Abstract
Infectious bursal disease virus (IBDV) is an important poultry pathogen. The VP2 protein of IBDV is the major host-protective immunogen. Although the functions of the VP2 protein have been well studied, the factors shaping synonymous codon usage bias and nucleotide composition in the VP2 gene have not yet been reported. In the present study, we have analyzed the relative synonymous codon usage and effective number of codons (ENC) using 69 IBDV VP2 genes. The major trend in codon usage variation was studied using correspondence analysis. The plot of ENC values and GC3s as well as the correlation between base composition and codon usage bias suggests that mutational pressure rather than natural selection is the main factor that determines the codon usage bias in the VP2 gene. In addition, other factors, such as the aromaticity, hydrophobicity and aliphatic index also influence the codon usage variation of the VP2 gene. This study represents a comprehensive analysis of IBDV VP2 gene codon usage patterns and provides a basic understanding of the codon usage bias.
References
Lukert PD, Leonard J, Davis RB (1975) Infectious bursal disease virus: antigen production and immunity. Am J Vet Res 36(4 Pt 2):539–540
Sharma JM, Kim IJ, Rautenschlein S, Yeh HY (2000) Infectious bursal disease virus of chickens: pathogenesis and immunosuppression. Dev Comp Immunol 24(2–3):223–235 (S0145-305X(99)00074-9)
Lasher HN, Davis VS (1997) History of infectious bursal disease in the U.S.A.—the first two decades. Avian Dis 41(1):11–19
Saif YM (1998) Infectious bursal disease and hemorrhagic enteritis. Poult Sci 77(8):1186–1189
Banda A, Villegas P, El-Attrache J (2003) Molecular characterization of infectious bursal disease virus from commercial poultry in the United States and Latin America. Avian Dis 47(1):87–95
Bahmaninejad MA, Hair-Bejo M, Omar AR, Aini I, Toroghi R (2008) Characterization of three infectious bursal disease virus isolates obtained from layer chickens in Iran. Acta Virol 52(3):167–174
Kasanga CJ, Yamaguchi T, Munang’andu HM, Ohya K, Fukushi H (2013) Genomic sequence of an infectious bursal disease virus isolate from Zambia: classical attenuated segment B reassortment in nature with existing very virulent segment A. Arch Virol 158(3):685–689. doi:10.1007/s00705-012-1531-4
Negash T, Gelaye E, Petersen H, Grummer B, Rautenschlein S (2012) Molecular evidence of very virulent infectious bursal disease viruses in chickens in Ethiopia. Avian Dis 56(3):605–610
Nagarajan MM, Kibenge FS (1997) Infectious bursal disease virus: a review of molecular basis for variations in antigenicity and virulence. Can J Vet Res 61(2):81–88
Jackwood DJ, Jackwood RJ (1994) Infectious bursal disease viruses: molecular differentiation of antigenic subtypes among serotype 1 viruses. Avian Dis 38(3):531–537
Snyder DB, Vakharia VN, Savage PK (1992) Naturally occurring-neutralizing monoclonal antibody escape variants define the epidemiology of infectious bursal disease viruses in the United States. Arch Virol 127(1–4):89–101
Caston JR, Martinez-Torrecuadrada JL, Maraver A, Lombardo E, Rodriguez JF, Casal JI, Carrascosa JL (2001) C terminus of infectious bursal disease virus major capsid protein VP2 is involved in definition of the T number for capsid assembly. J Virol 75(22):10815–10828. doi:10.1128/JVI.75.22.10815-10828.2001
Kumar S, Ahi YS, Salunkhe SS, Koul M, Tiwari AK, Gupta PK, Rai A (2009) Effective protection by high efficiency bicistronic DNA vaccine against infectious bursal disease virus expressing VP2 protein and chicken IL-2. Vaccine 27(6):864–869. doi:10.1016/j.vaccine.2008.11.085
Perozo F, Villegas AP, Fernandez R, Cruz J, Pritchard N (2009) Efficacy of single dose recombinant herpesvirus of turkey infectious bursal disease virus (IBDV) vaccination against a variant IBDV strain. Avian Dis 53(4):624–628
Zhou X, Wang D, Xiong J, Zhang P, Li Y, She R (2010) Protection of chickens, with or without maternal antibodies, against IBDV infection by a recombinant IBDV-VP2 protein. Vaccine 28(23):3990–3996. doi:10.1016/j.vaccine.2010.03.021
Fahey KJ, Chapman AJ, Macreadie IG, Vaughan PR, McKern NM, Skicko JI, Ward CW, Azad AA (1991) A recombinant subunit vaccine that protects progeny chickens from infectious bursal disease. Avian Pathol 20(3):447–460. doi:10.1080/03079459108418783
Kumar S (2015) DNA vaccine against infectious bursal disease virus: still more to explore. Vet Microbiol 175(2–4):389–390. doi:10.1016/j.vetmic.2014.12.014
Fernandez-Arias A, Martinez S, Rodriguez JF (1997) The major antigenic protein of infectious bursal disease virus, VP2, is an apoptotic inducer. J Virol 71(10):8014–8018
Deka H, Chakraborty S (2014) Compositional Constraint Is the Key Force in Shaping Codon Usage Bias in Hemagglutinin Gene in H1N1 Subtype of Influenza A Virus. Int J Genomics 2014:349139. doi:10.1155/2014/349139
Wang M, Liu YS, Zhou JH, Chen HT, Ma LN, Ding YZ, Liu WQ, Gu YX, Zhang J (2011) Analysis of codon usage in Newcastle disease virus. Virus Genes 42(2):245–253. doi:10.1007/s11262-011-0574-z
Ding YZ, You YN, Sun DJ, Chen HT, Wang YL, Chang HY, Pan L, Fang YZ, Zhang ZW, Zhou P, Lv JL, Liu XS, Shao JJ, Zhao FR, Lin T, Stipkovits L, Pejsak Z, Zhang YG, Zhang J (2014) The Effects of the Context-Dependent Codon Usage Bias on the Structure of the nsp1alpha of Porcine Reproductive and Respiratory Syndrome Virus. Biomed Res Int 2014:765320. doi:10.1155/2014/765320
Hu C, Chen J, Ye L, Chen R, Zhang L, Xue X (2014) Codon usage bias in human cytomegalovirus and its biological implication. Gene 545(1):5–14. doi:10.1016/j.gene.2014.05.018
Kumar CS, Kumar S (2014) Species based synonymous codon usage in fusion protein gene of Newcastle disease virus. PLoS One 9(12):e114754. doi:10.1371/journal.pone.0114754PONE-D-14-25870
Li WH (1997) Molecular Evolution. second edition edn. Sinauer Associates, Sunderland
Babbitt GA, Alawad MA, Schulze KV, Hudson AO (2014) Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid. Nucleic Acids Res. doi:10.1093/nar/gku811
Butt AM, Nasrullah I, Tong Y (2014) Genome-wide analysis of codon usage and influencing factors in chikungunya viruses. PLoS One 9(3):e90905. doi:10.1371/journal.pone.0090905PONE-D-13-50453
Grantham R, Gautier C, Gouy M (1980) Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type. Nucleic Acids Res 8(9):1893–1912
Gu W, Zhou T, Ma J, Sun X, Lu Z (2004) The relationship between synonymous codon usage and protein structure in Escherichia coli and Homo sapiens. Biosystems 73(2):89–97. doi:10.1016/j.biosystems.2003.10.001 (S0303264703001965)
Epstein RJ, Lin K, Tan TW (2000) A functional significance for codon third bases. Gene 245(2):291–298 (S0378-1119(00)00042-1)
Li Y, Wang C, Cheng X, Wu T, Zhang C (2011) Synonymous codon usage of the VP2 gene of a very virulent infectious bursal disease virus isolate serial passaged in chicken embryos. Biosystems 104(1):42–47. doi:10.1016/j.biosystems.2010.12.009
Ermolaeva MD (2001) Synonymous codon usage in bacteria. Curr Issues Mol Biol 3(4):91–97
Lynn DJ, Singer GA, Hickey DA (2002) Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res 30(19):4272–4277
Paul S, Bag SK, Das S, Harvill ET, Dutta C (2008) Molecular signature of hypersaline adaptation: insights from genome and proteome composition of halophilic prokaryotes. Genome Biol 9(4):R70. doi:10.1186/gb-2008-9-4-r70
Kober KM, Pogson GH (2013) Genome-wide patterns of codon bias are shaped by natural selection in the purple sea urchin, Strongylocentrotus purpuratus. G3 (Bethesda) 3(7):1069–1083. doi:10.1534/g3.113.005769 (g3.113.005769 [pii])
Sharp PM, Li WH (1986) Codon usage in regulatory genes in Escherichia coli does not reflect selection for ‘rare’ codons. Nucleic Acids Res 14(19):7737–7749
LA Sharp PM (1993) An atlas of drosophila genes. Oxford University Press, New York
Wright F (1990) The ‘effective number of codons’ used in a gene. Gene 87(1):23–29 (0378-1119(90)90491-9)
Ikai A (1980) Thermostability and aliphatic index of globular proteins. J Biochem 88(6):1895–1898
Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157(1):105–132 (0022-2836(82)90515-0 [pii])
Greenacre MJ (1984) Theory and applications of correspondence analysis. Academic Press, London
Zhong J, Li Y, Zhao S, Liu S, Zhang Z (2007) Mutation pressure shapes codon usage in the GC-Rich genome of foot-and-mouth disease virus. Virus Genes 35(3):767–776. doi:10.1007/s11262-007-0159-z
Jenkins GM, Holmes EC (2003) The extent of codon usage bias in human RNA viruses and its evolutionary origin. Virus Res 92(1):1–7 (S016817020200309X)
Lobry JR, Gautier C (1994) Hydrophobicity, expressivity and aromaticity are the major trends of amino-acid usage in 999 Escherichia coli chromosome-encoded genes. Nucleic Acids Res 22(15):3174–3180
Acknowledgments
We are thankful to Mr. Rohit Koul at Seasia Infotech for proofreading the manuscript. The IBDV research in our laboratory is currently supported by an IITG start-up grant, and partly by the Department of Biotechnology (NER-BPMC/2013/AAB21).
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Kumar, C.S., Hazarika, N.M.J. & Kumar, S. Analysis of synonymous codon usage in the VP2 protein gene of infectious bursal disease virus. Arch Virol 160, 2359–2366 (2015). https://doi.org/10.1007/s00705-015-2505-0
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DOI: https://doi.org/10.1007/s00705-015-2505-0