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Intracellular bottlenecking permits no more than three tomato yellow leaf curl virus genomes to initiate replication in a single cell

文献类型： 外文期刊

作者： Ren, Ruifan 1 ; Zheng, Limin 2 ; Han, Junping 2 ; Carvalho, Camila Perdoncini 2 ; Miyashita, Shuhei 4 ; Zhang, Deyong 1 ; Qu, Feng 2 ;

作者机构： 1.Hunan Univ, Coll Biol, Longping Branch, Changsha, Peoples R China

2.Ohio State Univ, Dept Plant Pathol, Wooster, OH 43210 USA

3.Hunan Plant Protect Inst, Changsha, Peoples R China

4.Tohoku Univ, Grad Sch Agr Sci, Sendai, Japan

期刊名称：PLOS PATHOGENS （ 影响因子：6.7； 五年影响因子：6.7 ）

ISSN： 1553-7366

年卷期： 2023 年 19 卷 5 期

页码：

收录情况： SCI

摘要： Viruses are constantly subject to natural selection to enrich beneficial mutations and weed out deleterious ones. However, it remains unresolved as to how the phenotypic gains or losses brought about by these mutations cause the viral genomes carrying the very mutations to become more or less numerous. Previous investigations by us and others suggest that viruses with plus strand (+) RNA genomes may compel such selection by bottlenecking the replicating genome copies in each cell to low single digits. Nevertheless, it is unclear if similarly stringent reproductive bottlenecks also occur in cells invaded by DNA viruses. Here we investigated whether tomato yellow leaf curl virus (TYLCV), a small virus with a single-stranded DNA genome, underwent population bottlenecking in cells of its host plants. We engineered a TYLCV genome to produce two replicons that express green fluorescent protein and mCherry, respectively, in a replication-dependent manner. We found that among the cells entered by both replicons, less than 65% replicated both, whereas at least 35% replicated either of them alone. Further probability computation concluded that replication in an average cell was unlikely to have been initiated with more than three replicon genome copies. Furthermore, sequential inoculations unveiled strong mutual exclusions of these two replicons at the intracellular level. In conclusion, the intracellular population of the small DNA virus TYLCV is actively bottlenecked, and such bottlenecking may be a virus-encoded, evolutionarily conserved trait that assures timely selection of new mutations emerging through error-prone replication. An important unresolved issue in virus life cycles is how natural selection acts on individual virus copies occupying the same cell. Unlike cellular organisms in which a chromosome harboring an advantageous or deleterious mutation usually shares the hosting cells with no more than one homologous sister chromosome, viruses could potentially reproduce with numerous genome copies per cell, permitting sharing of protein products, thereby greatly diminishing phenotypic impacts of otherwise eventful mutations. Previous investigations suggest that (+) RNA viruses solve this problem by bottlenecking the number of replicating genome copies in each cell to low single digits. The current study reveals strikingly similar intracellular population bottlenecks for a small DNA virus. Further mechanistic interrogations could avail the virus-encoded bottleneck-enforcing apparatus as targets for antiviral therapy and prevention.

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