{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T01:31:37Z","timestamp":1760232697079,"version":"build-2065373602"},"reference-count":79,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2022,11,21]],"date-time":"2022-11-21T00:00:00Z","timestamp":1668988800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Recombination and mutation of viral genomes represent major mechanisms for viral evolution and, in many cases, moderate pathogenicity. Segmented genome viruses frequently undergo reassortment of the genome via multiple infection of host organisms, with influenza and reoviruses being well-known examples. Specifically, major genomic shifts mediated by reassortment are responsible for radical changes in the influenza antigenic determinants that can result in pandemics requiring rapid preventative responses by vaccine modifications. In contrast, smaller mutational changes brought about by the error-prone viral RNA polymerases that, for the most part, lack a replication base mispairing editing function produce small mutational changes in the RNA genome during replication. Referring again to the influenza example, the accumulated mutations\u2014known as drift\u2014require yearly vaccine updating and rapid worldwide distribution of each new formulation. Coronaviruses with a large positive-sense RNA genome have long been known to undergo intramolecular recombination likely mediated by copy choice of the RNA template by the viral RNA polymerase in addition to the polymerase-based mutations. The current SARS-CoV-2 origin debate underscores the importance of understanding the plasticity of viral genomes, particularly the mechanisms responsible for intramolecular recombination. This review describes the use of the cystovirus bacteriophage as an experimental model for recombination studies in a controlled manner, resulting in the development of a model for intramolecular RNA genome alterations. The review relates the sequence of experimental studies from the laboratory of Leonard Mindich, PhD at the Public Health Research Institute\u2014then in New York City\u2014and covers a period of approximately 12 years. Hence, this is a historical scientific review of research that has the greatest relevance to current studies of emerging RNA virus pathogens.<\/jats:p>","DOI":"10.3390\/v14112589","type":"journal-article","created":{"date-parts":[[2022,11,22]],"date-time":"2022-11-22T03:04:20Z","timestamp":1669086260000},"page":"2589","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Heterologous RNA Recombination in the Cystoviruses \u03c66 and \u03c68: A Mechanism of Viral Variation and Genome Repair"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1963-2732","authenticated-orcid":false,"given":"Paul","family":"Gottlieb","sequence":"first","affiliation":[{"name":"School of Medicine, The City College of New York, The City University of New York (CUNY), New York, NY 10030, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aleksandra","family":"Alimova","sequence":"additional","affiliation":[{"name":"School of Medicine, The City College of New York, The City University of New York (CUNY), New York, NY 10030, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,11,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1101\/SQB.1962.027.001.028","article-title":"Genetic Recombination with Newcastle Disease Virus, Polioviruses, and Influenza","volume":"27","author":"Hirst","year":"1962","journal-title":"Cold Spring Harb. Symp. Quant. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1016\/0092-8674(86)90600-8","article-title":"The mechanism of RNA recombination in poliovirus","volume":"47","author":"Kirkegaard","year":"1986","journal-title":"Cell"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1128\/mr.56.1.61-79.1992","article-title":"RNA recombination in animal and plant viruses","volume":"56","author":"Lai","year":"1992","journal-title":"Microbiol. Rev."},{"key":"ref_4","first-page":"21","article-title":"Genetic Recombination in RNA Viruses","volume":"176","author":"Lai","year":"1992","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"6117","DOI":"10.1128\/jvi.66.10.6117-6124.1992","article-title":"RNA recombination in a coronavirus: Recombination between viral genomic RNA and transfected RNA fragments","volume":"66","author":"Liao","year":"1992","journal-title":"J. Virol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1016\/0042-6822(91)90801-H","article-title":"Comparison of the 5\u2032 and 3\u2032 termini of tomato ringspot virus RNA1 and RNA2: Evidence for RNA recombination","volume":"185","author":"Rott","year":"1991","journal-title":"Virology"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Bentley, K., Alnaji, F.G., Woodford, L., Jones, S., Woodman, A., and Evans, D.J. (2021). Imprecise recombinant viruses evolve via a fitness-driven, iterative process of polymerase template-switching events. PLOS Pathog., 17.","DOI":"10.1101\/2021.06.01.446546"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.1099\/jgv.0.001142","article-title":"Mechanisms and consequences of positive-strand RNA virus recombination","volume":"99","author":"Bentley","year":"2018","journal-title":"J. Gen. Virol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Bentley, K., Tee, H.K., Pearson, A., Lowry, K., Waugh, S., Jones, S., Chan, Y.F., and Evans, D.J. (2021). Isolation and Identification of Inter-Species Enterovirus Recombinant Genomes. Viruses, 13.","DOI":"10.3390\/v13122390"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1016\/j.tim.2016.03.003","article-title":"Epidemiology, Genetic Recombination, and Pathogenesis of Coronaviruses","volume":"24","author":"Su","year":"2016","journal-title":"Trends Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1146\/annurev-virology-101416-041726","article-title":"Constraints, Drivers, and Implications of Influenza A Virus Reassortment","volume":"4","author":"Lowen","year":"2017","journal-title":"Annu. Rev. Virol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/S0065-3527(08)60795-2","article-title":"Genomic Segment Reassortment in Rotaviruses and Other Reoviridae","volume":"39","author":"Ramig","year":"1991","journal-title":"Adv. Virus Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1016\/j.cell.2020.08.021","article-title":"Emerging Pandemic Diseases: How We Got to COVID-19","volume":"182","author":"Morens","year":"2020","journal-title":"Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.virusres.2003.12.008","article-title":"Packaging, replication and recombination of the segmented genomes of bacteriophage \u03a66 and its relatives","volume":"101","author":"Mindich","year":"2004","journal-title":"Virus Res."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Focosi, D., and Maggi, F. (2022). Recombination in Coronaviruses, with a Focus on SARS-CoV-2. Viruses, 14.","DOI":"10.3390\/v14061239"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1224","DOI":"10.1016\/S0140-6736(22)01585-9","article-title":"The Lancet Commission on lessons for the future from the COVID-19 pandemic","volume":"400","author":"Sachs","year":"2022","journal-title":"Lancet"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4848","DOI":"10.1016\/j.cell.2021.08.017","article-title":"The origins of SARS-CoV-2: A critical review","volume":"184","author":"Holmes","year":"2021","journal-title":"Cell"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"4505","DOI":"10.1128\/JB.181.15.4505-4508.1999","article-title":"Isolation of Additional Bacteriophages with Genomes of Segmented Double-Stranded RNA","volume":"181","author":"Mindich","year":"1999","journal-title":"J. Bacteriol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1186\/1471-2180-10-55","article-title":"Characterization of \u03a62954, a newly isolated bacteriophage containing three dsRNA genomic segments","volume":"10","author":"Qiao","year":"2010","journal-title":"BMC Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1128\/jvi.11.5.799-805.1973","article-title":"Bacteriophage \u03c66: A Lipid-Containing Virus of Pseudomonas phaseolicola","volume":"11","author":"Vidaver","year":"1973","journal-title":"J. Virol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"706","DOI":"10.1016\/S0042-6822(03)00460-4","article-title":"Temperature requirements for initiation of RNA-dependent RNA polymerization","volume":"314","author":"Yang","year":"2003","journal-title":"Virology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1007\/s12098-020-03625-0","article-title":"Rotavirus Gastroenteritis in Eastern Uttar Pradesh, India","volume":"88","author":"Gupta","year":"2021","journal-title":"Indian J. Pediatr."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1016\/j.str.2006.03.018","article-title":"Structure of the Bacteriophage \u03d56 Nucleocapsid Suggests a Mechanism for Sequential RNA Packaging","volume":"14","author":"Huiskonen","year":"2006","journal-title":"Structure"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1374","DOI":"10.1016\/j.str.2013.06.007","article-title":"Subunit Folds and Maturation Pathway of a dsRNA Virus Capsid","volume":"21","author":"Nemecek","year":"2013","journal-title":"Structure"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.jmb.2011.10.004","article-title":"Stepwise Expansion of the Bacteriophage \u03d56 Procapsid: Possible Packaging Intermediates","volume":"414","author":"Nemecek","year":"2011","journal-title":"J. Mol. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Wei, H., Cheng, R.H., Berriman, J., Rice, W.J., Stokes, D.L., Katz, A., Morgan, D.G., and Gottlieb, P. (2009). Three-Dimensional Structure of the Enveloped Bacteriophage \u03a612: An Incomplete T = 13 Lattice Is Superposed on an Enclosed T = 1 Shell. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0006850"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.virol.2011.03.020","article-title":"Toroidal surface complexes of bacteriophage \u03d512 are responsible for host-cell attachment","volume":"414","author":"Katz","year":"2011","journal-title":"Virology"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/0042-6822(88)90245-0","article-title":"Nucleotide sequence of the middle dsRNA segment of bacteriophage \u03c66: Placement of the genes of membrane-associated proteins","volume":"163","author":"Gottlieb","year":"1988","journal-title":"Virology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1128\/jvi.58.1.142-151.1986","article-title":"Nucleotide sequence of the small double-stranded RNA segment of bacteriophage phi 6: Novel mechanism of natural translational control","volume":"58","author":"McGraw","year":"1986","journal-title":"J. Virol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1180","DOI":"10.1128\/jvi.62.4.1180-1185.1988","article-title":"Nucleotide sequence of the large double-stranded RNA segment of bacteriophage phi 6: Genes specifying the viral replicase and transcriptase","volume":"62","author":"Mindich","year":"1988","journal-title":"J. Virol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1562\/2005-01-14-RA-416R1.1","article-title":"Virus Particle and Receptor Interaction Monitored by Fluorescence Spectroscopy","volume":"81","author":"Alimova","year":"2005","journal-title":"Photochem. Photobiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/0005-2736(80)90530-1","article-title":"Structure of the lipid-containing bacteriophage \u03c66 Disruption by triton X-100 treatment","volume":"601","author":"Bamford","year":"1980","journal-title":"Biochim. et Biophys. Acta (BBA) -Biomembr."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1128\/jb.126.1.177-182.1976","article-title":"Isolation of nonsense suppressor mutants in Pseudomonas","volume":"126","author":"Mindich","year":"1976","journal-title":"J. Bacteriol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1180","DOI":"10.1099\/vir.0.000063","article-title":"New enveloped dsRNA phage from freshwater habitat","volume":"96","author":"Laanto","year":"2015","journal-title":"J. Gen. Virol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"38795","DOI":"10.1038\/srep38795","article-title":"Characterization of the first double-stranded RNA bacteriophage infecting Pseudomonas aeruginosa","volume":"6","author":"Yang","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1006\/viro.2002.1436","article-title":"Characterization of \u03c612, a Bacteriophage Related to \u03c66: Nucleotide Sequence of the Large Double-Stranded RNA","volume":"295","author":"Gottlieb","year":"2002","journal-title":"Virology"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1006\/viro.2001.1288","article-title":"Characterization of \u03c612, a Bacteriophage Related to \u03c66: Nucleotide Sequence of the Small and Middle Double-Stranded RNA","volume":"293","author":"Gottlieb","year":"2002","journal-title":"Virology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1006\/viro.2000.0501","article-title":"Characterization of \u03a613, a Bacteriophage Related to \u03a66 and Containing Three dsRNA Genomic Segments","volume":"275","author":"Qiao","year":"2000","journal-title":"Virology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"5774","DOI":"10.1128\/jb.172.10.5774-5782.1990","article-title":"In vitro replication, packaging, and transcription of the segmented double-stranded RNA genome of bacteriophage phi 6: Studies with procapsids assembled from plasmid-encoded proteins","volume":"172","author":"Gottlieb","year":"1990","journal-title":"J. Bacteriol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1006\/viro.1994.1160","article-title":"Identification of the Packaging Regions within the Genomic RNA Segments of Bacteriophage \u03a66","volume":"200","author":"Gottlieb","year":"1994","journal-title":"Virology"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1038\/s41586-019-1229-9","article-title":"Multiple liquid crystalline geometries of highly compacted nucleic acid in a dsRNA virus","volume":"570","author":"Ilca","year":"2019","journal-title":"Nature"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Oliveira, L.M., Ye, Z., Katz, A., Alimova, A., Wei, H., Herman, G.T., and Gottlieb, P. (2018). Component tree analysis of cystovirus \u03c66 nucleocapsid Cryo-EM single particle reconstructions. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0188858"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Gottlieb, P., and Alimova, A. (2022). RNA Packaging in the Cystovirus Bacteriophages: Dynamic Interactions during Capsid Maturation. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23052677"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"9173","DOI":"10.1073\/pnas.87.23.9173","article-title":"In vitro assembly of infectious nucleocapsids of bacteriophage phi 6: Formation of a recombinant double-stranded RNA virus","volume":"87","author":"Olkkonen","year":"1990","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1128\/jvi.66.1.190-196.1992","article-title":"Construction of a transducing virus from double-stranded RNA bacteriophage phi6: Establishment of carrier states in host cells","volume":"66","author":"Onodera","year":"1992","journal-title":"J. Virol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/0092-8674(81)90050-7","article-title":"Role of the host cell in persistent viral infection: Coevolution of L cells and reovirus during persistent infection","volume":"25","author":"Ahmed","year":"1981","journal-title":"Cell"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1128\/jvi.35.1.249-251.1980","article-title":"In vitro translation of the three bacteriophage phi 6 RNAs","volume":"35","author":"Cuppels","year":"1980","journal-title":"J. Virol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1099\/0022-1317-56-2-287","article-title":"6-Resistant Phage-producing Mutants of Pseudomonas phaseolicola","volume":"56","author":"Romantschuk","year":"1981","journal-title":"J. Gen. Virol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"2605","DOI":"10.1128\/jvi.66.5.2605-2610.1992","article-title":"Heterologous recombination in the double-stranded RNA bacteriophage phi 6","volume":"66","author":"Mindich","year":"1992","journal-title":"J. Virol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"4914","DOI":"10.1128\/jvi.67.8.4914-4922.1993","article-title":"RNA structure and heterologous recombination in the double-stranded RNA bacteriophage phi 6","volume":"67","author":"Onodera","year":"1993","journal-title":"J. Virol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3642","DOI":"10.1073\/pnas.74.9.3642","article-title":"Filamentous coliphage M13 as a cloning vehicle: Insertion of a HindII fragment of the lac regulatory region in M13 replicative form in vitro","volume":"74","author":"Messing","year":"1977","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1006\/viro.1994.1341","article-title":"RNA Structural Requirements for Stability and Minus-Strand Synthesis in the dsRNA Bacteriophage 6","volume":"202","author":"Mindich","year":"1994","journal-title":"Virology"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"5013","DOI":"10.1128\/jvi.66.8.5013-5017.1992","article-title":"Dependence of minus-strand synthesis on complete genomic packaging in the double-stranded RNA bacteriophage phi 6","volume":"66","author":"Frilander","year":"1992","journal-title":"J. Virol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2926","DOI":"10.1128\/jvi.69.5.2926-2931.1995","article-title":"In vitro packaging of individual genomic segments of bacteriophage phi 6 RNA: Serial dependence relationships","volume":"69","author":"Qiao","year":"1995","journal-title":"J. Virol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2611","DOI":"10.1128\/jvi.66.5.2611-2616.1992","article-title":"In vitro packaging and replication of individual genomic segments of bacteriophage phi 6 RNA","volume":"66","author":"Gottlieb","year":"1992","journal-title":"J. Virol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1006\/jmbi.1994.0096","article-title":"In VitroPackaging of the Single-stranded RNA Genomic Precursors of the Segmented Double-stranded RNA Bacteriophage \u03c8: The Three Segments Modulate Each Other\u2019s Packaging Efficiency","volume":"246","author":"Frilander","year":"1995","journal-title":"J. Mol. Biol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1016\/j.jsb.2006.08.021","article-title":"Structure of a hexameric RNA packaging motor in a viral polymerase complex","volume":"158","author":"Huiskonen","year":"2007","journal-title":"J. Struct. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"5502","DOI":"10.1128\/jvi.69.9.5502-5505.1995","article-title":"Interference with bacteriophage phi 6 genomic RNA packaging by hairpin structures","volume":"69","author":"Qiao","year":"1995","journal-title":"J. Virol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"10122","DOI":"10.1128\/JVI.76.20.10122-10127.2002","article-title":"Nonspecific Nucleoside Triphosphatase P4 of Double-Stranded RNA Bacteriophage \u03c66 Is Required for Single-Stranded RNA Packaging and Transcription","volume":"76","author":"Pirttimaa","year":"2002","journal-title":"J. Virol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1016\/j.cell.2004.09.007","article-title":"Atomic Snapshots of an RNA Packaging Motor Reveal Conformational Changes Linking ATP Hydrolysis to RNA Translocation","volume":"118","author":"Mancini","year":"2004","journal-title":"Cell"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1006\/viro.1995.1470","article-title":"Packaging of Multiple Copies of Reduced-Size Genomic Segments by Bacteriophage 6","volume":"212","author":"Mindich","year":"1995","journal-title":"Virology"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1006\/viro.1995.1469","article-title":"Acquisition of a Fourth Genomic Segment in Bacteriophage \u03a66, a Bacteriophage with a Genome of Three Segments of dsRNA","volume":"212","author":"Onodera","year":"1995","journal-title":"Virology"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/0042-6822(76)90018-0","article-title":"The isolation of suppressible nonsense mutants of bacteriophage phi6","volume":"75","author":"Sinclair","year":"1976","journal-title":"Virology"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1016\/S0042-6822(03)00013-8","article-title":"Unique properties of the inner core of bacteriophage \u03c68, a virus with a segmented dsRNA genome","volume":"308","author":"Sun","year":"2003","journal-title":"Virology"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1006\/viro.1996.8311","article-title":"Anin Vitro System for the Investigation of Heterologous RNA Recombination","volume":"227","author":"Qiao","year":"1997","journal-title":"Virology"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1006\/viro.2000.0374","article-title":"Characterization of \u03a68, a Bacteriophage Containing Three Double-Stranded RNA Genomic Segments and Distantly Related to \u03a66","volume":"272","author":"Hoogstraten","year":"2000","journal-title":"Virology"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1006\/viro.2001.0995","article-title":"Reverse Genetics and Recombination in \u03a68, a dsRNA Bacteriophage","volume":"286","author":"Onodera","year":"2001","journal-title":"Virology"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1261\/rna.348307","article-title":"Large-scale production of dsRNA and siRNA pools for RNA interference utilizing bacteriophage \u03d56 RNA-dependent RNA polymerase","volume":"13","author":"Aalto","year":"2007","journal-title":"RNA"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.virol.2003.10.022","article-title":"Construction of carrier state viruses with partial genomes of the segmented dsRNA bacteriophages","volume":"319","author":"Sun","year":"2004","journal-title":"Virology"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1006\/viro.1998.9479","article-title":"Isolation of a Mutant That Changes Genomic Packaging Specificity in \u03c66","volume":"252","author":"Onodera","year":"1998","journal-title":"Virology"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"4074","DOI":"10.1073\/pnas.94.8.4074","article-title":"Stoichiometric packaging of the three genomic segments of double-stranded RNA bacteriophage \u03a66","volume":"94","author":"Qiao","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1384","DOI":"10.1016\/j.str.2013.06.017","article-title":"Plate Tectonics of Virus Shell Assembly and Reorganization in Phage \u03a68, a Distant Relative of Mammalian Reoviruses","volume":"21","author":"Sutton","year":"2013","journal-title":"Structure"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1016\/0042-6822(83)90157-5","article-title":"Morphogenesis of bacteriophage \u03c66. A presumptive viral membrane precursor","volume":"127","author":"Stitt","year":"1983","journal-title":"Virology"},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Huang, C., Liu, W.J., Xu, W., Jin, T., Zhao, Y., Song, J., Shi, Y., Ji, W., Jia, H., and Zhou, Y. (2016). A Bat-Derived Putative Cross-Family Recombinant Coronavirus with a Reovirus Gene. PLOS Pathog., 12.","DOI":"10.1371\/journal.ppat.1005883"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"2341","DOI":"10.1007\/s00705-020-04750-z","article-title":"A palindromic RNA sequence as a common breakpoint contributor to copy-choice recombination in SARS-CoV-2","volume":"165","author":"Gallaher","year":"2020","journal-title":"Arch. Virol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1056\/NEJMoa2001017","article-title":"A Novel Coronavirus from Patients with Pneumonia in China, 2019","volume":"382","author":"Zhu","year":"2020","journal-title":"N. Engl. J. Med."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1038\/d41586-022-01209-w","article-title":"Risky \u2018gain-of-function\u2019 studies need stricter guidance, say US researchers","volume":"605","author":"Kozlov","year":"2022","journal-title":"Nature"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1038\/s41467-022-28603-2","article-title":"Secondary structural ensembles of the SARS-CoV-2 RNA genome in infected cells","volume":"13","author":"Lan","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"5885","DOI":"10.1038\/s41467-020-19619-7","article-title":"SARS-CoV-2 structure and replication characterized by in situ cryo-electron tomography","volume":"11","author":"Klein","year":"2020","journal-title":"Nat. Commun."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/11\/2589\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:23:13Z","timestamp":1760145793000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/11\/2589"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,21]]},"references-count":79,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2022,11]]}},"alternative-id":["v14112589"],"URL":"https:\/\/doi.org\/10.3390\/v14112589","relation":{},"ISSN":["1999-4915"],"issn-type":[{"type":"electronic","value":"1999-4915"}],"subject":[],"published":{"date-parts":[[2022,11,21]]}}}