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BMC genomics2017; 18(1); 652; doi: 10.1186/s12864-017-4063-1

Genetic and codon usage bias analyses of polymerase genes of equine influenza virus and its relation to evolution.

Abstract: Equine influenza is a major health problem of equines worldwide. The polymerase genes of influenza virus have key roles in virus replication, transcription, transmission between hosts and pathogenesis. Hence, the comprehensive genetic and codon usage bias of polymerase genes of equine influenza virus (EIV) were analyzed to elucidate the genetic and evolutionary relationships in a novel perspective. Results: The group - specific consensus amino acid substitutions were identified in all polymerase genes of EIVs that led to divergence of EIVs into various clades. The consistent amino acid changes were also detected in the Florida clade 2 EIVs circulating in Europe and Asia since 2007. To study the codon usage patterns, a total of 281,324 codons of polymerase genes of EIV H3N8 isolates from 1963 to 2015 were systemically analyzed. The polymerase genes of EIVs exhibit a weak codon usage bias. The ENc-GC3s and Neutrality plots indicated that natural selection is the major influencing factor of codon usage bias, and that the impact of mutation pressure is comparatively minor. The methods for estimating host imposed translation pressure suggested that the polymerase acidic (PA) gene seems to be under less translational pressure compared to polymerase basic 1 (PB1) and polymerase basic 2 (PB2) genes. The multivariate statistical analysis of polymerase genes divided EIVs into four evolutionary diverged clusters - Pre-divergent, Eurasian, Florida sub-lineage 1 and 2. Conclusions: Various lineage specific amino acid substitutions observed in all polymerase genes of EIVs and especially, clade 2 EIVs underwent major variations which led to the emergence of a phylogenetically distinct group of EIVs originating from Richmond/1/07. The codon usage bias was low in all the polymerase genes of EIVs that was influenced by the multiple factors such as the nucleotide compositions, mutation pressure, aromaticity and hydropathicity. However, natural selection was the major influencing factor in defining the codon usage patterns and evolution of polymerase genes of EIVs.
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Publication Date: 2017-08-23 PubMed ID: 28830350PubMed Central: PMC5568313DOI: 10.1186/s12864-017-4063-1Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article delves into the complex genetic interactions of the polymerase genes in the Equine Influenza Virus (EIV), focusing on the factors that have influenced the evolution of these genes. Key findings indicate natural selection as a major driver of these genes’ evolution and the role of various mutations leading to diverse EIV clades.

Understanding Polymerase Genes in EIV

  • The research examined in-depth the polymerase genes present within the EIV. These genes have vital roles in the virus’s replication, transcription, and transmission between hosts. They also play a significant role in the pathogenesis of the virus.
  • By analyzing the genetic sequences and codon usage bias of these genes, the researchers aimed to build a better understanding of the genetic relationships and the evolution of the EIV.
  • Through their research, they managed to identify group-specific consensus amino acid substitutions in all polymerase genes of EIV, leading to divergence into different clades, which are groups of organisms with a common ancestor.

Nature and Evolution of Codon Usage

  • A total of 281,324 codons of polymerase genes of EIV H3N8 isolates from 1963 to 2015 were analyzed to study codon usage patterns.
  • The polymerase genes in EIV exhibited a weak codon usage bias, indicating a lack of preference for specific codons in gene sequences.
  • The influencing factors of this bias were found to be a mixture of natural selection and mutation pressure, with natural selection playing a greater role.
  • Additional influences such as nucleotide compositions, aromaticity, and hydropathicity also played a part in shaping the codon usage patterns.

Impact on EIV Evolution

  • The polymerase acidic (PA) gene was found to be under less translational pressure compared to polymerase basic 1 (PB1) and polymerase basic 2 (PB2) genes. This difference suggests varying rates of mutation and evolution among these genes.
  • The EIVs were divided into four evolutionary diverged clusters based on multivariate statistical analysis of these polymerase genes.
  • Lineage-specific amino acid substitutions were observed across all polymerase genes. Particularly notable were major variations in the clade 2 EIVs, which have given rise to a distinctly different group of EIVs originating from Richmond/1/07.

Cite This Article

APA
Bera BC, Virmani N, Kumar N, Anand T, Pavulraj S, Rash A, Elton D, Rash N, Bhatia S, Sood R, Singh RK, Tripathi BN. (2017). Genetic and codon usage bias analyses of polymerase genes of equine influenza virus and its relation to evolution. BMC Genomics, 18(1), 652. https://doi.org/10.1186/s12864-017-4063-1

Publication

BMC genomics
ISSN: 1471-2164
NlmUniqueID: 100965258
Country: England
Language: English
Volume: 18
Issue: 1
Pages: 652
PII: 652

Researcher Affiliations

Bera, Bidhan Ch
  • National Research Centre on Equines, Sirsa Road, Hisar, Haryana, India.
Virmani, Nitin
  • National Research Centre on Equines, Sirsa Road, Hisar, Haryana, India. nvirmani@gmail.com.
Kumar, Naveen
  • National Institute of High Security Animal Diseases, Hathai Kheda Dam Road, Anand Nagar, Bhopal, Madhya Pradesh, India.
Anand, Taruna
  • National Research Centre on Equines, Sirsa Road, Hisar, Haryana, India.
Pavulraj, S
  • National Research Centre on Equines, Sirsa Road, Hisar, Haryana, India.
Rash, Adam
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, Suffolk, CB8 7UU, UK.
Elton, Debra
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, Suffolk, CB8 7UU, UK.
Rash, Nicola
  • Animal Health Trust, Lanwades Park, Kentford, Newmarket, Suffolk, CB8 7UU, UK.
Bhatia, Sandeep
  • National Institute of High Security Animal Diseases, Hathai Kheda Dam Road, Anand Nagar, Bhopal, Madhya Pradesh, India.
Sood, Richa
  • National Institute of High Security Animal Diseases, Hathai Kheda Dam Road, Anand Nagar, Bhopal, Madhya Pradesh, India.
Singh, Raj Kumar
  • Indian Veterinary Research Institute, Izatnagar, Bareilly, Uttar Pradesh, India.
Tripathi, Bhupendra Nath
  • National Research Centre on Equines, Sirsa Road, Hisar, Haryana, India.

MeSH Terms

  • Codon / genetics
  • DNA-Directed DNA Polymerase / genetics
  • Evolution, Molecular
  • Influenza A Virus, H3N8 Subtype / enzymology
  • Influenza A Virus, H3N8 Subtype / genetics
  • Phylogeny
  • Selection, Genetic

Conflict of Interest Statement

ETHICS APPROVAL AND CONSENT TO PARTICIPATE: Not applicable. CONSENT FOR PUBLICATION: Not applicable. COMPETING INTERESTS: The authors declare that they have no competing interests. PUBLISHER’S NOTE: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

This article includes 108 references
  1. Newton JR, Daly JM, Spencer L, Mumford JA. Description of the outbreak of equine influenza (H3N8) in the United Kingdom in 2003, during which recently vaccinated horses in Newmarket developed respiratory disease.. Vet Rec 2006 Feb 11;158(6):185-92.
    doi: 10.1136/vr.158.6.185pubmed: 16474051google scholar: lookup
  2. Barbic L, Madic J, Turk N, Daly J. Vaccine failure caused an outbreak of equine influenza in Croatia.. Vet Microbiol 2009 Jan 1;133(1-2):164-71.
    doi: 10.1016/j.vetmic.2008.06.009pubmed: 18632226google scholar: lookup
  3. Steinbrück L, Klingen TR, McHardy AC. Computational prediction of vaccine strains for human influenza A (H3N2) viruses.. J Virol 2014 Oct;88(20):12123-32.
    doi: 10.1128/JVI.01861-14pmc: PMC4178748pubmed: 25122778google scholar: lookup
  4. Ping J, Lopes TJS, Nidom CA, Ghedin E, Macken CA, Fitch A, Imai M, Maher EA, Neumann G, Kawaoka Y. Development of high-yield influenza A virus vaccine viruses.. Nat Commun 2015 Sep 2;6:8148.
    doi: 10.1038/ncomms9148pmc: PMC4569720pubmed: 26334134google scholar: lookup
  5. Bryant NA, Rash AS, Russell CA, Ross J, Cooke A, Bowman S, MacRae S, Lewis NS, Paillot R, Zanoni R, Meier H, Griffiths LA, Daly JM, Tiwari A, Chambers TM, Newton JR, Elton DM. Antigenic and genetic variations in European and North American equine influenza virus strains (H3N8) isolated from 2006 to 2007.. Vet Microbiol 2009 Jul 2;138(1-2):41-52.
    doi: 10.1016/j.vetmic.2009.03.004pubmed: 19346084google scholar: lookup
  6. Damiani AM, Scicluna MT, Ciabatti I, Cardeti G, Sala M, Vulcano G, Cordioli P, Martella V, Amaddeo D, Autorino GL. Genetic characterization of equine influenza viruses isolated in Italy between 1999 and 2005.. Virus Res 2008 Jan;131(1):100-5.
    doi: 10.1016/j.virusres.2007.08.001pubmed: 17889395google scholar: lookup
  7. Lai AC, Chambers TM, Holland RE Jr, Morley PS, Haines DM, Townsend HG, Barrandeguy M. Diverged evolution of recent equine-2 influenza (H3N8) viruses in the Western Hemisphere.. Arch Virol 2001;146(6):1063-74.
    doi: 10.1007/s007050170106pubmed: 11504416google scholar: lookup
  8. Daly JM, Lai AC, Binns MM, Chambers TM, Barrandeguy M, Mumford JA. Antigenic and genetic evolution of equine H3N8 influenza A viruses.. J Gen Virol 1996 Apr;77 ( Pt 4):661-71.
    doi: 10.1099/0022-1317-77-4-661pubmed: 8627254google scholar: lookup
  9. Bountouri M, Ntafis V, Fragkiadaki E, Kanellos T, Xylouri E. Phylogenetic analysis of the five internal genes and evolutionary pathways of the Greek H3N8 equine influenza virus. Nat Sci 2012;4:839–847.
  10. Kirkland PD, Finlaison DS, Crispe E, Hurt AC. Influenza virus transmission from horses to dogs, Australia.. Emerg Infect Dis 2010 Apr;16(4):699-702.
    doi: 10.3201/eid1604.091489pmc: PMC3321956pubmed: 20350392google scholar: lookup
  11. Daly JM, Blunden AS, Macrae S, Miller J, Bowman SJ, Kolodziejek J, Nowotny N, Smith KC. Transmission of equine influenza virus to English foxhounds.. Emerg Infect Dis 2008 Mar;14(3):461-4.
    doi: 10.3201/eid1403.070643pmc: PMC2570814pubmed: 18325262google scholar: lookup
  12. Crawford PC, Dubovi EJ, Castleman WL, Stephenson I, Gibbs EP, Chen L, Smith C, Hill RC, Ferro P, Pompey J, Bright RA, Medina MJ, Johnson CM, Olsen CW, Cox NJ, Klimov AI, Katz JM, Donis RO. Transmission of equine influenza virus to dogs.. Science 2005 Oct 21;310(5747):482-5.
    doi: 10.1126/science.1117950pubmed: 16186182google scholar: lookup
  13. Tu J, Zhou H, Jiang T, Li C, Zhang A, Guo X, Zou W, Chen H, Jin M. Isolation and molecular characterization of equine H3N8 influenza viruses from pigs in China.. Arch Virol 2009;154(5):887-90.
    doi: 10.1007/s00705-009-0381-1pubmed: 19396578google scholar: lookup
  14. Fodor E. The RNA polymerase of influenza a virus: mechanisms of viral transcription and replication.. Acta Virol 2013;57(2):113-22.
    doi: 10.4149/av_2013_02_113pubmed: 23600869google scholar: lookup
  15. Resa-Infante P, Jorba N, Coloma R, Ortin J. The influenza virus RNA synthesis machine: advances in its structure and function.. RNA Biol 2011 Mar-Apr;8(2):207-15.
    doi: 10.4161/rna.8.2.14513pmc: PMC3127100pubmed: 21358279google scholar: lookup
  16. Jambrina E, Bárcena J, Uez O, Portela A. The three subunits of the polymerase and the nucleoprotein of influenza B virus are the minimum set of viral proteins required for expression of a model RNA template.. Virology 1997 Sep 1;235(2):209-17.
    doi: 10.1006/viro.1997.8682pubmed: 9281500google scholar: lookup
  17. Chu C, Fan S, Li C, Macken C, Kim JH, Hatta M, Neumann G, Kawaoka Y. Functional analysis of conserved motifs in influenza virus PB1 protein.. PLoS One 2012;7(5):e36113.
    doi: 10.1371/journal.pone.0036113pmc: PMC3352917pubmed: 22615752google scholar: lookup
  18. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, He X, Lv Z, Ge R, Li X, Deng T, Fodor E, Rao Z, Liu Y. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site.. Nature 2009 Apr 16;458(7240):909-13.
    doi: 10.1038/nature07720pubmed: 19194458google scholar: lookup
  19. Sugiyama K, Obayashi E, Kawaguchi A, Suzuki Y, Tame JR, Nagata K, Park SY. Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase.. EMBO J 2009 Jun 17;28(12):1803-11.
    doi: 10.1038/emboj.2009.138pmc: PMC2699363pubmed: 19461581google scholar: lookup
  20. He X, Zhou J, Bartlam M, Zhang R, Ma J, Lou Z, Li X, Li J, Joachimiak A, Zeng Z, Ge R, Rao Z, Liu Y. Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus.. Nature 2008 Aug 28;454(7208):1123-6.
    doi: 10.1038/nature07120pubmed: 18615018google scholar: lookup
  21. Kobayashi M, Toyoda T, Ishihama A. Influenza virus PB1 protein is the minimal and essential subunit of RNA polymerase.. Arch Virol 1996;141(3-4):525-39.
    doi: 10.1007/BF01718315pubmed: 8645093google scholar: lookup
  22. Biswas SK, Nayak DP. Mutational analysis of the conserved motifs of influenza A virus polymerase basic protein 1.. J Virol 1994 Mar;68(3):1819-26.
    pmc: PMC236644pubmed: 8107244doi: 10.1128/jvi.68.3.1819-1826.1994google scholar: lookup
  23. Wise HM, Foeglein A, Sun J, Dalton RM, Patel S, Howard W, Anderson EC, Barclay WS, Digard P. A complicated message: Identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA.. J Virol 2009 Aug;83(16):8021-31.
    doi: 10.1128/JVI.00826-09pmc: PMC2715786pubmed: 19494001google scholar: lookup
  24. Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O'Neill R, Schickli J, Palese P, Henklein P, Bennink JR, Yewdell JW. A novel influenza A virus mitochondrial protein that induces cell death.. Nat Med 2001 Dec;7(12):1306-12.
    doi: 10.1038/nm1201-1306pubmed: 11726970google scholar: lookup
  25. Weeks-Gorospe JN, Hurtig HR, Iverson AR, Schuneman MJ, Webby RJ, McCullers JA, Huber VC. Naturally occurring swine influenza A virus PB1-F2 phenotypes that contribute to superinfection with Gram-positive respiratory pathogens.. J Virol 2012 Sep;86(17):9035-43.
    doi: 10.1128/JVI.00369-12pmc: PMC3416121pubmed: 22674997google scholar: lookup
  26. Varga ZT, Ramos I, Hai R, Schmolke M, García-Sastre A, Fernandez-Sesma A, Palese P. The influenza virus protein PB1-F2 inhibits the induction of type I interferon at the level of the MAVS adaptor protein.. PLoS Pathog 2011 Jun;7(6):e1002067.
    doi: 10.1371/journal.ppat.1002067pmc: PMC3111539pubmed: 21695240google scholar: lookup
  27. Dias A, Bouvier D, Crépin T, McCarthy AA, Hart DJ, Baudin F, Cusack S, Ruigrok RW. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit.. Nature 2009 Apr 16;458(7240):914-8.
    doi: 10.1038/nature07745pubmed: 19194459google scholar: lookup
  28. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, Sehr P, Lewis J, Ruigrok RW, Ortin J, Hart DJ, Cusack S. The structural basis for cap binding by influenza virus polymerase subunit PB2.. Nat Struct Mol Biol 2008 May;15(5):500-6.
    doi: 10.1038/nsmb.1421pubmed: 18454157google scholar: lookup
  29. Fechter P, Mingay L, Sharps J, Chambers A, Fodor E, Brownlee GG. Two aromatic residues in the PB2 subunit of influenza A RNA polymerase are crucial for cap binding.. J Biol Chem 2003 May 30;278(22):20381-8.
    doi: 10.1074/jbc.M300130200pubmed: 12646557google scholar: lookup
  30. Rodriguez A, Pérez-González A, Nieto A. Influenza virus infection causes specific degradation of the largest subunit of cellular RNA polymerase II.. J Virol 2007 May;81(10):5315-24.
    doi: 10.1128/JVI.02129-06pmc: PMC1900203pubmed: 17344288google scholar: lookup
  31. Hara K, Shiota M, Kido H, Ohtsu Y, Kashiwagi T, Iwahashi J, Hamada N, Mizoue K, Tsumura N, Kato H, Toyoda T. Influenza virus RNA polymerase PA subunit is a novel serine protease with Ser624 at the active site.. Genes Cells 2001 Feb;6(2):87-97.
    doi: 10.1046/j.1365-2443.2001.00399.xpubmed: 11260254google scholar: lookup
  32. Regan JF, Liang Y, Parslow TG. Defective assembly of influenza A virus due to a mutation in the polymerase subunit PA.. J Virol 2006 Jan;80(1):252-61.
    doi: 10.1128/JVI.80.1.252-261.2006pmc: PMC1317532pubmed: 16352550google scholar: lookup
  33. Jagger BW, Wise HM, Kash JC, Walters KA, Wills NM, Xiao YL, Dunfee RL, Schwartzman LM, Ozinsky A, Bell GL, Dalton RM, Lo A, Efstathiou S, Atkins JF, Firth AE, Taubenberger JK, Digard P. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response.. Science 2012 Jul 13;337(6091):199-204.
    doi: 10.1126/science.1222213pmc: PMC3552242pubmed: 22745253google scholar: lookup
  34. Hayashi T, MacDonald LA, Takimoto T. Influenza A Virus Protein PA-X Contributes to Viral Growth and Suppression of the Host Antiviral and Immune Responses.. J Virol 2015 Jun;89(12):6442-52.
    doi: 10.1128/JVI.00319-15pmc: PMC4474289pubmed: 25855745google scholar: lookup
  35. Desmet EA, Bussey KA, Stone R, Takimoto T. Identification of the N-terminal domain of the influenza virus PA responsible for the suppression of host protein synthesis.. J Virol 2013 Mar;87(6):3108-18.
    doi: 10.1128/JVI.02826-12pmc: PMC3592176pubmed: 23283952google scholar: lookup
  36. Ping J, Dankar SK, Forbes NE, Keleta L, Zhou Y, Tyler S, Brown EG. PB2 and hemagglutinin mutations are major determinants of host range and virulence in mouse-adapted influenza A virus.. J Virol 2010 Oct;84(20):10606-18.
    doi: 10.1128/JVI.01187-10pmc: PMC2950562pubmed: 20702632google scholar: lookup
  37. Naffakh N, Tomoiu A, Rameix-Welti MA, van der Werf S. Host restriction of avian influenza viruses at the level of the ribonucleoproteins.. Annu Rev Microbiol 2008;62:403-24.
    doi: 10.1146/annurev.micro.62.081307.162746pubmed: 18785841google scholar: lookup
  38. Rodriguez-Frandsen A, Alfonso R, Nieto A. Influenza virus polymerase: Functions on host range, inhibition of cellular response to infection and pathogenicity.. Virus Res 2015 Nov 2;209:23-38.
    doi: 10.1016/j.virusres.2015.03.017pubmed: 25916175google scholar: lookup
  39. Zhang H, Li X, Guo J, Li L, Chang C, Li Y, Bian C, Xu K, Chen H, Sun B. The PB2 E627K mutation contributes to the high polymerase activity and enhanced replication of H7N9 influenza virus.. J Gen Virol 2014 Apr;95(Pt 4):779-786.
    doi: 10.1099/vir.0.061721-0pubmed: 24394699google scholar: lookup
  40. Linster M, van Boheemen S, de Graaf M, Schrauwen EJA, Lexmond P, Mänz B, Bestebroer TM, Baumann J, van Riel D, Rimmelzwaan GF, Osterhaus ADME, Matrosovich M, Fouchier RAM, Herfst S. Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus.. Cell 2014 Apr 10;157(2):329-339.
    doi: 10.1016/j.cell.2014.02.040pmc: PMC4003409pubmed: 24725402google scholar: lookup
  41. Mehle A, Dugan VG, Taubenberger JK, Doudna JA. Reassortment and mutation of the avian influenza virus polymerase PA subunit overcome species barriers.. J Virol 2012 Feb;86(3):1750-7.
    doi: 10.1128/JVI.06203-11pmc: PMC3264373pubmed: 22090127google scholar: lookup
  42. Almond JW. A single gene determines the host range of influenza virus.. Nature 1977 Dec 15;270(5638):617-8.
    doi: 10.1038/270617a0pubmed: 593388google scholar: lookup
  43. Pepin KM, Domsic J, McKenna R. Genomic evolution in a virus under specific selection for host recognition.. Infect Genet Evol 2008 Dec;8(6):825-34.
    doi: 10.1016/j.meegid.2008.08.008pubmed: 18804189google scholar: lookup
  44. Chen H, Sun S, Norenburg JL, Sundberg P. Mutation and selection cause codon usage and bias in mitochondrial genomes of ribbon worms (Nemertea).. PLoS One 2014;9(1):e85631.
    doi: 10.1371/journal.pone.0085631pmc: PMC3893253pubmed: 24454907google scholar: lookup
  45. Grantham R, Gautier C, Gouy M, Mercier R, Pavé A. Codon catalog usage and the genome hypothesis.. Nucleic Acids Res 1980 Jan 11;8(1):r49-r62.
    pmc: PMC327256pubmed: 6986610doi: 10.1093/nar/8.1.197-cgoogle scholar: lookup
  46. Agashe D, Martinez-Gomez NC, Drummond DA, Marx CJ. Good codons, bad transcript: large reductions in gene expression and fitness arising from synonymous mutations in a key enzyme.. Mol Biol Evol 2013 Mar;30(3):549-60.
    doi: 10.1093/molbev/mss273pmc: PMC3563975pubmed: 23223712google scholar: lookup
  47. Plotkin JB, Kudla G. Synonymous but not the same: the causes and consequences of codon bias.. Nat Rev Genet 2011 Jan;12(1):32-42.
    doi: 10.1038/nrg2899pmc: PMC3074964pubmed: 21102527google scholar: lookup
  48. Hershberg R, Petrov DA. Selection on codon bias.. Annu Rev Genet 2008;42:287-99.
    doi: 10.1146/annurev.genet.42.110807.091442pubmed: 18983258google scholar: lookup
  49. Parmley JL, Hurst LD. How do synonymous mutations affect fitness?. Bioessays 2007 Jun;29(6):515-9.
    doi: 10.1002/bies.20592pubmed: 17508390google scholar: lookup
  50. Goñi N, Iriarte A, Comas V, Soñora M, Moreno P, Moratorio G, Musto H, Cristina J. Pandemic influenza A virus codon usage revisited: biases, adaptation and implications for vaccine strain development.. Virol J 2012 Nov 8;9:263.
    doi: 10.1186/1743-422X-9-263pmc: PMC3543350pubmed: 23134595google scholar: lookup
  51. Liu X, Wu C, Chen AY. Codon usage bias and recombination events for neuraminidase and hemagglutinin genes in Chinese isolates of influenza A virus subtype H9N2.. Arch Virol 2010 May;155(5):685-93.
    doi: 10.1007/s00705-010-0631-2pubmed: 20300785google scholar: lookup
  52. Kumar N, Bera BC, Greenbaum BD, Bhatia S, Sood R, Selvaraj P, Anand T, Tripathi BN, Virmani N. Revelation of Influencing Factors in Overall Codon Usage Bias of Equine Influenza Viruses.. PLoS One 2016;11(4):e0154376.
    doi: 10.1371/journal.pone.0154376pmc: PMC4847779pubmed: 27119730google scholar: lookup
  53. Lu G, Guo W, Qi T, Ma J, Zhao S, Tian Z, Pan J, Zhu C, Wang X, Xiang W. Genetic analysis of the PB1-F2 gene of equine influenza virus.. Virus Genes 2013 Oct;47(2):250-8.
    pubmed: 23780220doi: 10.1007/s11262-013-0935-xgoogle scholar: lookup
  54. Rash A, Woodward A, Bryant N, McCauley J, Elton D. An efficient genome sequencing method for equine influenza [H3N8] virus reveals a new polymorphism in the PA-X protein.. Virol J 2014 Sep 2;11:159.
    doi: 10.1186/1743-422X-11-159pmc: PMC4161859pubmed: 25183201google scholar: lookup
  55. Sharp PM, Li WH. An evolutionary perspective on synonymous codon usage in unicellular organisms.. J Mol Evol 1986;24(1-2):28-38.
    doi: 10.1007/BF02099948pubmed: 3104616google scholar: lookup
  56. Lee DY, Kim KA, Yu YG, Kim KS. Substitution of aspartic acid with glutamic acid increases the unfolding transition temperature of a protein.. Biochem Biophys Res Commun 2004 Jul 30;320(3):900-6.
    doi: 10.1016/j.bbrc.2004.06.031pubmed: 15240133google scholar: lookup
  57. Gibbs JS, Malide D, Hornung F, Bennink JR, Yewdell JW. The influenza A virus PB1-F2 protein targets the inner mitochondrial membrane via a predicted basic amphipathic helix that disrupts mitochondrial function.. J Virol 2003 Jul;77(13):7214-24.
    doi: 10.1128/JVI.77.13.7214-7224.2003pmc: PMC164823pubmed: 12805420google scholar: lookup
  58. Yamada H, Chounan R, Higashi Y, Kurihara N, Kido H. Mitochondrial targeting sequence of the influenza A virus PB1-F2 protein and its function in mitochondria.. FEBS Lett 2004 Dec 17;578(3):331-6.
    doi: 10.1016/j.febslet.2004.11.017pubmed: 15589841google scholar: lookup
  59. Krumbholz A, Philipps A, Oehring H, Schwarzer K, Eitner A, Wutzler P, Zell R. Current knowledge on PB1-F2 of influenza A viruses.. Med Microbiol Immunol 2011 May;200(2):69-75.
    doi: 10.1007/s00430-010-0176-8pubmed: 20953627google scholar: lookup
  60. Blazejewska P, Koscinski L, Viegas N, Anhlan D, Ludwig S, Schughart K. Pathogenicity of different PR8 influenza A virus variants in mice is determined by both viral and host factors.. Virology 2011 Mar 30;412(1):36-45.
    doi: 10.1016/j.virol.2010.12.047pubmed: 21256531google scholar: lookup
  61. Schnitzler SU, Schnitzler P. An update on swine-origin influenza virus A/H1N1: a review.. Virus Genes 2009 Dec;39(3):279-92.
    doi: 10.1007/s11262-009-0404-8pmc: PMC7088521pubmed: 19809872google scholar: lookup
  62. Bogs J, Veits J, Gohrbandt S, Hundt J, Stech O, Breithaupt A, Teifke JP, Mettenleiter TC, Stech J. Highly pathogenic H5N1 influenza viruses carry virulence determinants beyond the polybasic hemagglutinin cleavage site.. PLoS One 2010 Jul 27;5(7):e11826.
    doi: 10.1371/journal.pone.0011826pmc: PMC2910732pubmed: 20676399google scholar: lookup
  63. Murcia PR, Wood JL, Holmes EC. Genome-scale evolution and phylodynamics of equine H3N8 influenza A virus.. J Virol 2011 Jun;85(11):5312-22.
    doi: 10.1128/JVI.02619-10pmc: PMC3094979pubmed: 21430049google scholar: lookup
  64. Gorman OT, Bean WJ, Kawaoka Y, Webster RG. Evolution of the nucleoprotein gene of influenza A virus.. J Virol 1990 Apr;64(4):1487-97.
    pmc: PMC249282pubmed: 2319644doi: 10.1128/jvi.64.4.1487-1497.1990google scholar: lookup
  65. Gorman OT, Donis RO, Kawaoka Y, Webster RG. Evolution of influenza A virus PB2 genes: implications for evolution of the ribonucleoprotein complex and origin of human influenza A virus.. J Virol 1990 Oct;64(10):4893-902.
    pmc: PMC247979pubmed: 2398532doi: 10.1128/jvi.64.10.4893-4902.1990google scholar: lookup
  66. Virmani N, Bera BC, Singh BK, Shanmugasundaram K, Gulati BR, Barua S, Vaid RK, Gupta AK, Singh RK. Equine influenza outbreak in India (2008-09): virus isolation, sero-epidemiology and phylogenetic analysis of HA gene.. Vet Microbiol 2010 Jul 14;143(2-4):224-37.
    doi: 10.1016/j.vetmic.2009.12.007pubmed: 20053509google scholar: lookup
  67. Virmani N, Bera BC, Shanumugasundaram K, Singh BK, Gulati BR, Singh RK, Vaid RK. Genetic analysis of the matrix and non-structural genes of equine influenza virus (H3N8) from epizootic of 2008-2009 in India.. Vet Microbiol 2011 Aug 26;152(1-2):169-75.
    doi: 10.1016/j.vetmic.2011.04.011pubmed: 21620592google scholar: lookup
  68. Fodor E, Crow M, Mingay LJ, Deng T, Sharps J, Fechter P, Brownlee GG. A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs.. J Virol 2002 Sep;76(18):8989-9001.
    doi: 10.1128/JVI.76.18.8989-9001.2002pmc: PMC136441pubmed: 12186883google scholar: lookup
  69. Puthavathana P, Auewarakul P, Charoenying PC, Sangsiriwut K, Pooruk P, Boonnak K, Khanyok R, Thawachsupa P, Kijphati R, Sawanpanyalert P. Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand.. J Gen Virol 2005 Feb;86(Pt 2):423-433.
    doi: 10.1099/vir.0.80368-0pubmed: 15659762google scholar: lookup
  70. Zhu W, Zhu Y, Qin K, Yu Z, Gao R, Yu H, Zhou J, Shu Y. Mutations in polymerase genes enhanced the virulence of 2009 pandemic H1N1 influenza virus in mice.. PLoS One 2012;7(3):e33383.
    doi: 10.1371/journal.pone.0033383pmc: PMC3305307pubmed: 22438920google scholar: lookup
  71. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JS, Guan Y, Rambaut A. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic.. Nature 2009 Jun 25;459(7250):1122-5.
    doi: 10.1038/nature08182pubmed: 19516283google scholar: lookup
  72. Wong EH, Smith DK, Rabadan R, Peiris M, Poon LL. Codon usage bias and the evolution of influenza A viruses. Codon Usage Biases of Influenza Virus.. BMC Evol Biol 2010 Aug 19;10:253.
    doi: 10.1186/1471-2148-10-253pmc: PMC2933640pubmed: 20723216google scholar: lookup
  73. Zhao Y, Zheng H, Xu A, Yan D, Jiang Z, Qi Q, Sun J. Analysis of codon usage bias of envelope glycoprotein genes in nuclear polyhedrosis virus (NPV) and its relation to evolution.. BMC Genomics 2016 Aug 24;17(1):677.
    doi: 10.1186/s12864-016-3021-7pmc: PMC4997668pubmed: 27558469google scholar: lookup
  74. Wei L, He J, Jia X, Qi Q, Liang Z, Zheng H, Ping Y, Liu S, Sun J. Analysis of codon usage bias of mitochondrial genome in Bombyx mori and its relation to evolution.. BMC Evol Biol 2014 Dec 17;14:262.
    doi: 10.1186/s12862-014-0262-4pmc: PMC4276022pubmed: 25515024google scholar: lookup
  75. Zhou T, Gu W, Ma J, Sun X, Lu Z. Analysis of synonymous codon usage in H5N1 virus and other influenza A viruses.. Biosystems 2005 Jul;81(1):77-86.
    doi: 10.1016/j.biosystems.2005.03.002pubmed: 15917130google scholar: lookup
  76. Jenkins GM, Holmes EC. The extent of codon usage bias in human RNA viruses and its evolutionary origin.. Virus Res 2003 Mar;92(1):1-7.
    doi: 10.1016/S0168-1702(02)00309-Xpubmed: 12606071google scholar: lookup
  77. Cristina J, Moreno P, Moratorio G, Musto H. Genome-wide analysis of codon usage bias in Ebolavirus.. Virus Res 2015 Jan 22;196:87-93.
    doi: 10.1016/j.virusres.2014.11.005pubmed: 25445348google scholar: lookup
  78. Butt AM, Nasrullah I, Qamar R, Tong Y. Evolution of codon usage in Zika virus genomes is host and vector specific.. Emerg Microbes Infect 2016 Oct 12;5(10):e107.
    doi: 10.1038/emi.2016.106pmc: PMC5117728pubmed: 27729643google scholar: lookup
  79. Anhlan D, Grundmann N, Makalowski W, Ludwig S, Scholtissek C. Origin of the 1918 pandemic H1N1 influenza A virus as studied by codon usage patterns and phylogenetic analysis.. RNA 2011 Jan;17(1):64-73.
    doi: 10.1261/rna.2395211pmc: PMC3004067pubmed: 21068184google scholar: lookup
  80. Zhong J, Li Y, Zhao S, Liu S, Zhang Z. Mutation pressure shapes codon usage in the GC-Rich genome of foot-and-mouth disease virus.. Virus Genes 2007 Dec;35(3):767-76.
    doi: 10.1007/s11262-007-0159-zpmc: PMC7089325pubmed: 17768673google scholar: lookup
  81. Yin X, Lin Y, Cai W, Wei P, Wang X. Comprehensive analysis of the overall codon usage patterns in equine infectious anemia virus.. Virol J 2013 Dec 20;10:356.
    doi: 10.1186/1743-422X-10-356pmc: PMC3878193pubmed: 24359511google scholar: lookup
  82. Cheng X, Virk N, Chen W, Ji S, Ji S, Sun Y, Wu X. CpG usage in RNA viruses: data and hypotheses.. PLoS One 2013;8(9):e74109.
    doi: 10.1371/journal.pone.0074109pmc: PMC3781069pubmed: 24086312google scholar: lookup
  83. Shackelton LA, Parrish CR, Holmes EC. Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses.. J Mol Evol 2006 May;62(5):551-63.
    doi: 10.1007/s00239-005-0221-1pubmed: 16557338google scholar: lookup
  84. Rabadan R, Levine AJ, Robins H. Comparison of avian and human influenza A viruses reveals a mutational bias on the viral genomes.. J Virol 2006 Dec;80(23):11887-91.
    doi: 10.1128/JVI.01414-06pmc: PMC1642607pubmed: 16987977google scholar: lookup
  85. Tao P, Dai L, Luo M, Tang F, Tien P, Pan Z. Analysis of synonymous codon usage in classical swine fever virus.. Virus Genes 2009 Feb;38(1):104-12.
    doi: 10.1007/s11262-008-0296-zpmc: PMC7089228pubmed: 18958611google scholar: lookup
  86. van Weringh A, Ragonnet-Cronin M, Pranckeviciene E, Pavon-Eternod M, Kleiman L, Xia X. HIV-1 modulates the tRNA pool to improve translation efficiency.. Mol Biol Evol 2011 Jun;28(6):1827-34.
    doi: 10.1093/molbev/msr005pmc: PMC3098512pubmed: 21216840google scholar: lookup
  87. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza A viruses.. Arch Virol 2001 Dec;146(12):2275-89.
    doi: 10.1007/s007050170002pubmed: 11811679google scholar: lookup
  88. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.. Mol Biol Evol 2011 Oct;28(10):2731-9.
    doi: 10.1093/molbev/msr121pmc: PMC3203626pubmed: 21546353google scholar: lookup
  89. Pond SL, Frost SD. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments.. Bioinformatics 2005 May 15;21(10):2531-3.
    doi: 10.1093/bioinformatics/bti320pubmed: 15713735google scholar: lookup
  90. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD. GARD: a genetic algorithm for recombination detection.. Bioinformatics 2006 Dec 15;22(24):3096-8.
    doi: 10.1093/bioinformatics/btl474pubmed: 17110367google scholar: lookup
  91. Kosakovsky Pond SL, Frost SD. Not so different after all: a comparison of methods for detecting amino acid sites under selection.. Mol Biol Evol 2005 May;22(5):1208-22.
    doi: 10.1093/molbev/msi105pubmed: 15703242google scholar: lookup
  92. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. Detecting individual sites subject to episodic diversifying selection.. PLoS Genet 2012;8(7):e1002764.
    doi: 10.1371/journal.pgen.1002764pmc: PMC3395634pubmed: 22807683google scholar: lookup
  93. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K. FUBAR: a fast, unconstrained bayesian approximation for inferring selection.. Mol Biol Evol 2013 May;30(5):1196-205.
    pmc: PMC3670733pubmed: 23420840doi: 10.1093/molbev/mst030google scholar: lookup
  94. Sharp PM, Li WH. Codon usage in regulatory genes in Escherichia coli does not reflect selection for 'rare' codons.. Nucleic Acids Res 1986 Oct 10;14(19):7737-49.
    doi: 10.1093/nar/14.19.7737pmc: PMC311793pubmed: 3534792google scholar: lookup
  95. Wright F. The 'effective number of codons' used in a gene.. Gene 1990 Mar 1;87(1):23-9.
    doi: 10.1016/0378-1119(90)90491-9pubmed: 2110097google scholar: lookup
  96. Comeron JM, Aguadé M. An evaluation of measures of synonymous codon usage bias.. J Mol Evol 1998 Sep;47(3):268-74.
    doi: 10.1007/PL00006384pubmed: 9732453google scholar: lookup
  97. Sueoka N. Intrastrand parity rules of DNA base composition and usage biases of synonymous codons.. J Mol Evol 1995 Mar;40(3):318-25.
    doi: 10.1007/BF00163236pubmed: 7723058google scholar: lookup
  98. Sueoka N. 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 1999 Sep 30;238(1):53-8.
    doi: 10.1016/S0378-1119(99)00320-0pubmed: 10570983google scholar: lookup
  99. Sueoka N. Directional mutation pressure and neutral molecular evolution.. Proc Natl Acad Sci U S A 1988 Apr;85(8):2653-7.
    doi: 10.1073/pnas.85.8.2653pmc: PMC280056pubmed: 3357886google scholar: lookup
  100. Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein.. J Mol Biol 1982 May 5;157(1):105-32.
    doi: 10.1016/0022-2836(82)90515-0pubmed: 7108955google scholar: lookup
  101. Puigbò P, Aragonès L, Garcia-Vallvé S. RCDI/eRCDI: a web-server to estimate codon usage deoptimization.. BMC Res Notes 2010 Mar 31;3:87.
    doi: 10.1186/1756-0500-3-87pmc: PMC2853550pubmed: 20356391google scholar: lookup
  102. Mueller S, Papamichail D, Coleman JR, Skiena S, Wimmer E. Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity.. J Virol 2006 Oct;80(19):9687-96.
    doi: 10.1128/JVI.00738-06pmc: PMC1617239pubmed: 16973573google scholar: lookup
  103. Zhou JH, Zhang J, Sun DJ, Ma Q, Chen HT, Ma LN, Ding YZ, Liu YS. The distribution of synonymous codon choice in the translation initiation region of dengue virus.. PLoS One 2013;8(10):e77239.
    doi: 10.1371/journal.pone.0077239pmc: PMC3808402pubmed: 24204777google scholar: lookup
  104. Greenacre M. Theory and applications of correspondence analysis. London: Academic; 1984.
  105. Peden JF. Analysis of Codon usage [dissertation] Nottingham University: Department of Genetics; 1999.
  106. Supek F, Vlahovicek K. INCA: synonymous codon usage analysis and clustering by means of self-organizing map.. Bioinformatics 2004 Sep 22;20(14):2329-30.
    doi: 10.1093/bioinformatics/bth238pubmed: 15059815google scholar: lookup
  107. Nakamura Y, Gojobori T, Ikemura T. Codon usage tabulated from international DNA sequence databases: status for the year 2000.. Nucleic Acids Res 2000 Jan 1;28(1):292.
    doi: 10.1093/nar/28.1.292pmc: PMC102460pubmed: 10592250google scholar: lookup
  108. Chan PP, Lowe TM. GtRNAdb: a database of transfer RNA genes detected in genomic sequence.. Nucleic Acids Res 2009 Jan;37(Database issue):D93-7.
    doi: 10.1093/nar/gkn787pmc: PMC2686519pubmed: 18984615google scholar: lookup

Citations

This article has been cited 22 times.
  1. Wang X, Sun J, Lu L, Pu FY, Zhang DR, Xie FQ. Evolutionary dynamics of codon usages for peste des petits ruminants virus. Front Vet Sci 2022;9:968034.
    doi: 10.3389/fvets.2022.968034pubmed: 36032280google scholar: lookup
  2. Li B, Wu H, Miao Z, Hu L, Zhou L, Lu Y. Codon Usage of Hepatitis E Viruses: A Comprehensive Analysis. Front Microbiol 2022;13:938651.
    doi: 10.3389/fmicb.2022.938651pubmed: 35801104google scholar: lookup
  3. Cui Y, Hou L, Pan Y, Feng X, Zhou J, Wang D, Guo J, Liu C, Shi Y, Sun T, Yang X, Zhu N, Tong X, Wang Y, Liu J. Reconstruction of the Evolutionary Origin, Phylodynamics, and Phylogeography of the Porcine Circovirus Type 3. Front Microbiol 2022;13:898212.
    doi: 10.3389/fmicb.2022.898212pubmed: 35663871google scholar: lookup
  4. Oladunni FS, Oseni SO, Martinez-Sobrido L, Chambers TM. Equine Influenza Virus and Vaccines. Viruses 2021 Aug 20;13(8).
    doi: 10.3390/v13081657pubmed: 34452521google scholar: lookup
  5. Kumar U, Khandia R, Singhal S, Puranik N, Tripathi M, Pateriya AK, Khan R, Emran TB, Dhama K, Munjal A, Alqahtani T, Alqahtani AM. Insight into Codon Utilization Pattern of Tumor Suppressor Gene EPB41L3 from Different Mammalian Species Indicates Dominant Role of Selection Force. Cancers (Basel) 2021 Jun 1;13(11).
    doi: 10.3390/cancers13112739pubmed: 34205890google scholar: lookup
  6. Yu X, Liu J, Li H, Liu B, Zhao B, Ning Z. Comprehensive analysis of synonymous codon usage patterns and influencing factors of porcine epidemic diarrhea virus. Arch Virol 2021 Jan;166(1):157-165.
    doi: 10.1007/s00705-020-04857-3pubmed: 33125585google scholar: lookup
  7. Sun J, Zhao W, Wang R, Zhang W, Li G, Lu M, Shao Y, Yang Y, Wang N, Gao Q, Su S. Analysis of the Codon Usage Pattern of HA and NA Genes of H7N9 Influenza A Virus. Int J Mol Sci 2020 Sep 27;21(19).
    doi: 10.3390/ijms21197129pubmed: 32992529google scholar: lookup
  8. Dutta R, Buragohain L, Borah P. Analysis of codon usage of severe acute respiratory syndrome corona virus 2 (SARS-CoV-2) and its adaptability in dog. Virus Res 2020 Oct 15;288:198113.
    doi: 10.1016/j.virusres.2020.198113pubmed: 32771430google scholar: lookup
  9. Guo F, Yang J, Pan J, Liang X, Shen X, Irwin DM, Chen RA, Shen Y. Origin and Evolution of H1N1/pdm2009: A Codon Usage Perspective. Front Microbiol 2020;11:1615.
    doi: 10.3389/fmicb.2020.01615pubmed: 32760376google scholar: lookup
  10. Nigam D, LaTourrette K, Souza PFN, Garcia-Ruiz H. Genome-Wide Variation in Potyviruses. Front Plant Sci 2019;10:1439.
    doi: 10.3389/fpls.2019.01439pubmed: 31798606google scholar: lookup
  11. Zhang W, Zhang L, He W, Zhang X, Wen B, Wang C, Xu Q, Li G, Zhou J, Veit M, Su S. Genetic Evolution and Molecular Selection of the HE Gene of Influenza C Virus. Viruses 2019 Feb 19;11(2).
    doi: 10.3390/v11020167pubmed: 30791465google scholar: lookup
  12. Kumar N, Kulkarni DD, Lee B, Kaushik R, Bhatia S, Sood R, Pateriya AK, Bhat S, Singh VP. Evolution of Codon Usage Bias in Henipaviruses Is Governed by Natural Selection and Is Host-Specific. Viruses 2018 Nov 1;10(11).
    doi: 10.3390/v10110604pubmed: 30388838google scholar: lookup
  13. Zhang X, Cai Y, Zhai X, Liu J, Zhao W, Ji S, Su S, Zhou J. Comprehensive Analysis of Codon Usage on Rabies Virus and Other Lyssaviruses. Int J Mol Sci 2018 Aug 14;19(8).
    doi: 10.3390/ijms19082397pubmed: 30110957google scholar: lookup
  14. Li G, Wang H, Wang S, Xing G, Zhang C, Zhang W, Liu J, Zhang J, Su S, Zhou J. Insights into the genetic and host adaptability of emerging porcine circovirus 3. Virulence 2018;9(1):1301-1313.
    doi: 10.1080/21505594.2018.1492863pubmed: 29973122google scholar: lookup
  15. Li G, Wang R, Zhang C, Wang S, He W, Zhang J, Liu J, Cai Y, Zhou J, Su S. Genetic and evolutionary analysis of emerging H3N2 canine influenza virus. Emerg Microbes Infect 2018 Apr 25;7(1):73.
    doi: 10.1038/s41426-018-0079-0pubmed: 29691381google scholar: lookup
  16. Man Y, Wang H, Xu X, Li D, Ji J, Yao L, Bi Y, Xie Q. Natural selection dominates the codon preference and host adaptability of the novel goose astrovirus related to gout symptons, with non-structural protein playing a key role. Poult Sci 2026 Mar;105(3):106320.
    doi: 10.1016/j.psj.2025.106320pubmed: 41485352google scholar: lookup
  17. Ren X, Xu L, Yan Y, Wang Y, Huang A. Codon Usage Bias Analysis of Citrus Leaf Blotch Virus. Viruses 2025 Nov 12;17(11).
    doi: 10.3390/v17111497pubmed: 41305517google scholar: lookup
  18. Aktürk Dizman Y. Codon Usage Bias of the Polyphenol Oxidase Genes in Camellia sinensis: A Comprehensive Analysis. Plants (Basel) 2025 Oct 4;14(19).
    doi: 10.3390/plants14193074pubmed: 41095214google scholar: lookup
  19. Wei Y, Cai Y, Han X, Han Z, Zhang Y, Xu Y, Jiang C, Li Q. Genetic and codon usage analyses reveal the evolution of the seoul virus. Front Genet 2025;16:1544577.
    doi: 10.3389/fgene.2025.1544577pubmed: 40574799google scholar: lookup
  20. Rahman SU, Hu Y, Rehman HU, Alrashed MM, Attia KA, Ullah U, Liang H. Analysis of synonymous codon usage bias of Lassa virus. Virus Res 2025 Mar;353:199528.
    doi: 10.1016/j.virusres.2025.199528pubmed: 39832535google scholar: lookup
  21. Aktürk Dizman Y. Codon usage bias analysis of the gene encoding NAD(+)-dependent DNA ligase protein of Invertebrate iridescent virus 6. Arch Microbiol 2023 Oct 9;205(11):352.
    doi: 10.1007/s00203-023-03688-5pubmed: 37812231google scholar: lookup
  22. Chambers TM. Equine Influenza. Cold Spring Harb Perspect Med 2022 Jan 4;12(1).
    doi: 10.1101/cshperspect.a038331pubmed: 32152243google scholar: lookup
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