{"title":"芜菁皱纹病毒(-)链复制中间体的单细胞突变率。","authors":"Camila Perdoncini Carvalho, Junping Han, Khwannarin Khemsom, Ruifan Ren, Luis Eduardo Aranha Camargo, Shuhei Miyashita, Feng Qu","doi":"10.1371/journal.ppat.1011395","DOIUrl":null,"url":null,"abstract":"<p><p>Viruses with single-stranded, positive-sense (+) RNA genomes incur high numbers of errors during replication, thereby creating diversified genome populations from which new, better adapted viral variants can emerge. However, a definitive error rate is known for a relatively few (+) RNA plant viruses, due to challenges to account for perturbations caused by natural selection and/or experimental set-ups. To address these challenges, we developed a new approach that exclusively profiled errors in the (-)-strand replication intermediates of turnip crinkle virus (TCV), in singly infected cells. A series of controls and safeguards were devised to ensure errors inherent to the experimental process were accounted for. This approach permitted the estimation of a TCV error rate of 8.47 X 10-5 substitution per nucleotide site per cell infection. Importantly, the characteristic error distribution pattern among the 50 copies of 2,363-base-pair cDNA fragments predicted that nearly all TCV (-) strands were products of one replication cycle per cell. Furthermore, some of the errors probably elevated error frequencies by lowering the fidelity of TCV RNA-dependent RNA polymerase, and/or permitting occasional re-replication of progeny genomes. In summary, by profiling errors in TCV (-)-strand intermediates incurred during replication in single cells, this study provided strong support for a stamping machine mode of replication employed by a (+) RNA virus.</p>","PeriodicalId":20178,"journal":{"name":"PLoS Pathogens","volume":"19 8","pages":"e1011395"},"PeriodicalIF":6.7000,"publicationDate":"2023-08-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10449226/pdf/","citationCount":"0","resultStr":"{\"title\":\"Single-cell mutation rate of turnip crinkle virus (-)-strand replication intermediates.\",\"authors\":\"Camila Perdoncini Carvalho, Junping Han, Khwannarin Khemsom, Ruifan Ren, Luis Eduardo Aranha Camargo, Shuhei Miyashita, Feng Qu\",\"doi\":\"10.1371/journal.ppat.1011395\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Viruses with single-stranded, positive-sense (+) RNA genomes incur high numbers of errors during replication, thereby creating diversified genome populations from which new, better adapted viral variants can emerge. However, a definitive error rate is known for a relatively few (+) RNA plant viruses, due to challenges to account for perturbations caused by natural selection and/or experimental set-ups. To address these challenges, we developed a new approach that exclusively profiled errors in the (-)-strand replication intermediates of turnip crinkle virus (TCV), in singly infected cells. A series of controls and safeguards were devised to ensure errors inherent to the experimental process were accounted for. This approach permitted the estimation of a TCV error rate of 8.47 X 10-5 substitution per nucleotide site per cell infection. Importantly, the characteristic error distribution pattern among the 50 copies of 2,363-base-pair cDNA fragments predicted that nearly all TCV (-) strands were products of one replication cycle per cell. Furthermore, some of the errors probably elevated error frequencies by lowering the fidelity of TCV RNA-dependent RNA polymerase, and/or permitting occasional re-replication of progeny genomes. In summary, by profiling errors in TCV (-)-strand intermediates incurred during replication in single cells, this study provided strong support for a stamping machine mode of replication employed by a (+) RNA virus.</p>\",\"PeriodicalId\":20178,\"journal\":{\"name\":\"PLoS Pathogens\",\"volume\":\"19 8\",\"pages\":\"e1011395\"},\"PeriodicalIF\":6.7000,\"publicationDate\":\"2023-08-14\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10449226/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"PLoS Pathogens\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1371/journal.ppat.1011395\",\"RegionNum\":1,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2023/8/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q1\",\"JCRName\":\"Immunology and Microbiology\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Pathogens","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1371/journal.ppat.1011395","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2023/8/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"Immunology and Microbiology","Score":null,"Total":0}
引用次数: 0
摘要
具有单链正义(+)RNA基因组的病毒在复制过程中会产生大量错误,从而产生多样化的基因组群体,从中可以出现新的、更适应的病毒变体。然而,由于难以解释自然选择和/或实验设置引起的干扰,相对较少的(+)RNA植物病毒的确切错误率是已知的。为了应对这些挑战,我们开发了一种新的方法,专门描述了在单独感染的细胞中,芜菁皱纹病毒(TCV)的(-)链复制中间体的错误。设计了一系列控制和保障措施,以确保考虑到实验过程中固有的错误。这种方法允许估计每个核苷酸位点每细胞感染8.47 X 10-5个取代的TCV错误率。重要的是,2363个碱基对cDNA片段的50个拷贝之间的特征误差分布模式预测,几乎所有的TCV(-)链都是每个细胞一个复制周期的产物。此外,一些错误可能通过降低TCV RNA依赖性RNA聚合酶的保真度和/或允许子代基因组的偶尔重新复制来提高错误频率。总之,通过分析单细胞复制过程中TCV(-)链中间体的错误,本研究为(+)RNA病毒采用的冲压机复制模式提供了有力的支持。
Single-cell mutation rate of turnip crinkle virus (-)-strand replication intermediates.
Viruses with single-stranded, positive-sense (+) RNA genomes incur high numbers of errors during replication, thereby creating diversified genome populations from which new, better adapted viral variants can emerge. However, a definitive error rate is known for a relatively few (+) RNA plant viruses, due to challenges to account for perturbations caused by natural selection and/or experimental set-ups. To address these challenges, we developed a new approach that exclusively profiled errors in the (-)-strand replication intermediates of turnip crinkle virus (TCV), in singly infected cells. A series of controls and safeguards were devised to ensure errors inherent to the experimental process were accounted for. This approach permitted the estimation of a TCV error rate of 8.47 X 10-5 substitution per nucleotide site per cell infection. Importantly, the characteristic error distribution pattern among the 50 copies of 2,363-base-pair cDNA fragments predicted that nearly all TCV (-) strands were products of one replication cycle per cell. Furthermore, some of the errors probably elevated error frequencies by lowering the fidelity of TCV RNA-dependent RNA polymerase, and/or permitting occasional re-replication of progeny genomes. In summary, by profiling errors in TCV (-)-strand intermediates incurred during replication in single cells, this study provided strong support for a stamping machine mode of replication employed by a (+) RNA virus.
期刊介绍:
Bacteria, fungi, parasites, prions and viruses cause a plethora of diseases that have important medical, agricultural, and economic consequences. Moreover, the study of microbes continues to provide novel insights into such fundamental processes as the molecular basis of cellular and organismal function.