Natural selection acts on cellular organisms by ensuring the genes responsible for an advantageous phenotype consistently reap the phenotypic advantage. This is possible because reproductive cells of these organisms are almost always haploid, separating the beneficial gene from its rival allele at every generation. How natural selection acts on plus-strand RNA viruses is unclear because these viruses frequently load host cells with numerous genome copies and replicate thousands of progeny genomes in each cell. Recent studies suggest that these viruses encode the Bottleneck, Isolate, Amplify, Select (BIAS) mechanism that blocks all but a few viral genome copies from replication, thus creating the environment in which the bottleneck-escaping viral genome copies are isolated from each other, allowing natural selection to reward beneficial mutations and purge lethal errors. This BIAS mechanism also blocks the genomes of highly homologous superinfecting viruses, thus explaining cellular-level superinfection exclusion. Expected final online publication date for the Annual Review of Virology, Volume 9 is September 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Myzus persicae (Sulzer), commonly known as the green peach aphid, is a notorious pest that causes substantial losses to a range of crops and can transmit several plant viruses, including potato virus Y (PVY). Chemical insecticides provide only partial control of this pest and their use is not environmentally sustainable. In recent years, many genes related to growth, development, and reproduction have been used as targets for pest control. These include Gustavus (Gus), a highly conserved gene that has been reported to play an essential part in the genesis of germline cells and, hence, in fecundity in the model insect Drosophila melanogaster. We hypothesized that the Gustavus (Gus) gene was a potential target that could be used to regulate the M. persicae population. In this study, we report the first investigation of an ortholog of Gus in M. persicae, designated MpGus, and describe its role in the fecundity of this insect. First, we identified the MpGus mRNA sequence in the M. persicae transcriptome database, verified its identity with reverse transcription-polymerase chain reaction (RT-PCR), and then evaluated the transcription levels of MpGus in M. persicae nymphs of different instars and tissues with real-time quantitative PCR (RT-qPCR). To investigate its role in regulating the fecundity of M. persicae, we used RNA interference (RNAi) to silence the expression of MpGus in adult insects; this resulted in a significant reduction in the number of embryos (50.6%, P < 0.01) and newborn nymphs (55.7%, P < 0.01) in the treated aphids compared with controls. Interestingly, MpGus was also significantly downregulated in aphids fed on tobacco plants that had been pre-infected with PVYN, concomitant with a significant reduction (34.1%, P < 0.01) in M. persicae fecundity. Collectively, these data highlight the important role of MpGus in regulating fecundity in M. persicae and indicate that MpGus is a promising RNAi target gene for control of this pest species.
Cellular organisms purge lethal mutations as they occur (in haploids), or as soon as they become homozygous (in sexually reproducing diploids), thus making the mutation-carrying genomes the sole victims of lethality. How lethal mutations in viruses are purged remains an unresolved question because numerous viral genomes could potentially replicate in the same cell, sharing their encoded proteins, hence shielding lethal mutations from selection. 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. However, it is unclear if similar 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 the TYLCV genome to produce two replicons that express green fluorescent protein and mCherry, respectively, in a replication-dependent manner. We found that less than 65% of cells penetrated by both replicons replicated both, whereas at least 35% of cells replicated either of them alone, illustrating an intracellular population bottleneck size of no more than three. Furthermore, sequential inoculations unveiled strong mutual exclusions of these two replicons in most cells. Collectively our data demonstrated for the first time that DNA viruses like TYLCV are subject to stringent intracellular population bottlenecks, suggesting that such population bottlenecks may be a virus-encoded, evolutionarily conserved trait that assures timely elimination of lethal mutations.
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.
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