, X., Liu, S., Zheng, H., Li, B. & Qi, Q. (2015) Non-uniqueness of factors constraint on the codon usage in Bombyx mori . BMC Genomics 16, 356.CrossRefGoogle ScholarPubMed
Kaufmann, W.K. & Paules, R.S. (1996) DNA damage and cell cycle checkpoints. FASEB Journal 10, 238–247.CrossRefGoogle ScholarPubMed
Knight, R.D., Freeland, S.J. & Landweber, L.F. (2001) A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biology 2, research0010.CrossRefGoogle ScholarPubMed
Kumar, V., Abbas, A., Fausto, N. & Aster, J.C. (2010) Robbins and Cotran pathological basis of disease. 8th edn. Philadelphia, Elsevier, Sauders.Google Scholar
Kurland, C. (1992) Translational accuracy and the fitness of bacteria. Annual Review of Genetics 26, 29–50.CrossRefGoogle ScholarPubMed
Linacre, A. & ToBe, S.S. (2009) Species identification using DNA loci. p. 61 in Forensic Science in Wildlife Investigations. Boca Raton, Florida, CRC Press.Google Scholar
Lithwick, G. & Margalit, H. (2005) Relative predicted protein levels of functionally associated proteins are conserved across organisms. Nucleic Acids Research 33, 1051–1057.CrossRefGoogle ScholarPubMed
Liu, Q., Feng, Y., Zhao, X., Dong, H. & Xue, Q. (2004) Synonymous codon usage bias in Oryza sativa . Plant Science 167, 101–105.CrossRefGoogle Scholar
Manguin, S., Bangs, M.J., Pothikasikorn, J. & Chareonviriyaphap, T. (2010) Review on global co-transmission of human Plasmodium species and Wuchereria bancrofti by Anopheles mosquitoes . Infection, Genetics and Evolution 10, 159–177.CrossRefGoogle ScholarPubMed
Melrose, W.D. (2002) Lymphatic filariasis: new insights into an old disease. International Journal for Parasitology 32, 947–960.CrossRefGoogle ScholarPubMed
Moriyama, E.N. & Powell, J.R. (2001) Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli . Nucleic Acids Research 26, 3188–3193.CrossRefGoogle Scholar
Naya, H., Romero, H., Carels, N., Zavala, A. & Musto, H. (2001) Translational selection shapes codon usage in the GC-rich genome of Chlamydomonas reinhardtii . FEBS Letters 501, 127–130.CrossRefGoogle ScholarPubMed
Peixoto, L., Fernandez, V. & Musto, H. (2004) The effect of expression levels on codon usage in Plasmodium falciparum . Parasitology 128, 245–251.CrossRefGoogle ScholarPubMed
Plotkin, J.B. & Kudla, G. (2011) Synonymous but not the same: the causes and consequences of codon bias. Nature Reviews Genetics 12, 32–42.CrossRefGoogle Scholar
Powell, J.R. & Moriyama, E.N. (1997) Evolution of codon usage bias in Drosophila . Proceedings of the National Academy of Sciences, USA 94, 7784–7790.CrossRefGoogle ScholarPubMed
Shackelton, L.A., Parrish, C.R. & Holmes, E.C. (2006) Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. Journal of Molecular Evolution 62, 551–563.CrossRefGoogle ScholarPubMed
Sharp, P.M. & Matassi, G. (1994) Codon usage and genome evolution. Current Opinion in Genetics and Development 4, 851–860.CrossRefGoogle ScholarPubMed
Sharp, P.M., Tuohy, T.M.F. & Mosurski, K.R. (1986) Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Research 14, 5125–5143.CrossRefGoogle ScholarPubMed
Sharp, P.M., Cowe, E. & Higgins, D.G. (1988) Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Research 16, 8207–8211.CrossRefGoogle ScholarPubMed
Sueoka, N. (1988) Directional mutation pressure and neutral molecular evolution. Proceedings of the National Academy of Sciences, USA 85, 2653–2657.CrossRefGoogle ScholarPubMed
Sueoka, N. (1999) Two aspects of DNA base composition: G+C content and translation-coupled deviation from intra-strand rule of A = T and G = C. Journal of Molecular Evolution 49, 49–62.CrossRefGoogle ScholarPubMed
Wang, H.C. & Hickey, D.A. (2007) Rapid divergence of codon usage patterns within the rice genome. BMC Evolutionary Biology 7, S6.CrossRefGoogle ScholarPubMed
Wei, L., He, J., Jia, X., Qi, Q. & Liang, Z. (2014) Analysis of codon usage bias of mitochondrial genome in Bombyx mori and its relation to evolution. BMC Evolutionary Biology 14, 262.CrossRefGoogle ScholarPubMed
Wright, F. (1990) The ‘effective number of codons’ used in a gene. Gene 87, 23–29.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Zhang, Z., Dai, W. & Dai, D. (2013a) Synonymous codon usage in TTSuV2: analysis and comparison with TTSuV1. PLoS ONE 8, e81469.CrossRefGoogle ScholarPubMed
Zhang, Z., Dai, W., Wang, Y., Lu, C. & Fa, H. (2013b) Analysis of synonymous codon usage patterns in torque teno sus virus 1 (TTSuV1). Archives of Virology 158, 145–154.CrossRefGoogle ScholarPubMed
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