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PloS one2016; 11(4); e0154376; doi: 10.1371/journal.pone.0154376

Revelation of Influencing Factors in Overall Codon Usage Bias of Equine Influenza Viruses.

Abstract: Equine influenza viruses (EIVs) of H3N8 subtype are culprits of severe acute respiratory infections in horses, and are still responsible for significant outbreaks worldwide. Adaptability of influenza viruses to a particular host is significantly influenced by their codon usage preference, due to an absolute dependence on the host cellular machinery for their replication. In the present study, we analyzed genome-wide codon usage patterns in 92 EIV strains, including both H3N8 and H7N7 subtypes by computing several codon usage indices and applying multivariate statistical methods. Relative synonymous codon usage (RSCU) analysis disclosed bias of preferred synonymous codons towards A/U-ended codons. The overall codon usage bias in EIVs was slightly lower, and mainly affected by the nucleotide compositional constraints as inferred from the RSCU and effective number of codon (ENc) analysis. Our data suggested that codon usage pattern in EIVs is governed by the interplay of mutation pressure, natural selection from its hosts and undefined factors. The H7N7 subtype was found less fit to its host (horse) in comparison to H3N8, by possessing higher codon bias, lower mutation pressure and much less adaptation to tRNA pool of equine cells. To the best of our knowledge, this is the first report describing the codon usage analysis of the complete genomes of EIVs. The outcome of our study is likely to enhance our understanding of factors involved in viral adaptation, evolution, and fitness towards their hosts.
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Publication Date: 2016-04-27 PubMed ID: 27119730PubMed Central: PMC4847779DOI: 10.1371/journal.pone.0154376Google 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 study analyzed how equine influenza viruses (EIVs) adapt to their hosts through changes in their codon usage, revealing that several factors, including mutation pressure and natural selection, play a role in this process.

Understanding Codon Usage in Equine Influenza Viruses

In this study, the researchers worked on understanding the codon usage patterns of equine influenza viruses. They focused on genome-wide codon usage patterns across 92 EIV strains from both H3N8 and H7N7 subtypes.

  • EIVs are responsible for severe respiratory infections in horses and can trigger significant outbreaks.
  • The codon usage of these viruses affects how they adapt to different hosts. Codons are sequences of three DNA or RNA nucleotides that correspond to a specific amino acid or signal during protein synthesis.

Study Methods and Data Analysis

Several methodologies were employed in analyzing the genome-wide codon usage patterns, including computing codon usage indices and utilizing multivariate statistical methods.

  • The researchers conducted a Relative Synonymous Codon Usage (RSCU) analysis, revealing that preferred synonymous codons are predominantly A/U-ended codons.
  • Through the application of RSCU and Effective Number of Codon(ENc) analyses, it was inferred that the overall codon usage bias in EIVs is mainly affected by nucleotide compositional constraints.

Findings and Significance

The study found that codon usage patterns in EIVs are governed by an interplay of factors, including mutation pressure, influences from natural hosts, and other undetermined factors.

  • Among the two studied EIV subtypes, H7N7 was found to be less adapted to its host (the horse), exhibiting a higher codon bias, lower mutation pressure, and less adaptation to the tRNA pool of equine cells.
  • These findings enhance our understanding of factors involved in viral adaptation, evolution, and fitness towards their hosts.
  • This research is significant as it is reportedly the first to describe the codon usage analysis of the complete genomes of EIVs.

Cite This Article

APA
Kumar N, Bera BC, Greenbaum BD, Bhatia S, Sood R, Selvaraj P, Anand T, Tripathi BN, Virmani N. (2016). Revelation of Influencing Factors in Overall Codon Usage Bias of Equine Influenza Viruses. PLoS One, 11(4), e0154376. https://doi.org/10.1371/journal.pone.0154376

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 11
Issue: 4
Pages: e0154376
PII: e0154376

Researcher Affiliations

Kumar, Naveen
  • Immunology Lab, National Institute of High Security Animal Diseases (NIHSAD), Bhopal, Madhya Pradesh, India.
Bera, Bidhan Chandra
  • Biotechnology Lab, Veterinary Type Culture Collection, National Research Center on Equines (NRCE), Hisar, Haryana, India.
Greenbaum, Benjamin D
  • Tisch Cancer Institute, Departments of Medicine, Hematology and Medical Pathology, and Pathology, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America.
Bhatia, Sandeep
  • Immunology Lab, National Institute of High Security Animal Diseases (NIHSAD), Bhopal, Madhya Pradesh, India.
Sood, Richa
  • Immunology Lab, National Institute of High Security Animal Diseases (NIHSAD), Bhopal, Madhya Pradesh, India.
Selvaraj, Pavulraj
  • Equine Pathology Lab, National Research Center on Equines (NRCE), Hisar, Haryana, India.
Anand, Taruna
  • Biotechnology Lab, Veterinary Type Culture Collection, National Research Center on Equines (NRCE), Hisar, Haryana, India.
Tripathi, Bhupendra Nath
  • Equine Pathology Lab, National Research Center on Equines (NRCE), Hisar, Haryana, India.
Virmani, Nitin
  • Equine Pathology Lab, National Research Center on Equines (NRCE), Hisar, Haryana, India.

MeSH Terms

  • Adaptation, Physiological / genetics
  • Animals
  • Biological Evolution
  • Codon
  • Gene Expression Regulation, Viral
  • Genetic Code
  • Genome, Viral
  • Horse Diseases / virology
  • Horses
  • Host-Pathogen Interactions
  • Influenza A Virus, H3N8 Subtype / genetics
  • Influenza A Virus, H3N8 Subtype / metabolism
  • Influenza A Virus, H7N7 Subtype / genetics
  • Influenza A Virus, H7N7 Subtype / metabolism
  • Models, Statistical
  • Mutation Rate
  • Orthomyxoviridae Infections / veterinary
  • Orthomyxoviridae Infections / virology
  • RNA, Transfer / genetics
  • RNA, Transfer / metabolism
  • Species Specificity
  • Virus Replication

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 83 references
  1. 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.
    pubmed: 11726970doi: 10.1038/nm1201-1306google scholar: lookup
  2. 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
  3. Webster RG. Are equine 1 influenza viruses still present in horses?. Equine Vet J 1993 Nov;25(6):537-8.
    pubmed: 8276003doi: 10.1111/j.2042-3306.1993.tb03009.xgoogle scholar: lookup
  4. Webster RG, Laver WG, Air GM, Schild GC. Molecular mechanisms of variation in influenza viruses.. Nature 1982 Mar 11;296(5853):115-21.
    pubmed: 6174870doi: 10.1038/296115a0google scholar: lookup
  5. Hilleman MR. Realities and enigmas of human viral influenza: pathogenesis, epidemiology and control.. Vaccine 2002 Aug 19;20(25-26):3068-87.
    pubmed: 12163258doi: 10.1016/s0264-410x(02)00254-2google scholar: lookup
  6. Gorman OT, Bean WJ, Kawaoka Y, Donatelli I, Guo YJ, Webster RG. Evolution of influenza A virus nucleoprotein genes: implications for the origins of H1N1 human and classical swine viruses.. J Virol 1991 Jul;65(7):3704-14.
    pmc: PMC241390pubmed: 2041090doi: 10.1128/jvi.65.7.3704-3714.1991google scholar: lookup
  7. Ermolaeva MD. Synonymous codon usage in bacteria.. Curr Issues Mol Biol 2001 Oct;3(4):91-7.
    pubmed: 11719972
  8. 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
  9. Sharp PM, Averof M, Lloyd AT, Matassi G, Peden JF. DNA sequence evolution: the sounds of silence.. Philos Trans R Soc Lond B Biol Sci 1995 Sep 29;349(1329):241-7.
    pubmed: 8577834doi: 10.1098/rstb.1995.0108google scholar: lookup
  10. 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
  11. Biro JC. Does codon bias have an evolutionary origin?. Theor Biol Med Model 2008 Jul 30;5:16.
    pmc: PMC2519059pubmed: 18667081doi: 10.1186/1742-4682-5-16google scholar: lookup
  12. Parmley JL, Hurst LD. How do synonymous mutations affect fitness?. Bioessays 2007 Jun;29(6):515-9.
    pubmed: 17508390doi: 10.1002/bies.20592google scholar: lookup
  13. 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
  14. 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
  15. Bulmer M. The selection-mutation-drift theory of synonymous codon usage.. Genetics 1991 Nov;129(3):897-907.
    pmc: PMC1204756pubmed: 1752426doi: 10.1093/genetics/129.3.897google scholar: lookup
  16. Yang Z, Nielsen R. Mutation-selection models of codon substitution and their use to estimate selective strengths on codon usage.. Mol Biol Evol 2008 Mar;25(3):568-79.
    doi: 10.1093/molbev/msm284pubmed: 18178545google scholar: lookup
  17. Kurland CG. Major codon preference: theme and variations.. Biochem Soc Trans 1993 Nov;21(4):841-6.
    pubmed: 8132078doi: 10.1042/bst0210841google scholar: lookup
  18. Smith JM, Smith NH. Site-specific codon bias in bacteria.. Genetics 1996 Mar;142(3):1037-43.
    pmc: PMC1207003pubmed: 8849909doi: 10.1093/genetics/142.3.1037google scholar: lookup
  19. Deschavanne P, Filipski J. Correlation of GC content with replication timing and repair mechanisms in weakly expressed E.coli genes.. Nucleic Acids Res 1995 Apr 25;23(8):1350-3.
    pmc: PMC306860pubmed: 7753625doi: 10.1093/nar/23.8.1350google scholar: lookup
  20. Irwin B, Heck JD, Hatfield GW. Codon pair utilization biases influence translational elongation step times.. J Biol Chem 1995 Sep 29;270(39):22801-6.
    pubmed: 7559409doi: 10.1074/jbc.270.39.22801google scholar: lookup
  21. Karlin S, Mrázek J, Campbell AM. Codon usages in different gene classes of the Escherichia coli genome.. Mol Microbiol 1998 Sep;29(6):1341-55.
    pubmed: 9781873doi: 10.1046/j.1365-2958.1998.01008.xgoogle scholar: lookup
  22. 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.
    pubmed: 15917130doi: 10.1016/j.biosystems.2005.03.002google scholar: lookup
  23. 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
  24. 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
  25. 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
  26. Chen Y. Natural Selection Determines Synonymous Codon Usage Patterns of Neuraminidase (NA) Gene of the Different Subtypes of Influenza A Virus in Canada. J Viruses 2014; 2014.
    doi: 10.1155/2014/329049google scholar: lookup
  27. 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.
    pmc: PMC1642607pubmed: 16987977doi: 10.1128/jvi.01414-06google scholar: lookup
  28. Greenbaum BD, Levine AJ, Bhanot G, Rabadan R. Patterns of evolution and host gene mimicry in influenza and other RNA viruses.. PLoS Pathog 2008 Jun 6;4(6):e1000079.
    doi: 10.1371/journal.ppat.1000079pmc: PMC2390760pubmed: 18535658google scholar: lookup
  29. Solovyov A, Greenbaum B, Palacios G, Lipkin WI, Rabadan R. Host Dependent Evolutionary Patterns and the Origin of 2009 H1N1 Pandemic Influenza.. PLoS Curr 2010 Jan 29;2:RRN1147.
    pmc: PMC2814059pubmed: 20126278doi: 10.1371/currents.rrn1147google scholar: lookup
  30. 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.
    doi: 10.1007/s11262-013-0935-xpubmed: 23780220google scholar: lookup
  31. 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.
    pmc: PMC311793pubmed: 3534792doi: 10.1093/nar/14.19.7737google scholar: lookup
  32. Karlin S, Burge C. Dinucleotide relative abundance extremes: a genomic signature.. Trends Genet 1995 Jul;11(7):283-90.
    pubmed: 7482779doi: 10.1016/s0168-9525(00)89076-9google scholar: lookup
  33. Greenbaum BD, Cocco S, Levine AJ, Monasson R. Quantitative theory of entropic forces acting on constrained nucleotide sequences applied to viruses.. Proc Natl Acad Sci U S A 2014 Apr 1;111(13):5054-9.
    doi: 10.1073/pnas.1402285111pmc: PMC3977288pubmed: 24639520google scholar: lookup
  34. Wright F. The 'effective number of codons' used in a gene.. Gene 1990 Mar 1;87(1):23-9.
    pubmed: 2110097doi: 10.1016/0378-1119(90)90491-9google scholar: lookup
  35. Comeron JM, Aguadé M. An evaluation of measures of synonymous codon usage bias.. J Mol Evol 1998 Sep;47(3):268-74.
    pubmed: 9732453doi: 10.1007/pl00006384google scholar: lookup
  36. Sueoka N. Directional mutation pressure and neutral molecular evolution.. Proc Natl Acad Sci U S A 1988 Apr;85(8):2653-7.
    pmc: PMC280056pubmed: 3357886doi: 10.1073/pnas.85.8.2653google scholar: lookup
  37. Sharp PM, Li WH. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications.. Nucleic Acids Res 1987 Feb 11;15(3):1281-95.
    pmc: PMC340524pubmed: 3547335doi: 10.1093/nar/15.3.1281google scholar: lookup
  38. 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.
    pubmed: 7108955doi: 10.1016/0022-2836(82)90515-0google scholar: lookup
  39. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees.. Mol Biol Evol 1987 Jul;4(4):406-25.
    pubmed: 3447015doi: 10.1093/oxfordjournals.molbev.a040454google scholar: lookup
  40. 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
  41. Greenacre M. (1984) Theory and applications of correspondence analysis. London: Academic; 1984.
  42. Peden JF. Analysis of Codon Usage [dissertation]. Department of Genetics: Nottingham University; 1999.
  43. 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.
    pubmed: 15059815doi: 10.1093/bioinformatics/bth238google scholar: lookup
  44. 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.
    pmc: PMC102460pubmed: 10592250doi: 10.1093/nar/28.1.292google scholar: lookup
  45. Puigbò P, Bravo IG, Garcia-Vallve S. CAIcal: a combined set of tools to assess codon usage adaptation.. Biol Direct 2008 Sep 16;3:38.
    doi: 10.1186/1745-6150-3-38pmc: PMC2553769pubmed: 18796141google scholar: lookup
  46. 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
  47. Karlin S, Doerfler W, Cardon LR. Why is CpG suppressed in the genomes of virtually all small eukaryotic viruses but not in those of large eukaryotic viruses?. J Virol 1994 May;68(5):2889-97.
    pmc: PMC236777pubmed: 8151759doi: 10.1128/jvi.68.5.2889-2897.1994google scholar: lookup
  48. 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
  49. Greenbaum BD, Rabadan R, Levine AJ. Patterns of oligonucleotide sequences in viral and host cell RNA identify mediators of the host innate immune system.. PLoS One 2009 Jun 18;4(6):e5969.
    pmc: PMC2694999pubmed: 19536338doi: 10.1371/journal.pone.0005969google scholar: lookup
  50. Jimenez-Baranda S, Greenbaum B, Manches O, Handler J, Rabadán R, Levine A, Bhardwaj N. Oligonucleotide motifs that disappear during the evolution of influenza virus in humans increase alpha interferon secretion by plasmacytoid dendritic cells.. J Virol 2011 Apr;85(8):3893-904.
    doi: 10.1128/JVI.01908-10pmc: PMC3126114pubmed: 21307198google scholar: lookup
  51. Dorn A, Kippenberger S. Clinical application of CpG-, non-CpG-, and antisense oligodeoxynucleotides as immunomodulators.. Curr Opin Mol Ther 2008 Feb;10(1):10-20.
    pubmed: 18228177
  52. Rothberg PG, Wimmer E. Mononucleotide and dinucleotide frequencies, and codon usage in poliovirion RNA.. Nucleic Acids Res 1981 Dec 11;9(23):6221-9.
    pmc: PMC327599pubmed: 6275352doi: 10.1093/nar/9.23.6221google scholar: lookup
  53. Gómez MM, Tort LF, Volotao Ede M, Recarey R, Moratorio G, Musto H, Leite JP, Cristina J. Analysis of human P[4]G2 rotavirus strains isolated in Brazil reveals codon usage bias and strong compositional constraints.. Infect Genet Evol 2011 Apr;11(3):580-6.
    pmc: PMC7172681pubmed: 21255687doi: 10.1016/j.meegid.2011.01.006google scholar: lookup
  54. Vetsigian K, Goldenfeld N. Genome rhetoric and the emergence of compositional bias.. Proc Natl Acad Sci U S A 2009 Jan 6;106(1):215-20.
    doi: 10.1073/pnas.0810122106pmc: PMC2629207pubmed: 19116280google scholar: lookup
  55. Bisbal C, Silverman RH. Diverse functions of RNase L and implications in pathology.. Biochimie 2007 Jun-Jul;89(6-7):789-98.
    pmc: PMC2706398pubmed: 17400356doi: 10.1016/j.biochi.2007.02.006google scholar: lookup
  56. Scherbik SV, Paranjape JM, Stockman BM, Silverman RH, Brinton MA. RNase L plays a role in the antiviral response to West Nile virus.. J Virol 2006 Mar;80(6):2987-99.
    pmc: PMC1395436pubmed: 16501108doi: 10.1128/jvi.80.6.2987-2999.2006google scholar: lookup
  57. Cooper DA, Banerjee S, Chakrabarti A, García-Sastre A, Hesselberth JR, Silverman RH, Barton DJ. RNase L targets distinct sites in influenza A virus RNAs.. J Virol 2015 Mar;89(5):2764-76.
    doi: 10.1128/JVI.02953-14pmc: PMC4325751pubmed: 25540362google scholar: lookup
  58. Karlin S, Mrázek J. Compositional differences within and between eukaryotic genomes.. Proc Natl Acad Sci U S A 1997 Sep 16;94(19):10227-32.
    pmc: PMC23344pubmed: 9294192doi: 10.1073/pnas.94.19.10227google scholar: lookup
  59. Bird AP. DNA methylation and the frequency of CpG in animal DNA.. Nucleic Acids Res 1980 Apr 11;8(7):1499-504.
    pmc: PMC324012pubmed: 6253938doi: 10.1093/nar/8.7.1499google scholar: lookup
  60. Butt AM, Nasrullah I, Tong Y. Genome-wide analysis of codon usage and influencing factors in chikungunya viruses.. PLoS One 2014;9(3):e90905.
    doi: 10.1371/journal.pone.0090905pmc: PMC3942501pubmed: 24595095google scholar: lookup
  61. 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.
    pmc: PMC7089325pubmed: 17768673doi: 10.1007/s11262-007-0159-zgoogle scholar: lookup
  62. 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
  63. Wang M, Zhang J, Zhou JH, Chen HT, Ma LN, Ding YZ, Liu WQ, Liu YS. Analysis of codon usage in bovine viral diarrhea virus.. Arch Virol 2011 Jan;156(1):153-60.
    doi: 10.1007/s00705-010-0848-0pmc: PMC7087306pubmed: 21069395google scholar: lookup
  64. 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
  65. Moratorio G, Iriarte A, Moreno P, Musto H, Cristina J. A detailed comparative analysis on the overall codon usage patterns in West Nile virus.. Infect Genet Evol 2013 Mar;14:396-400.
    doi: 10.1016/j.meegid.2013.01.001pubmed: 23333335google scholar: lookup
  66. Adams MJ, Antoniw JF. Codon usage bias amongst plant viruses.. Arch Virol 2004 Jan;149(1):113-35.
    pubmed: 14689279doi: 10.1007/s00705-003-0186-6google scholar: lookup
  67. Fu M. Codon usage bias in herpesvirus.. Arch Virol 2010 Mar;155(3):391-6.
    doi: 10.1007/s00705-010-0597-0pubmed: 20107845google scholar: lookup
  68. Zhao KN, Liu WJ, Frazer IH. Codon usage bias and A+T content variation in human papillomavirus genomes.. Virus Res 2003 Dec;98(2):95-104.
    pubmed: 14659556doi: 10.1016/j.virusres.2003.08.019google scholar: lookup
  69. Zhang Y, Liu Y, Liu W, Zhou J, Chen H, Wang Y, Ma L, Ding Y, Zhang J. Analysis of synonymous codon usage in hepatitis A virus.. Virol J 2011 Apr 16;8:174.
    doi: 10.1186/1743-422X-8-174pmc: PMC3087699pubmed: 21496278google scholar: lookup
  70. Skinner JA, Zurawski SM, Sugimoto C, Vinet-Oliphant H, Vinod P, Xue Y, Russell-Lodrigue K, Albrecht RA, García-Sastre A, Salazar AM, Roy CJ, Kuroda MJ, Oh S, Zurawski G. Immunologic characterization of a rhesus macaque H1N1 challenge model for candidate influenza virus vaccine assessment.. Clin Vaccine Immunol 2014 Dec;21(12):1668-80.
    doi: 10.1128/CVI.00547-14pmc: PMC4248778pubmed: 25298110google scholar: lookup
  71. Carroll TD, Matzinger SR, Barry PA, McChesney MB, Fairman J, Miller CJ. Efficacy of influenza vaccination of elderly rhesus macaques is dramatically improved by addition of a cationic lipid/DNA adjuvant.. J Infect Dis 2014 Jan 1;209(1):24-33.
    doi: 10.1093/infdis/jit540pmc: PMC3864389pubmed: 24141979google scholar: lookup
  72. Kitano M, Itoh Y, Kodama M, Ishigaki H, Nakayama M, Nagata T, Ishida H, Tsuchiya H, Torii R, Baba K, Yoshida R, Sato A, Ogasawara K. Establishment of a cynomolgus macaque model of influenza B virus infection.. Virology 2010 Nov 25;407(2):178-84.
    doi: 10.1016/j.virol.2010.08.006pubmed: 20822788google scholar: lookup
  73. Karlsson EA, Engel GA, Feeroz MM, San S, Rompis A, Lee BP, Shaw E, Oh G, Schillaci MA, Grant R, Heidrich J, Schultz-Cherry S, Jones-Engel L. Influenza virus infection in nonhuman primates.. Emerg Infect Dis 2012 Oct;18(10):1672-5.
    doi: 10.3201/eid1810.120214pmc: PMC3471624pubmed: 23017256google scholar: lookup
  74. 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.
    pubmed: 16186182doi: 10.1126/science.1117950google scholar: lookup
  75. Feng KH, Gonzalez G, Deng L, Yu H, Tse VL, Huang L, Huang K, Wasik BR, Zhou B, Wentworth DE, Holmes EC, Chen X, Varki A, Murcia PR, Parrish CR. Equine and Canine Influenza H3N8 Viruses Show Minimal Biological Differences Despite Phylogenetic Divergence.. J Virol 2015 Jul;89(13):6860-73.
    doi: 10.1128/JVI.00521-15pmc: PMC4468500pubmed: 25903329google scholar: lookup
  76. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms.. Mol Biol Evol 1985 Jan;2(1):13-34.
    pubmed: 3916708doi: 10.1093/oxfordjournals.molbev.a040335google scholar: lookup
  77. 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
  78. Romero H, Zavala A, Musto H, Bernardi G. The influence of translational selection on codon usage in fishes from the family Cyprinidae.. Gene 2003 Oct 23;317(1-2):141-7.
    pubmed: 14604802doi: 10.1016/s0378-1119(03)00701-7google scholar: lookup
  79. Vider-Shalit T, Fishbain V, Raffaeli S, Louzoun Y. Phase-dependent immune evasion of herpesviruses.. J Virol 2007 Sep;81(17):9536-45.
    pmc: PMC1951411pubmed: 17609281doi: 10.1128/jvi.02636-06google scholar: lookup
  80. Guo Y, Wang M, Kawaoka Y, Gorman O, Ito T, Saito T, Webster RG. Characterization of a new avian-like influenza A virus from horses in China.. Virology 1992 May;188(1):245-55.
    pubmed: 1314452doi: 10.1016/0042-6822(92)90754-dgoogle scholar: lookup
  81. 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
  82. Eigen M. From Strange Simplicity to Complex familiarity: A Treatise on Matter, Information, Life and Thought. 1st ed Oxford: Oxford University Press; 2013.
  83. Eigen M. Selforganization of matter and the evolution of biological macromolecules.. Naturwissenschaften 1971 Oct;58(10):465-523.
    pubmed: 4942363doi: 10.1007/bf00623322google scholar: lookup

Citations

This article has been cited 57 times.
  1. Noor F, Ashfaq UA, Bakar A, Qasim M, Masoud MS, Alshammari A, Alharbi M, Riaz MS. Identification and characterization of codon usage pattern and influencing factors in HFRS-causing hantaviruses. Front Immunol 2023;14:1131647.
    doi: 10.3389/fimmu.2023.1131647pubmed: 37492567google scholar: lookup
  2. Fisher M, Nebroski M, Davies J, Janzen E, Sullivan D, Lung O. Discovery and comparative genomic analysis of a novel equine anellovirus, representing the first complete Mutorquevirus genome. Sci Rep 2023 Mar 6;13(1):3703.
    doi: 10.1038/s41598-023-30875-7pubmed: 36878942google scholar: lookup
  3. Rahman SU, Rehman HU, Rahman IU, Khan MA, Rahim F, Ali H, Chen D, Ma W. Evolution of codon usage in Taenia saginata genomes and its impact on the host. Front Vet Sci 2022;9:1021440.
    doi: 10.3389/fvets.2022.1021440pubmed: 36713873google scholar: lookup
  4. Rahman SU, Rehman HU, Rahman IU, Rauf A, Alshammari A, Alharbi M, Haq NU, Suleria HAR, Raza SHA. Analysis of codon usage bias of lumpy skin disease virus causing livestock infection. Front Vet Sci 2022;9:1071097.
    doi: 10.3389/fvets.2022.1071097pubmed: 36544551google scholar: lookup
  5. Wang Q, Lyu X, Cheng J, Fu Y, Lin Y, Abdoulaye AH, Jiang D, Xie J. Codon Usage Provides Insights into the Adaptive Evolution of Mycoviruses in Their Associated Fungi Host. Int J Mol Sci 2022 Jul 4;23(13).
    doi: 10.3390/ijms23137441pubmed: 35806445google scholar: lookup
  6. He Z, Ding S, Guo J, Qin L, Xu X. Synonymous Codon Usage Analysis of Three Narcissus Potyviruses. Viruses 2022 Apr 19;14(5).
    doi: 10.3390/v14050846pubmed: 35632588google scholar: lookup
  7. Nair RR, Mohan M, Rudramurthy GR, Vivekanandam R, Satheshkumar PS. Strategies and Patterns of Codon Bias in Molluscum Contagiosum Virus. Pathogens 2021 Dec 20;10(12).
    doi: 10.3390/pathogens10121649pubmed: 34959603google scholar: lookup
  8. Amat JAR, Patton V, Chauché C, Goldfarb D, Crispell J, Gu Q, Coburn AM, Gonzalez G, Mair D, Tong L, Martinez-Sobrido L, Marshall JF, Marchesi F, Murcia PR. Long-term adaptation following influenza A virus host shifts results in increased within-host viral fitness due to higher replication rates, broader dissemination within the respiratory epithelium and reduced tissue damage. PLoS Pathog 2021 Dec;17(12):e1010174.
    doi: 10.1371/journal.ppat.1010174pubmed: 34919598google scholar: lookup
  9. Si F, Jiang L, Yu R, Wei W, Li Z. Study on the Characteristic Codon Usage Pattern in Porcine Epidemic Diarrhea Virus Genomes and Its Host Adaptation Phenotype. Front Microbiol 2021;12:738082.
    doi: 10.3389/fmicb.2021.738082pubmed: 34733253google scholar: lookup
  10. Kumar N, Kaushik R, Tennakoon C, Uversky VN, Mishra A, Sood R, Srivastava P, Tripathi M, Zhang KYJ, Bhatia S. Evolutionary Signatures Governing the Codon Usage Bias in Coronaviruses and Their Implications for Viruses Infecting Various Bat Species. Viruses 2021 Sep 16;13(9).
    doi: 10.3390/v13091847pubmed: 34578428google scholar: lookup
  11. 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
  12. Gaunt ER, Digard P. Compositional biases in RNA viruses: Causes, consequences and applications. Wiley Interdiscip Rev RNA 2022 Mar;13(2):e1679.
    doi: 10.1002/wrna.1679pubmed: 34155814google scholar: lookup
  13. Wu W, Ge X, Zhang Y, Han J, Guo X, Zhou L, Yang H. Evolutionary Patterns of Codon Usage in Major Lineages of Porcine Reproductive and Respiratory Syndrome Virus in China. Viruses 2021 May 31;13(6).
    doi: 10.3390/v13061044pubmed: 34072978google scholar: lookup
  14. Franzo G, Tucciarone CM, Legnardi M, Cecchinato M. Effect of genome composition and codon bias on infectious bronchitis virus evolution and adaptation to target tissues. BMC Genomics 2021 Apr 7;22(1):244.
    doi: 10.1186/s12864-021-07559-5pubmed: 33827429google scholar: lookup
  15. Saha J, Bhattacharjee S, Pal Sarkar M, Saha BK, Basak HK, Adhikary S, Roy V, Mandal P, Chatterjee A, Pal A. A comparative genomics-based study of positive strand RNA viruses emphasizing on SARS-CoV-2 utilizing dinucleotide signature, codon usage and codon context analyses. Gene Rep 2021 Jun;23:101055.
    doi: 10.1016/j.genrep.2021.101055pubmed: 33615042google scholar: lookup
  16. Luo W, Roy A, Guo F, Irwin DM, Shen X, Pan J, Shen Y. Host Adaptation and Evolutionary Analysis of Zaire ebolavirus: Insights From Codon Usage Based Investigations. Front Microbiol 2020;11:570131.
    doi: 10.3389/fmicb.2020.570131pubmed: 33224111google scholar: lookup
  17. 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
  18. Wu H, Bao Z, Mou C, Chen Z, Zhao J. Comprehensive Analysis of Codon Usage on Porcine Astrovirus. Viruses 2020 Sep 6;12(9).
    doi: 10.3390/v12090991pubmed: 32899965google scholar: lookup
  19. 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
  20. Yao X, Fan Q, Yao B, Lu P, Rahman SU, Chen D, Tao S. Codon Usage Bias Analysis of Bluetongue Virus Causing Livestock Infection. Front Microbiol 2020;11:655.
    doi: 10.3389/fmicb.2020.00655pubmed: 32508755google scholar: lookup
  21. Gu H, Chu DKW, Peiris M, Poon LLM. Multivariate analyses of codon usage of SARS-CoV-2 and other betacoronaviruses. Virus Evol 2020 Jan;6(1):veaa032.
    doi: 10.1093/ve/veaa032pubmed: 32431949google scholar: lookup
  22. Deb B, Uddin A, Chakraborty S. Codon usage pattern and its influencing factors in different genomes of hepadnaviruses. Arch Virol 2020 Mar;165(3):557-570.
    doi: 10.1007/s00705-020-04533-6pubmed: 32036428google scholar: lookup
  23. Sheikh A, Al-Taher A, Al-Nazawi M, Al-Mubarak AI, Kandeel M. Analysis of preferred codon usage in the coronavirus N genes and their implications for genome evolution and vaccine design. J Virol Methods 2020 Mar;277:113806.
    doi: 10.1016/j.jviromet.2019.113806pubmed: 31911390google scholar: lookup
  24. He W, Wang N, Tan J, Wang R, Yang Y, Li G, Guan H, Zheng Y, Shi X, Ye R, Su S, Zhou J. Comprehensive codon usage analysis of porcine deltacoronavirus. Mol Phylogenet Evol 2019 Dec;141:106618.
    doi: 10.1016/j.ympev.2019.106618pubmed: 31536759google scholar: lookup
  25. Yao H, Chen M, Tang Z. Analysis of Synonymous Codon Usage Bias in Flaviviridae Virus. Biomed Res Int 2019;2019:5857285.
    doi: 10.1155/2019/5857285pubmed: 31346520google scholar: lookup
  26. Li G, Zhang W, Wang R, Xing G, Wang S, Ji X, Wang N, Su S, Zhou J. Genetic Analysis and Evolutionary Changes of the Torque teno sus Virus. Int J Mol Sci 2019 Jun 13;20(12).
    doi: 10.3390/ijms20122881pubmed: 31200479google scholar: lookup
  27. Khandia R, Singhal S, Kumar U, Ansari A, Tiwari R, Dhama K, Das J, Munjal A, Singh RK. Analysis of Nipah Virus Codon Usage and Adaptation to Hosts. Front Microbiol 2019;10:886.
    doi: 10.3389/fmicb.2019.00886pubmed: 31156564google scholar: lookup
  28. Biswas KK, Palchoudhury S, Chakraborty P, Bhattacharyya UK, Ghosh DK, Debnath P, Ramadugu C, Keremane ML, Khetarpal RK, Lee RF. Codon Usage Bias Analysis of Citrus tristeza Virus: Higher Codon Adaptation to Citrus reticulata Host. Viruses 2019 Apr 8;11(4).
    doi: 10.3390/v11040331pubmed: 30965565google scholar: lookup
  29. Blanco-Lobo P, Nogales A, Rodríguez L, Martínez-Sobrido L. Novel Approaches for The Development of Live Attenuated Influenza Vaccines. Viruses 2019 Feb 22;11(2).
    doi: 10.3390/v11020190pubmed: 30813325google scholar: lookup
  30. Gumpper RH, Li W, Luo M. Constraints of Viral RNA Synthesis on Codon Usage of Negative-Strand RNA Virus. J Virol 2019 Mar 1;93(5).
    doi: 10.1128/JVI.01775-18pubmed: 30541832google scholar: lookup
  31. Yan Z, Wang R, Zhang L, Shen B, Wang N, Xu Q, He W, He W, Li G, Su S. Evolutionary changes of the novel Influenza D virus hemagglutinin-esterase fusion gene revealed by the codon usage pattern. Virulence 2019 Dec;10(1):1-9.
    doi: 10.1080/21505594.2018.1551708pubmed: 30475085google scholar: lookup
  32. 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
  33. Singh RK, Dhama K, Karthik K, Khandia R, Munjal A, Khurana SK, Chakraborty S, Malik YS, Virmani N, Singh R, Tripathi BN, Munir M, van der Kolk JH. A Comprehensive Review on Equine Influenza Virus: Etiology, Epidemiology, Pathobiology, Advances in Developing Diagnostics, Vaccines, and Control Strategies. Front Microbiol 2018;9:1941.
    doi: 10.3389/fmicb.2018.01941pubmed: 30237788google scholar: lookup
  34. 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
  35. 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
  36. Franzo G, Segales J, Tucciarone CM, Cecchinato M, Drigo M. The analysis of genome composition and codon bias reveals distinctive patterns between avian and mammalian circoviruses which suggest a potential recombinant origin for Porcine circovirus 3. PLoS One 2018;13(6):e0199950.
    doi: 10.1371/journal.pone.0199950pubmed: 29958294google scholar: lookup
  37. Wang H, Meng T, Wei W. Analysis of synonymous codon usage bias in helicase gene from Autographa californica multiple nucleopolyhedrovirus. Genes Genomics 2018 Jul;40(7):767-780.
    doi: 10.1007/s13258-018-0689-xpubmed: 29934813google scholar: lookup
  38. Tian L, Shen X, Murphy RW, Shen Y. The adaptation of codon usage of +ssRNA viruses to their hosts. Infect Genet Evol 2018 Sep;63:175-179.
    doi: 10.1016/j.meegid.2018.05.034pubmed: 29864509google scholar: lookup
  39. 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
  40. Chen Y, Xu Q, Tan C, Li X, Chi X, Cai B, Yu Z, Ma Y, Chen JL. Genomic analysis of codon usage shows influence of mutation pressure, natural selection, and host features on Senecavirus A evolution. Microb Pathog 2017 Nov;112:313-319.
    doi: 10.1016/j.micpath.2017.09.040pubmed: 28943149google scholar: lookup
  41. Chen Y, Li X, Chi X, Wang S, Ma Y, Chen J. Comprehensive analysis of the codon usage patterns in the envelope glycoprotein E2 gene of the classical swine fever virus. PLoS One 2017;12(9):e0183646.
    doi: 10.1371/journal.pone.0183646pubmed: 28880881google scholar: lookup
  42. Bera BC, Virmani N, Kumar N, Anand T, Pavulraj S, Rash A, Elton D, Rash N, Bhatia S, Sood R, Singh RK, Tripathi BN. Genetic and codon usage bias analyses of polymerase genes of equine influenza virus and its relation to evolution. BMC Genomics 2017 Aug 23;18(1):652.
    doi: 10.1186/s12864-017-4063-1pubmed: 28830350google scholar: lookup
  43. Patil AB, Dalvi VS, Mishra AA, Krishna B, Azeez A. Analysis of synonymous codon usage bias and phylogeny of coat protein gene in banana bract mosaic virus isolates. Virusdisease 2017 Jun;28(2):156-163.
    doi: 10.1007/s13337-017-0380-xpubmed: 28770241google scholar: lookup
  44. Wang H, Liu S, Zhang B, Wei W. Analysis of Synonymous Codon Usage Bias of Zika Virus and Its Adaption to the Hosts. PLoS One 2016;11(11):e0166260.
    doi: 10.1371/journal.pone.0166260pubmed: 27893824google scholar: lookup
  45. Wang Y, Wang Z, Kou Z, Pang B, Wen H. Dissecting the evolutionary forces shaping codon usage bias in SFTSV from eastern China: Insights from a previously underrepresented region. Virulence 2026 Dec 31;17(1):2621490.
    doi: 10.1080/21505594.2026.2621490pubmed: 41571581google scholar: lookup
  46. Khatoon H, Chavan DD, Meena VK, Kashyap AS, Sathiyaseelan K, Elangovan M, Patil L, Meena BR, Gauns A, Bhattacharyya UK, Biswas KK. Differentiation and validation of mild and severe strains of citrus tristeza virus through codon usage bias, host adaptation, and biochemical profiling. Front Microbiol 2025;16:1665893.
    doi: 10.3389/fmicb.2025.1665893pubmed: 41103763google scholar: lookup
  47. Zhou Y, Sheng Z, Li D, Li W, Peng Y, Song Z, Quan Z, Liu Y. Codon usage bias is presumably affected by tRNA selection effects in Actinidia polyploidization events. BMC Genomics 2025 Jul 23;26(1):685.
    doi: 10.1186/s12864-025-11873-7pubmed: 40702430google scholar: lookup
  48. Chen L, Jiang W, Wu W, Zhang S, Cai J, Lv T, Xiang B, Lin Q, Liao M, Ding C, Ren T. Insights into the Epidemiology, Phylodynamics, and Evolutionary Changes of Lineage GI-7 Infectious Bronchitis Virus. Transbound Emerg Dis 2023;2023:9520616.
    doi: 10.1155/2023/9520616pubmed: 40303710google scholar: lookup
  49. Branda F, Yon DK, Albanese M, Binetti E, Giovanetti M, Ciccozzi A, Ciccozzi M, Scarpa F, Ceccarelli G. Equine Influenza: Epidemiology, Pathogenesis, and Strategies for Prevention and Control. Viruses 2025 Feb 21;17(3).
    doi: 10.3390/v17030302pubmed: 40143233google scholar: lookup
  50. Tan X, Zhou W, Jing S, Shen W, Lu B. Decoding codon usage in human papillomavirus type 59. Virus Genes 2025 Jun;61(3):313-323.
    doi: 10.1007/s11262-025-02148-0pubmed: 40038214google scholar: lookup
  51. 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
  52. Tan X, Bao S, Lu X, Lu B, Shen W, Jiang C. Comprehensive Analysis of Codon Usage Bias in Human Papillomavirus Type 51. Pol J Microbiol 2024 Dec 1;73(4):455-465.
    doi: 10.33073/pjm-2024-036pubmed: 39465910google scholar: lookup
  53. Li L, Li X, Liu Y, Li J, Zhen X, Huang Y, Ye J, Fan L. Comparative analysis of the complete mitogenomes of Camellia sinensis var. sinensis and C. sinensis var. assamica provide insights into evolution and phylogeny relationship. Front Plant Sci 2024;15:1396389.
    doi: 10.3389/fpls.2024.1396389pubmed: 39239196google scholar: lookup
  54. Castellano LA, McNamara RJ, Pallarés HM, Gamarnik AV, Alvarez DE, Bazzini AA. Dengue virus preferentially uses human and mosquito non-optimal codons. Mol Syst Biol 2024 Oct;20(10):1085-1108.
    doi: 10.1038/s44320-024-00052-7pubmed: 39039212google scholar: lookup
  55. Kaushik R, Kumar N, Yadav P, Sircar S, Shete-Aich A, Singh A, Tomar S, Launey T, Malik YS. Comprehensive Genomics Investigation of Neboviruses Reveals Distinct Codon Usage Patterns and Host Specificity. Microorganisms 2024 Mar 29;12(4).
    doi: 10.3390/microorganisms12040696pubmed: 38674640google scholar: lookup
  56. Li Y, Arcos S, Sabsay KR, Te Velthuis AJW, Lauring AS. Deep mutational scanning reveals the functional constraints and evolutionary potential of the influenza A virus PB1 protein. J Virol 2023 Nov 30;97(11):e0132923.
    doi: 10.1128/jvi.01329-23pubmed: 37882522google scholar: lookup
  57. 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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