Exploring Codon Usage Patterns and Influencing Factors in Ranavirus DNA Polymerase Genes.

DNA polymerase codon usage bias mutation pressure natural selection ranavirus

Journal

Journal of basic microbiology
ISSN: 1521-4028
Titre abrégé: J Basic Microbiol
Pays: Germany
ID NLM: 8503885

Informations de publication

Date de publication:
04 Aug 2024
Historique:
revised: 05 07 2024
received: 17 05 2024
accepted: 20 07 2024
medline: 5 8 2024
pubmed: 5 8 2024
entrez: 5 8 2024
Statut: aheadofprint

Résumé

Ranaviruses, members of the genus Ranavirus within the family Iridoviridae, have become a significant concern for amphibian populations globally, along with other cold-blooded vertebrates, due to their emergence as a significant threat. We employed bioinformatics tools to examine the codon usage patterns in 61 DNA pol genes from Ranavirus, Lymphocystivirus, Megalocytivirus, and two unclassified ranaviruses, as no prior studies had been conducted on this topic. The results showed a slight or low level of codon usage bias (CUB) in the DNA pol genes of Ranavirus. Relative synonymous codon usage (RSCU) analysis indicated that the predominant codons favored in Ranavirus DNA pol genes terminate with C or G. Correlation analysis examining nucleotide content, third codon position, effective number of codons (ENC), correspondence analysis (COA), Aroma values, and GRAVY values indicated that the CUB across DNA pol genes could be influenced by both mutation pressure and natural selection. The neutrality plot indicated that natural selection is the primary factor driving codon usage. Furthermore, the analysis of the codon adaptation index (CAI) illustrated the robust adaptability of Ranavirus DNA pol genes to their hosts. Analysis of the relative codon deoptimization index (RCDI) suggested that Ranavirus DNA pol genes underwent greater selection pressure from their hosts. These findings will aid in comprehending the factors influencing the evolution and adaptation of Ranavirus to its hosts.

Identifiants

pubmed: 39099168
doi: 10.1002/jobm.202400289
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2400289

Informations de copyright

© 2024 Wiley‐VCH GmbH.

Références

V. G. Chinchar, P. Hick, I. A. Ince, et al., “ICTV Virus Taxonomy Profile: Iridoviridae,” Journal of General Virology 98 (2017): 890–891.
V. G. Chinchar and A. L. J. Duffus, “Molecular and Ecological Studies of a Virus Family (Iridoviridae) Infecting Invertebrates and Ectothermic Vertebrates,” Viruses 11 (2019): 538.
A. L. J. Duffus, T. B. Waltzek and A. C. Stohr, et al., “Distribution and Host Range of Ranaviruses,” in Ranaviruses, eds. M. Gray and V. Chinchar (Cham: Springer, 2015), 9–57.
V. G. Chinchar and A. Granoff, “Isolation and Characterization of a Frog Virus 3 Variant Resistant to Phosphonoacetate: Genetic Evidence for a Virus‐Specific DNA Polymerase,” Virology 138 (1984): 357–361.
X. Y. Lei, T. Ou, R. L. Zhu, and Q. Y. Zhang, “Sequencing and Analysis of the Complete Genome of Rana Grylio Virus (RGV),” Archives of Virology 157 (2012): 1559–1564.
E. A. Morrison, S. Garner, P. Echaubard, D. Lesbarrères, C. J. Kyle, and C. R. Brunetti, “Complete Genome Analysis of a Frog Virus 3 (FV3) Isolate and Sequence Comparison With Isolates of Differing Levels of Virulence,” Virology Journal 11 (2014): 46.
R. Zhao, C. Gu, X. Zou, et al., “Comparative Genomic Analysis Reveals New Evidence of Genus Boundary for Family Iridoviridae and Explores Qualified Hallmark Genes,” Computational and Structural Biotechnology Journal 20 (2022): 3493–3502.
H. E. Eaton, J. Metcalf, E. Penny, V. Tcherepanov, C. Upton, and C. R. Brunetti, “Comparative Genomic Analysis of the Family Iridoviridae: Re‐Annotating and Defining the Core Set of Iridovirus Genes,” Virology Journal 4 (2007): 11.
K. H. Choi, “Viral Polymerases,” in Viral Molecular Machines, eds. M. Rossmann and V. Rao (Boston: Springer, 2012), 267–304.
J. Morcinek‐Orłowska, K. Zdrojewska, and A. Węgrzyn, “Bacteriophage‐Encoded DNA Polymerases—Beyond the Traditional View of Polymerase Activities,” International Journal of Molecular Sciences 23 (2022): 635.
S. Kausar, F. Said Khan, M. Ishaq Mujeeb Ur Rehman, et al., “A Review: Mechanism of Action of Antiviral Drugs,” International Journal of Immunopathology and Pharmacology 35 (2021): 205873842110026.
Y. Eizuru, “Development of New Antivirals for Herpesviruses,” Antiviral Chemistry and Chemotherapy 14 (2003): 299–308.
J. B. Plotkin and G. Kudla, “Synonymous But Not the Same: The Causes and Consequences of Codon Bias,” Nature Reviews Genetics 12 (2011): 32–42.
H. H. Schalkwijk, A. Georgala, S. Gillemot, et al., “A Herpes Simplex Virus 1 DNA Polymerase Multidrug Resistance Mutation Identified in a Patient With Immunodeficiency and Confirmed By Gene Editing,” Journal of Infectious Diseases 228 (2023): 1505–1515.
E. H. Im and S. S. Choi, “Synonymous Codon Usage Controls Various Molecular Aspects,” Genomics & Informatics 15 (2017): 123–127.
H. Wang, T. Meng, and W. Wei, “Analysis of Synonymous Codon Usage Bias in Helicase Gene From Autographa Californica Multiple Nucleopolyhedrovirus,” Genes & Genomics 40 (2018): 767–780.
M. N. Choudhury, A. Uddin, and S. Chakraborty, “Nucleotide Composition and Codon Usage Bias of SRY Gene,” Andrologia. 50 (2018): e12787.
Q. Li, Y. Luo, A. Sha, et al., “Analysis of Synonymous Codon Usage Patterns in Mitochondrial Genomes of Nine Amanita Species,” Frontiers in Microbiology 14 (2023): 1134228.
A. M. Anwar, M. Soudy, and R. Mohamed, “vhcub: Virus‐Host Codon Usage Co‐Adaptation Analysis,” F1000Research 8 (2020): 1–10.
H. Wang, S. Liu, Y. Lv, and W. Wei, “Codon Usage Bias of Venezuelan Equine Encephalitis Virus and Its Host Adaption,” Virus Research 328 (2023): 199081.
S. Chakraborty, B. Deb, P. A. Barbhuiya, and A. Uddin, “Analysis of Codon Usage Patterns and Influencing Factors in Nipah Virus,” Virus Research 263 (2019): 129–138.
L. Jiang, Q. Zhang, S. Xiao, and F. Si, “Deep Decoding of Codon Usage Strategies and Host Adaption Preferences of Soybean Mosaic Virus,” International Journal of Biological Macromolecules 222 (2022): 803–817.
S. Morla, A. Makhija, and S. Kumar, “Synonymous Codon Usage Pattern in Glycoprotein Gene of Rabies Virus,” Gene 584 (2016): 1–6.
X. Wang, W. Xu, K. Fan, H. Chiu, and C. Huang, “Codon Usage Bias in the H Gene of Canine Distemper Virus,” Microbial Pathogenesis 149 (2020): 104511.
S. U. Rahman, M. Abdullah, A. W. Khan, et al., “A Detailed Comparative Analysis of Codon Usage Bias in Alongshan Virus,” Virus Research 308 (2022): 198646.
J. Cristina, A. Fajardo, M. Soñora, G. Moratorio, and H. Musto, “A Detailed Comparative Analysis of Codon Usage Bias in Zika Virus,” Virus Research 223 (2016): 147–152.
Y. Aktürk Dizman, “Codon Usage Bias Analysis of the Gene Encoding NAD+‐Dependent DNA Ligase Protein of Invertebrate Iridescent Virus 6,” Archives of Microbiology 205 (2023): 352.
H. Tian, Q. Hu, H. Xiao, L. Zeng, Y. Meng, and Z. Li, “Genetic and Codon Usage Bias Analyses of Major Capsid Protein Gene in Ranavirus,” Infection, Genetics and Evolution 84 (2020): 104379.
C. T. Tsai, C. H. Lin, and C. Y. Chang, “Analysis of Codon Usage Bias and Base Compositional Constraints in Iridovirus Genomes,” Virus Research 126 (2007): 196–206.
K. Tamura, G. Stecher, and S. Kumar, “MEGA11: Molecular Evolutionary Genetics Analysis Version 11,” Molecular Biology and Evolution 38 (2021): 3022–3027.
M. Kimura, “A Simple Method for Estimating Evolutionary Rates of Base Substitutions Through Comparative Studies of Nucleotide Sequences,” Journal of Molecular Evolution 16 (1980): 111–120.
Z. Zhang, W. Dai, and D. Dai, “Synonymous Codon Usage in TTSuV2: Analysis and Comparison With TTSuV1,” PLoS One 8 (2013): e81469.
A. M. Butt, I. Nasrullah, and Y. Tong, “Genome‐Wide Analysis of Codon Usage and Influencing Factors in Chikungunya Viruses,” PLoS One 9 (2014): e90905.
P. M. Sharp and W. H. Li, “Codon Usage in Regulatory Genes in Escherichia coli Does Not Reflect Selection for “Rare” Codons,” Nucleic Acids Research 14 (1986): 7737–7749.
H. Feng, J. Segalés, F. Wang, et al., “Comprehensive Analysis of Codon Usage Patterns in Chinese Porcine Circoviruses Based on Their Major Protein‐Coding Sequences,” Viruses 14 (2022): 81.
S. Kariin and C. Burge, “Dinucleotide Relative Abundance Extremes: A Genomic Signature,” Trends in Genetics 11 (1995): 283–290.
Q. Xu, H. Chen, W. Sun, et al., “Genome‐Wide Analysis of the Synonymous Codon Usage Pattern of Streptococcus suis,” Microbial Pathogenesis 150 (2021): 104732.
F. Wright, “The ‘Effective Number of Codons’ Used in a Gene,” Gene 87 (1990): 23–29.
J. M. Comeron and M. Aguadé, “An Evaluation of Measures of Synonymous Codon Usage Bias,” Journal of Molecular Evolution 47 (1998): 268–274.
D. L. Hartl, E. N. Moriyama, and S. A. Sawyer, “Selection Intensity for Codon Bias,” Genetics 138 (1994): 227–234.
A. Fuglsang, “Impact of Bias Discrepancy and Amino Acid Usage on Estimates of the Effective Number of Codons Used in a Gene, and a Test for Selection on Codon Usage,” Gene 410 (2008): 82–88.
N. Sueoka, “Intrastrand Parity Rules of DNA Base Composition and Usage Biases of Synonymous Codons,” Journal of Molecular Evolution 40 (1995): 318–325.
H. Ji, J. Liu, Y. Chen, et al., “Bioinformatic Analysis of Codon Usage Bias of HSP20 Genes in Four Cruciferous Species,” Plants 13 (2024): 468.
Y. Zhao, H. Zheng, A. Xu, et al., “Analysis of Codon Usage Bias of Envelope Glycoprotein Genes in Nuclear Polyhedrosis Virus (NPV) and Its Relation to Evolution,” BMC Genomics 17 (2016): 677.
Z. He, H. Gan, and X. Liang, “Analysis of Synonymous Codon Usage Bias in Potato Virus M and Its Adaption to Hosts,” Viruses 11 (2019): 752.
Y. Chen, X. Li, X. Chi, S. Wang, Y. Ma, and J. Chen, “Comprehensive Analysis of the Codon Usage Patterns in the Envelope Glycoprotein E2 Gene of the Classical Swine Fever Virus,” PLoS One 12 (2017): e0183646.
L. Deng, Y. Geng, R. Zhao, et al., “CMTV‐Like Ranavirus Infection Associated With High Mortality in Captive Catfish‐Like Loach, Triplophysa Siluorides, in China,” Transboundary and Emerging Diseases 67 (2020): 1330–1335.
M. R. George, K. R. John, M. M. Mansoor, R. Saravanakumar, P. Sundar, and V. Pradeep, “Isolation and Characterization of a Ranavirus From Koi, Cyprinus carpio L., Experiencing Mass Mortalities in India,” Journal of Fish Diseases 38 (2015): 389–403.
P. Kayansamruaj, A. Rangsichol, H. T. Dong, et al., “Outbreaks of Ulcerative Disease Associated With Ranavirus Infection in Barcoo Grunter, Scortum barcoo (Mcculloch & Waite),” Journal of Fish Diseases 40 (2017): 1341–1350.
M. Kik, A. Martel, A. S. Sluijs, et al., “Ranavirus‐Associated Mass Mortality in Wild Amphibians, The Netherlands, 2010: A First Report,” Veterinary Journal 190 (2011): 284–286.
A. M. Hartmann, M. L. Maddox, R. J. Ossiboff, and A. V. Longo, “Sustained Ranavirus Outbreak Causes Mass Mortality and Morbidity of Imperiled Amphibians in Florida,” Ecohealth 19 (2022): 8–14.
R. M. Goodman, H. R. Carman, R. P. Mahaffy, and N. S. Cabrera, “Trace Amounts of Ranavirus Detected in Common Musk Turtles (Sternotherus odoratus) at a Site Where the Pathogen Was Previously Common,” Animals 13 (2023): 2951.
K. Tamukai, T. Tokiwa, H. Kobayashi, and Y. Une, “Ranavirus in an Outbreak of Dermatophilosis in Captive Inland Bearded Dragons (Pogona vitticeps),” Veterinary Dermatology 27 (2016): 99–e28.
R. Holopainen, S. Ohlemeyer, H. Schütze, S. Bergmann, and H. Tapiovaara, “Ranavirus Phylogeny and Differentiation Based on Major Capsid Protein, DNA Polymerase and Neurofilament Triplet H1‐Like Protein Genes,” Diseases of Aquatic Organisms 85 (2009): 81–91.
J. Herath, D. Sun, G. Ellepola, K. Subramaniam, and M. Meegaskumbura, “Emerging Threat of Ranavirus: Prevalence, Genetic Diversity, and Climatic Drivers of Ranavirus (Iridoviridae) in Ectothermic Vertebrates of Asia,” Frontiers in Veterinary Science 10 (2023): 1–13.
X. Yu, K. Gao, M. Pi, et al., “Phylogenetic and Codon Usage Analysis for Replicase and Capsid Genes of Porcine Circovirus 3,” Veterinary Research Communications 45 (2021): 353–361.
B. Deb, A. Uddin, and S. Chakraborty, “Composition, Codon Usage Pattern, Protein Properties, and Influencing Factors in the Genomes of Members of the Family Anelloviridae,” Archives of Virology 166 (2021): 461–474.
Y. Aktürk Dizman, “Analysis of Codon Usage Bias of Exonuclease Genes in Invertebrate Iridescent Viruses,” Virology 593 (2024): 110030.
S. U. Rahman, H. U. Rehman, I. U. Rahman, et al., “Analysis of Codon Usage Bias of Lumpy Skin Disease Virus Causing Livestock Infection,” Frontiers in Veterinary Science 9 (2022): 1071097.
X. Tan, Y. Xie, C. Jiang, et al., “Codon Usage Bias of Human Papillomavirus Type 33 and 58: A Comprehensive Analysis,” Journal of Basic Microbiology 64 (2024): 1–11.
F. Pu, R. Wang, X. Yang, et al., “Nucleotide and Codon Usage Biases Involved in the Evolution of African Swine Fever Virus: A Comparative Genomics Analysis,” Journal of Basic Microbiology 63 (2023): 499–518.
W. Wang, L. Zhou, X. Ge, et al., “Analysis of Codon Usage Patterns of Porcine Enteric Alphacoronavirus and Its Host Adaptability,” Virology 587 (2023): 109879.
R. Khandia, A. A. Khan, N. Karuvantevida, P. Gurjar, I. V. Rzhepakovsky, and I. Legaz, “Insights Into Synonymous Codon Usage Bias in Hepatitis C Virus and Its Adaptation to Hosts,” Pathogens 12 (2023): 325.
B. Li, H. Wu, Z. Miao, L. Hu, L. Zhou, and Y. Lu, “Codon Usage of Hepatitis E Viruses: A Comprehensive Analysis,” Frontiers in Microbiology 13 (2022): 938651.
J. Zhou, Y. Xing, Z. Zhou, and S. Wang, “A Comprehensive Analysis of Usutu Virus (USUV) Genomes Revealed Lineage‐Specific Codon Usage Patterns and Host Adaptations,” Frontiers in Microbiology 13 (2023): 1–15.
S. Hussain, S. T. Rasool, and A. H. Asif, “A Detailed Analysis of Synonymous Codon Usage in Human Bocavirus,” Archives of Virology 164 (2019): 335–347.
L. A. Shackelton, C. R. Parrish, and E. C. Holmes, “Evolutionary Basis of Codon Usage and Nucleotide Composition Bias in Vertebrate DNA Viruses,” Journal of Molecular Evolution 62 (2006): 551–563.
X. Xia, “Extreme Genomic CpG Deficiency in SARS‐CoV‐2 and Evasion of Host Antiviral Defense,” Molecular Biology and Evolution 37 (2020): 2699–2705.
S. V. Scherbik, J. M. Paranjape, B. M. Stockman, R. H. Silverman, and M. A. Brinton, “RNase L Plays a Role in the Antiviral Response to West Nile Virus,” Journal of Virology 80 (2006): 2987–2999.
L. Wei, J. He, X. Jia, et al., “Analysis of Codon Usage Bias of Mitochondrial Genome in Bombyx mori and Its Relation to Evolution,” BMC Evolutionary Biology 14 (2014): 262.
A. Tyagi and V. Nagar, “Genome Dynamics, Codon Usage Patterns and Influencing Factors in Aeromonas hydrophila Phages,” Virus Research 320 (2022): 198900.
N. S. Begum and S. Chakraborty, “Influencing Elements of Codon Usage Bias in Birnaviridae and Its Evolutionary Analysis,” Virus Research 310 (2022): 198672.
F. Van Hemert and B. Berkhout, “Nucleotide Composition of the Zika Virus RNA Genome and Its Codon Usage,” Virology Journal 13 (2016): 95.
D. A. Nyayanit, P. D. Yadav, R. Kharde, and S. Cherian, “Natural Selection Plays an Important Role in Shaping the Codon Usage of Structural Genes of the Viruses Belonging to the Coronaviridae Family,” Viruses 13 (2021): 3.
X. Huang, Y. Jiao, J. Guo, Y. Wang, G. Chu, and M. Wang, “Analysis of Codon Usage Patterns in Haloxylon ammodendron Based on Genomic and Transcriptomic Data,” Gene 845 (2022): 146842.
W. He, H. Zhang, Y. Zhang, et al., “Codon Usage Bias in the N Gene of Rabies Virus,” Infection, Genetics and Evolution 54 (2017): 458–465.
S. Hussain, P. Shinu, M. M. Islam, M. S. Chohan, and S. T. Rasool, “Analysis of Codon Usage and Nucleotide Bias in Middle East Respiratory Syndrome Coronavirus Genes,” Evolutionary Bioinformatics 16 (2020): 117693432091886.
C. Hu, J. Chen, L. Ye, R. Chen, L. Zhang, and X. Xue, “Codon Usage Bias in Human Cytomegalovirus and Its Biological Implication,” Gene. 545 (2014): 5–14.
F. van Hemert, A. C. van der Kuyl, and B. Berkhout, “Impact of the Biased Nucleotide Composition of Viral RNA Genomes on RNA Structure and Codon Usage,” Journal of General Virology 97 (2016): 2608–2619.
Q. Xu, J. Cao, K. R. Rai, B. Zhu, D. Liu, and C. Wan, “Codon Usage Bias of Goose Circovirus and Its Adaptation to Host,” Poultry Science 103 (2024): 103775.
M. Cho, X. Min, N. Been, and H. S. Son, “The Evolutionary and Genetic Patterns of African Swine Fever Virus,” Infection, Genetics and Evolution 122 (2024): 105612.
Z. Shafat, A. Ahmed, M. K. Parvez, and S. Parveen, “Decoding the Codon Usage Patterns in Y‐Domain Region of Hepatitis E Viruses,” Journal of Genetic Engineering and Biotechnology 20 (2022): 56.
R. Kaushik, N. Kumar, P. Yadav, et al., “Comprehensive Genomics Investigation of Neboviruses Reveals Distinct Codon Usage Patterns and Host Specificity,” Microorganisms. 12 (2024): 696.
Z. Zu, H. Lin, Y. Hu, et al., “The Genetic Evolution and Codon Usage Pattern of Severe Fever With Thrombocytopenia Syndrome Virus,” Infection, Genetics and Evolution 99 (2022): 105238.
Y. Chen, Q. Xu, X. Yuan, et al., “Analysis of the Codon Usage Pattern in Middle East Respiratory Syndrome Coronavirus,” Oncotarget 8 (2017): 110337–110349.
N. Tyagi, R. Sardar, and D. Gupta, “Natural Selection Plays a Significant Role in Governing the Codon Usage Bias in the Novel Sars‐Cov‐2 Variants of Concern (VOC),” PeerJ 10 (2022): e13562.
H. Wu, B. Li, Z. Miao, L. Hu, L. Zhou, and Y. Lu, “Codon Usage of Host‐Specific P Genotypes (VP4) in Group A Rotavirus,” BMC Genomics 23 (2022): 518.
X. Yu, J. Liu, H. Li, B. Liu, B. Zhao, and Z. Ning, “Comprehensive Analysis of Synonymous Codon Usage Patterns and Influencing Factors of Porcine Epidemic Diarrhea Virus,” Archives of Virology 166 (2021): 157–165.
C. S. Kumar, N. M. J. Hazarika, and S. Kumar, “Analysis of Synonymous Codon Usage in the VP2 Protein Gene of Infectious Bursal Disease Virus,” Archives of Virology 160 (2015): 2359–2366.
M. S. Beelagi, “Synonymous Codon Usage Pattern Among the S, M, and L Segments in Crimean‐Congo Hemorrhagic Fever Causing Virus,” Bioinformation 17 (2021): 479–491.
J. Wang, K. Liu, R. Xing, and X. Yan, “Peptide Self‐Assembly: Thermodynamics and Kinetics,” Chemical Society Reviews 45 (2016): 5589–5604.
M. Chetia, S. Debnath, S. Chowdhury, and S. Chatterjee, “Self‐Assembly and Multifunctionality of Peptide Organogels: Oil Spill Recovery, Dye Absorption and Synthesis of Conducting Biomaterials,” RSC Advances 10 (2020): 5220–5233.
J. N. Walters, G. L. Sexton, J. M. McCaffery, and P. Desai, “Mutation of Single Hydrophobic Residue I27, L35, F39, L58, L65, L67, or L71 in the N Terminus of Vp5 Abolishes Interaction With the Scaffold Protein and Prevents Closure of Herpes Simplex Virus Type 1 Capsid Shells,” Journal of Virology 77 (2003): 4043–4059.
R. M. Penczykowski, A. L. Laine, and B. Koskella, “Understanding the Ecology and Evolution of Host–Parasite Interactions Across Scales,” Evolutionary Applications 9 (2016): 37–52.
A. Papkou, C. S. Gokhale, A. Traulsen, and H. Schulenburg, “Host–Parasite Coevolution: Why Changing Population Size Matters,” Zoology 119 (2016): 330–338.
K. K. Biswas, S. Palchoudhury, P. Chakraborty, et al., “Codon Usage Bias Analysis of Citrus Tristeza Virus: Higher Codon Adaptation to Citrus reticulata Host,” Viruses 11 (2019): 331.
L. Qin, S. Ding, Z. Wang, R. Jiang, and Z. He, “Host Plants Shape the Codon Usage Pattern of Turnip Mosaic Virus,” Viruses 14 (2022): 2267.
W. Luo, A. Roy, F. Guo, et al., “Host Adaptation and Evolutionary Analysis of Zaire Ebolavirus: Insights From Codon Usage Based Investigations,” Frontiers in Microbiology 11 (2020): 570131.
P. Puigbò, L. Aragonès, and S. Garcia‐Vallvé, “RCDI/eRCDI: A Web‐Server to Estimate Codon Usage Deoptimization,” BMC Research Notes 3 (2010): 87.
W. Wu, X. Ge, Y. Zhang, et al., “Evolutionary Patterns of Codon Usage in Major Lineages of Porcine Reproductive and Respiratory Syndrome Virus in China,” Viruses 13 (2021): 1044.
G. Li, W. Zhang, R. Wang, et al., “Genetic Analysis and Evolutionary Changes of the Torque Teno Sus Virus,” International Journal of Molecular Sciences 20 (2019): 2881.
V. N. Vakharia, A. Ammayappan, S. Yusuff, T. M. Tesfaye, and G. Kurath, “Heterologous Exchanges of Glycoprotein and Non‐Virion Protein in Novirhabdoviruses: Assessment of Virulence in Yellow Perch (Perca flavescens) and Rainbow Trout (Oncorhynchus mykiss),” Viruses 16 (2024): 652.
I. S. Novella, D. K. Clarke, J. Quer, et al., “Extreme Fitness Differences in Mammalian and Insect Hosts After Continuous Replication of Vesicular Stomatitis Virus in Sandfly Cells,” Journal of Virology 69 (1995): 6805–6809.
F. Guo, J. Yang, A. M. Abd El‐Aty, R. Wang, and X. Ju, “Base Composition, Adaptation, and Evolution of Goose Astroviruses: Codon‐Based Investigation,” Poultry Science 102 (2023): 103029.

Auteurs

Yeşim Aktürk Dizman (Y)

Department of Biology, Faculty of Arts and Sciences, Recep Tayyip Erdoğan University, Rize, Türkiye.

Classifications MeSH