{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,16]],"date-time":"2026-03-16T12:17:19Z","timestamp":1773663439521,"version":"3.50.1"},"reference-count":99,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2021,12,20]],"date-time":"2021-12-20T00:00:00Z","timestamp":1639958400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Trends associated with codon usage in molluscum contagiosum virus (MCV) and factors governing the evolution of codon usage have not been investigated so far. In this study, attempts were made to decipher the codon usage trends and discover the major evolutionary forces that influence the patterns of codon usage in MCV with special reference to sub-types 1 and 2, MCV-1 and MCV-2, respectively. Three hypotheses were tested: (1) codon usage patterns of MCV-1 and MCV-2 are identical; (2) SCUB (synonymous codon usage bias) patterns of MCV-1 and MCV-2 slightly deviate from that of human host to avoid affecting the fitness of host; and (3) translational selection predominantly shapes the SCUB of MCV-1 and MCV-2. Various codon usage indices viz. relative codon usage value, effective number of codons and codon adaptation index were calculated to infer the nature of codon usage. Correspondence analysis and correlation analysis were performed to assess the relative contribution of silent base contents and significance of codon usage indices in defining bias in codon usage. Among the tested hypotheses, only the second and third hypotheses were accepted.<\/jats:p>","DOI":"10.3390\/pathogens10121649","type":"journal-article","created":{"date-parts":[[2021,12,20]],"date-time":"2021-12-20T08:43:32Z","timestamp":1639989812000},"page":"1649","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Strategies and Patterns of Codon Bias in Molluscum Contagiosum Virus"],"prefix":"10.3390","volume":"10","author":[{"given":"Rahul Raveendran","family":"Nair","sequence":"first","affiliation":[{"name":"Centre for Evolutionary Ecology, Aushmath Biosciences, Vadavalli Post, Coimbatore 641041, India"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manikandan","family":"Mohan","sequence":"additional","affiliation":[{"name":"College of Pharmacy, University of Georgia, Athens, GA 30605, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0179-5138","authenticated-orcid":false,"given":"Gudepalya R.","family":"Rudramurthy","sequence":"additional","affiliation":[{"name":"Poxvirus and Rabies Branch, Centers for Disease Control and Prevention, Atlanta, GA 30329, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Reethu","family":"Vivekanandam","sequence":"additional","affiliation":[{"name":"Department of Biotechnology, Bharathiyar University, Coimbatore 641046, India"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Panayampalli S.","family":"Satheshkumar","sequence":"additional","affiliation":[{"name":"Poxvirus and Rabies Branch, Centers for Disease Control and Prevention, Atlanta, GA 30329, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,12,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1146\/annurev.genet.42.110807.091442","article-title":"Selection on codon bias","volume":"42","author":"Hershberg","year":"2008","journal-title":"Annu. Rev. Genet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1038\/nrg2899","article-title":"Synonymous but not the same: The causes and consequences of codon bias","volume":"12","author":"Plotkin","year":"2011","journal-title":"Nat. Rev. Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/s00239-015-9714-8","article-title":"The Code of Silence: Widespread Associations between Synonymous Codon Biases and Gene Function","volume":"82","author":"Supek","year":"2016","journal-title":"J. Mol. Evol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1093\/nar\/8.1.197-c","article-title":"Codon catalog usage and the genome hypothesis","volume":"8","author":"Grantham","year":"1980","journal-title":"Nucleic Acids Res."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"LaBella, A.L., Opulente, D.A., Steenwyk, J.L., Hittinger, C.T., and Rokas, A. (2019). Variation and selection on codon usage bias across an entire subphylum. PLoS Genet., 15.","DOI":"10.1101\/608042"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1176934318761368","DOI":"10.1177\/1176934318761368","article-title":"Evolution of Synonymous Codon Usage Bias in West African and Central African Strains of Monkeypox Virus","volume":"14","author":"Karumathil","year":"2018","journal-title":"Evol. Bioinform. Online"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1016\/j.tig.2012.07.006","article-title":"Speeding with control: Codon usage, tRNAs, and ribosomes","volume":"28","author":"Novoa","year":"2012","journal-title":"Trends Genet."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2073","DOI":"10.1093\/nar\/gks1205","article-title":"Sounds of silence: Synonymous nucleotides as a key to biological regulation and complexity","volume":"41","author":"Shabalina","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Kumar, N., Bera, B.C., Greenbaum, B.D., Bhatia, S., Sood, R., Selvaraj, P., Anand, T., Tripathi, B.N., and Virmani, N. (2016). Revelation of Influencing Factors in Overall Codon Usage Bias of Equine Influenza Viruses. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0154376"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2328","DOI":"10.1093\/molbev\/msz124","article-title":"Elucidation of Codon Usage Signatures across the Domains of Life","volume":"36","author":"Novoa","year":"2019","journal-title":"Mol. Biol. Evol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1016\/j.resmic.2007.02.007","article-title":"Compositional dynamics of guanine and cytosine content in prokaryotic genomes","volume":"158","author":"Hu","year":"2007","journal-title":"Res. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Palidwor, G.A., Perkins, T.J., and Xia, X. (2010). A general model of codon bias due to GC mutational bias. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0013431"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.actatropica.2017.07.025","article-title":"New insights into the factors affecting synonymous codon usage in human infecting Plasmodium species","volume":"176","author":"Gajbhiye","year":"2017","journal-title":"Acta Trop."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2695","DOI":"10.1016\/j.ygeno.2020.03.002","article-title":"Genome-wide codon usage pattern analysis reveals the correlation between codon usage bias and gene expression in Cuscuta australis","volume":"112","author":"Liu","year":"2020","journal-title":"Genomics"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"123","DOI":"10.5808\/GI.2017.15.4.123","article-title":"Synonymous Codon Usage Controls Various Molecular Aspects","volume":"15","author":"Im","year":"2017","journal-title":"Genomics Inform."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"R77","DOI":"10.1093\/hmg\/ddw207","article-title":"The Yin and Yang of codon usage","volume":"25","author":"Komar","year":"2016","journal-title":"Hum. Mol. Genet."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1038\/nature16509","article-title":"Codon influence on protein expression in E. coli correlates with mRNA levels","volume":"529","author":"Boel","year":"2016","journal-title":"Nature"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1038\/nrm.2017.91","article-title":"Codon optimality, bias and usage in translation and mRNA decay","volume":"19","author":"Hanson","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1134\/S0026893319060098","article-title":"Synonymous Codon Usage-a Guide for Co-Translational Protein Folding in the Cell","volume":"53","author":"Komar","year":"2019","journal-title":"Mol. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1075","DOI":"10.2217\/14622416.8.8.1075","article-title":"Silent SNPs: Impact on gene function and phenotype","volume":"8","author":"Komar","year":"2007","journal-title":"Pharmacogenomics"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Behura, S.K., and Severson, D.W. (2012). Comparative analysis of codon usage bias and codon context patterns between dipteran and hymenopteran sequenced genomes. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0043111"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"5688","DOI":"10.1073\/pnas.091427698","article-title":"Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes","volume":"98","author":"Marais","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4482","DOI":"10.1073\/pnas.96.8.4482","article-title":"Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis","volume":"96","author":"Duret","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1093\/oxfordjournals.molbev.a025646","article-title":"Synonymous codon bias is related to gene length in Escherichia coli: Selection for translational accuracy?","volume":"13","year":"1996","journal-title":"Mol. Biol. Evol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Dittmar, K.A., Goodenbour, J.M., and Pan, T. (2006). Tissue-specific differences in human transfer RNA expression. PLoS Genet., 2.","DOI":"10.1371\/journal.pgen.0020221"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.gene.2007.09.020","article-title":"Amino acid and codon usage profiles: Adaptive changes in the frequency of amino acids and codons","volume":"407","author":"Goodarzi","year":"2008","journal-title":"Gene"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"5125","DOI":"10.1093\/nar\/14.13.5125","article-title":"Codon usage in yeast: Cluster analysis clearly differentiates highly and lowly expressed genes","volume":"14","author":"Sharp","year":"1986","journal-title":"Nucleic Acids Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3480","DOI":"10.1073\/pnas.0307827100","article-title":"Codon usage between genomes is constrained by genome-wide mutational processes","volume":"101","author":"Chen","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1098\/rstb.2009.0305","article-title":"Forces that influence the evolution of codon bias","volume":"365","author":"Sharp","year":"2010","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Lassalle, F., Perian, S., Bataillon, T., Nesme, X., Duret, L., and Daubin, V. (2015). GC-Content evolution in bacterial genomes: The biased gene conversion hypothesis expands. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1004941"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1038\/s41559-017-0425-y","article-title":"Evolutionary determinants of genome-wide nucleotide composition","volume":"2","author":"Long","year":"2018","journal-title":"Nat. Ecol. Evol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.gene.2018.10.030","article-title":"Compositional properties and codon usage of TP73 gene family","volume":"683","author":"Barbhuiya","year":"2019","journal-title":"Gene"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0168-1702(02)00309-X","article-title":"The extent of codon usage bias in human RNA viruses and its evolutionary origin","volume":"92","author":"Jenkins","year":"2003","journal-title":"Virus Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1007\/s00239-006-0257-x","article-title":"Reduced selection for codon usage bias in Drosophila miranda","volume":"64","author":"Bachtrog","year":"2007","journal-title":"J. Mol. Evol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1390","DOI":"10.1093\/oxfordjournals.molbev.a004201","article-title":"Accounting for background nucleotide composition when measuring codon usage bias","volume":"19","author":"Novembre","year":"2002","journal-title":"Mol. Biol. Evol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"e2023575118","DOI":"10.1073\/pnas.2023575118","article-title":"Weak selection on synonymous codons substantially inflates dN\/dS estimates in bacteria","volume":"118","author":"Rahman","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1006\/tpbi.1996.0007","article-title":"Development of Neutral and Nearly Neutral Theories","volume":"49","author":"Ohta","year":"1996","journal-title":"Theor. Popul. Biol."},{"key":"ref_38","unstructured":"Kreitman, M., and Antezana, M. (2000). The Population and Evolutionary Genetis of Codon Bias, Camridge University Press."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1038\/scientificamerican1204-100","article-title":"Are viruses alive?","volume":"291","author":"Villarreal","year":"2004","journal-title":"Sci. Am."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1038\/nri2802","article-title":"Immunity and immunopathology to viruses: What decides the outcome?","volume":"10","author":"Rouse","year":"2010","journal-title":"Nat. Rev. Immunol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1038\/msb.2009.71","article-title":"Viral adaptation to host: A proteome-based analysis of codon usage and amino acid preferences","volume":"5","author":"Bahir","year":"2009","journal-title":"Mol. Syst. Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"886","DOI":"10.3389\/fmicb.2019.00886","article-title":"Analysis of Nipah Virus Codon Usage and Adaptation to Hosts","volume":"10","author":"Khandia","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"114032","DOI":"10.1016\/j.jviromet.2020.114032","article-title":"Genomic and evolutionary comparison between SARS-CoV-2 and other human coronaviruses","volume":"289","author":"Chen","year":"2021","journal-title":"J. Virol. Methods"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.virusres.2019.01.011","article-title":"Analysis of codon usage patterns and influencing factors in Nipah virus","volume":"263","author":"Chakraborty","year":"2019","journal-title":"Virus Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1126\/science.273.5276.813","article-title":"Genome sequence of a human tumorigenic poxvirus: Prediction of specific host response-evasion genes","volume":"273","author":"Senkevich","year":"1996","journal-title":"Science"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1111\/jdv.16856","article-title":"2020 European guideline on the management of genital molluscum contagiosum","volume":"35","author":"Edwards","year":"2021","journal-title":"J. Eur. Acad. Dermatol. Venereol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"373","DOI":"10.2147\/CCID.S187224","article-title":"Molluscum contagiosum: An update and review of new perspectives in etiology, diagnosis, and treatment","volume":"12","author":"Downey","year":"2019","journal-title":"Clin. Cosmet. Investig. Dermatol."},{"key":"ref_48","unstructured":"Bateman, T. (1814). A Practical Synopsis of Cutaneous Diseases, Longman Hurst Rees Orme & Brown."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1598","DOI":"10.1055\/s-0029-1188377","article-title":"Zue kenntnis des virus des Molluscum contagiosum","volume":"31","author":"Juliusberg","year":"1905","journal-title":"Dtsch. Med. Wochenschr."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"S12","DOI":"10.1067\/S0002-9378(03)00793-2","article-title":"Molluscum contagiosum: The importance of early diagnosis and treatment","volume":"189","author":"Tyring","year":"2003","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1111\/pde.12504","article-title":"Molluscum contagiosum: To treat or not to treat? Experience with 170 children in an outpatient clinic setting in the northeastern United States","volume":"32","author":"Basdag","year":"2015","journal-title":"Pediatr. Dermatol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1007\/s13671-020-00289-z","article-title":"Molluscum contagiosum: Review and update on clinical presentation, diagnosis, risk, prevention and treatment","volume":"9","author":"Robinson","year":"2020","journal-title":"Curr. Dermatol. Rep."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Badri, T., and Gandhi, G.R. (2003). Molluscum contagiosum. Dermatol. Online J., 9.","DOI":"10.5070\/D36Z11D13P"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Bugert, J.J. (2008). Molluscum Contagiosum Virus, Elsevier-Academic Press.","DOI":"10.1016\/B978-012374410-4.00444-1"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1006\/viro.1997.8607","article-title":"The genome of molluscum contagiosum virus: Analysis and comparison with other poxviruses","volume":"233","author":"Senkevich","year":"1997","journal-title":"Virology"},{"key":"ref_56","unstructured":"Domingo, E., Parrish, C.R., and Holland, J.J. (2008). Origin and Evolution of Poxviruses, Academic Press (Elsevier)."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/bs.aivir.2014.11.004","article-title":"Immune evasion strategies of molluscum contagiosum virus","volume":"92","author":"Shisler","year":"2015","journal-title":"Adv. Virus Res."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Porter, C.D., Blake, N.W., Cream, J.J., and Archard, L.C. (1992). Molluscum Contagiosum Virus, Springer.","DOI":"10.1007\/978-94-011-2384-6_8"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/BF02715890","article-title":"Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species","volume":"84","author":"Liu","year":"2005","journal-title":"J. Genet."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/emi.2016.106","article-title":"Evolution of codon usage in Zika virus genomes is host and vector specific","volume":"5","author":"Butt","year":"2016","journal-title":"Emerg. Microbes Infect."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/s00425-020-03470-7","article-title":"Analysis of codon usage bias of chloroplast genes in Oryza species : Codon usage of chloroplast genes in Oryza species","volume":"252","author":"Chakraborty","year":"2020","journal-title":"Planta"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"646300","DOI":"10.3389\/fmicb.2021.646300","article-title":"Nucleotide Composition and Codon Usage across Viruses and Their Respective Hosts","volume":"12","author":"Simon","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"699788","DOI":"10.3389\/fmicb.2021.699788","article-title":"Edging on Mutational Bias, Induced Natural Selection From Host and Natural Reservoirs Predominates Codon Usage Evolution in Hantaan Virus","volume":"12","author":"Ata","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1146\/annurev-biophys-060414-034333","article-title":"Roles for Synonymous Codon Usage in Protein Biogenesis","volume":"44","author":"Chaney","year":"2015","journal-title":"Annu. Rev. Biophys."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"198113","DOI":"10.1016\/j.virusres.2020.198113","article-title":"Analysis of codon usage of severe acute respiratory syndrome corona virus 2 (SARS-CoV-2) and its adaptability in dog","volume":"288","author":"Dutta","year":"2020","journal-title":"Virus Res."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"167","DOI":"10.4137\/BBI.S38192","article-title":"Evolution of Synonymous Codon Usage in the Mitogenomes of Certain Species of Bilaterian Lineage with Special Reference to Chaetognatha","volume":"10","author":"Karumathil","year":"2016","journal-title":"Bioinform. Biol. Insights"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1168","DOI":"10.1016\/j.meegid.2011.02.018","article-title":"The characteristics of the synonymous codon usage in enterovirus 71 virus and the effects of host on the virus in codon usage pattern","volume":"11","author":"Liu","year":"2011","journal-title":"Infect. Genet. Evol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1007\/PL00006384","article-title":"An evaluation of measures of synonymous codon usage bias","volume":"47","author":"Comeron","year":"1998","journal-title":"J. Mol. Evol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"e20190240","DOI":"10.1590\/1678-4685-gmb-2019-0240","article-title":"Comparative analysis of codon usage patterns in Rift Valley fever virus","volume":"43","author":"Kim","year":"2020","journal-title":"Genet. Mol. Biol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.virusres.2009.11.018","article-title":"A detailed comparative analysis on the overall codon usage pattern in herpesviruses","volume":"148","author":"Roychoudhury","year":"2010","journal-title":"Virus Res."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/0378-1119(90)90491-9","article-title":"The \u2019effective number of codons\u2019 used in a gene","volume":"87","author":"Wright","year":"1990","journal-title":"Gene"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"e4595","DOI":"10.7717\/peerj.4595","article-title":"Gene characteristics of the complete mitochondrial genomes of Paratoxodera polyacantha and Toxodera hauseri (Mantodea: Toxoderidae)","volume":"6","author":"Zhang","year":"2018","journal-title":"PeerJ"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1007\/s00239-005-0221-1","article-title":"Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses","volume":"62","author":"Shackelton","year":"2006","journal-title":"J. Mol. Evol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"3746","DOI":"10.1073\/pnas.83.11.3746","article-title":"Predicting DNA duplex stability from the base sequence","volume":"83","author":"Breslauer","year":"1986","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1073\/pnas.86.1.192","article-title":"Evolution of the genome and the genetic code: Selection at the dinucleotide level by methylation and polyribonucleotide cleavage","volume":"86","author":"Beutler","year":"1989","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.celrep.2015.12.011","article-title":"Codon Pair Bias Is a Direct Consequence of Dinucleotide Bias","volume":"14","author":"Kunec","year":"2016","journal-title":"Cell Rep."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1093\/genetics\/136.3.927","article-title":"Synonymous codon usage in Drosophila melanogaster: Natural selection and translational accuracy","volume":"136","author":"Akashi","year":"1994","journal-title":"Genetics"},{"key":"ref_78","first-page":"13","article-title":"Codon usage and tRNA content in unicellular and multicellular organisms","volume":"2","author":"Ikemura","year":"1985","journal-title":"Mol. Biol. Evol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1093\/genetics\/163.1.239","article-title":"In vivo introduction of unpreferred synonymous codons into the Drosophila Adh gene results in reduced levels of ADH protein","volume":"163","author":"Carlini","year":"2003","journal-title":"Genetics"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"6663","DOI":"10.1093\/nar\/12.17.6663","article-title":"Codon usage can affect efficiency of translation of genes in Escherichia coli","volume":"12","author":"Robinson","year":"1984","journal-title":"Nucleic Acids Res."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/S0042-6822(03)00483-5","article-title":"Evidence for quasispecies distributions in the human hepatitis A virus genome","volume":"315","author":"Sanchez","year":"2003","journal-title":"Virology"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1073\/pnas.0810122106","article-title":"Genome rhetoric and the emergence of compositional bias","volume":"106","author":"Vetsigian","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"Vicario, S., Moriyama, E.N., and Powell, J.R. (2007). Codon usage in twelve species of Drosophila. BMC Evol. Biol., 7.","DOI":"10.1186\/1471-2148-7-226"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.virusres.2007.04.010","article-title":"Codon usage and replicative strategies of hepatitis A virus","volume":"127","author":"Pinto","year":"2007","journal-title":"Virus Res."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1626","DOI":"10.1126\/science.1089670","article-title":"Mobile elements: Drivers of genome evolution","volume":"303","author":"Kazazian","year":"2004","journal-title":"Science"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: Multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"Edgar","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1080\/07391102.2004.10506946","article-title":"Synonymous codon usage in Lactococcus lactis: Mutational bias versus translational selection","volume":"21","author":"Gupta","year":"2004","journal-title":"J. Biomol. Struct. Dyn."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1186\/2193-1801-2-492","article-title":"Mutational pressure dictates synonymous codon usage in freshwater unicellular alpha-cyanobacterial descendant Paulinella chromatophora and beta-cyanobacterium Synechococcus elongatus PCC6301","volume":"2","author":"Nair","year":"2013","journal-title":"Springerplus"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"2653","DOI":"10.1073\/pnas.85.8.2653","article-title":"Directional mutation pressure and neutral molecular evolution","volume":"85","author":"Sueoka","year":"1988","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1007\/BF00163236","article-title":"Intrastrand parity rules of DNA base composition and usage biases of synonymous codons","volume":"40","author":"Sueoka","year":"1995","journal-title":"J. Mol. Evol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1007\/s00705-020-04857-3","article-title":"Comprehensive analysis of synonymous codon usage patterns and influencing factors of porcine epidemic diarrhea virus","volume":"166","author":"Yu","year":"2021","journal-title":"Arch. Virol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.meegid.2014.09.004","article-title":"Characterization of the porcine epidemic diarrhea virus codon usage bias","volume":"28","author":"Chen","year":"2014","journal-title":"Infect. Genet. Evol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/S0378-1119(99)00320-0","article-title":"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","volume":"238","author":"Sueoka","year":"1999","journal-title":"Gene"},{"key":"ref_95","unstructured":"Greencare, M.J. (1984). Theory and Applications of Correspondence Analysis, Academic Press."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"4548","DOI":"10.1093\/nar\/gkf565","article-title":"Use and misuse of correspondence analysis in codon usage studies","volume":"30","author":"Perriere","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1007\/s12033-011-9383-9","article-title":"Synonymous codon usage, GC(3), and evolutionary patterns across plastomes of three pooid model species: Emerging grass genome models for monocots","volume":"49","author":"Sablok","year":"2011","journal-title":"Mol. Biotechnol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1550","DOI":"10.1093\/molbev\/msy073","article-title":"DAMBE7: New and Improved Tools for Data Analysis in Molecular Biology and Evolution","volume":"35","author":"Xia","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_99","first-page":"1","article-title":"PAST: Palaeontological statistics software package for education and data analysis","volume":"4","author":"Hammer","year":"2001","journal-title":"Palaeontol. Electron."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/12\/1649\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:49:55Z","timestamp":1760168995000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/12\/1649"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,20]]},"references-count":99,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["pathogens10121649"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10121649","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,12,20]]}}}