![]() Indeed, all else being equal, the probability of infecting a host cell successfully, that is, the probability that all genome segments are transmitted in at least one copy, would be maximized if all segments occurred at equal frequency deviations from this situation would increase the cost of genome compartmentalization. One aspect of multipartite virus biology that has not been investigated, empirically or theoretically, is the potential regulation of the relative frequencies of different genome segments. This cost increases dramatically with the number of segments constituting the viral genome, as amply discussed in the related literature, and recently reinvestigated in a theoretical study 12. Proposed advantages of genome compartmentalization are greater stability of smaller-sized segments 3, a potential faster replication of small genomic segments 4, or the increased genome shuffling that could result from genome segmentation and ‘multipartitism’ 5, 6, 7, 8, 9, 10.Īn obvious cost to genome compartmentalization is the necessity to either package together all segments, for segmented viruses, or to ensure the co-entry of an ensemble of virus particles containing at least one copy of each genomic segment 3, 6, 11, for multipartite viruses. The functioning of these biological systems has long intrigued virologists and evolutionary biologists, who have striven to understand how such systems have evolved by modelling the parametric space in which the cost/benefit ratio is positive. Among the segmented viruses, the most puzzling biological systems are found in the multipartite viruses 2 (described in plants and fungi), where the genome segments are not co-packaged in a single viral particle but are encapsidated individually, forming an ensemble of particles that must be transmitted together in order to infect new cells. Within this diversity, the so-called segmented viruses-DNA or RNA viruses infecting bacteria, animals or plants 1-have a genome composed of more than one nucleic acid molecule, with 2 to 12 genome segments depending on the viral species. Viral genomes can be composed of single- or double-stranded molecules of RNA or DNA, expressing genes from mono- or polycistronic mRNAs, which can be sub-genomic or full-genome-length mRNAs. Viruses exhibit a wide diversity of genome organizations, mechanisms of replication and gene expression strategies. We propose that the differential control of gene/segment copy number may represent an unforeseen benefit for multipartite viruses, which may compensate for the extra costs induced by the low-frequency segments. ![]() Earlier proposed benefits of viral genome segmentation do not depend on the segments’ frequency and cannot explain our observations. We further show that the relative frequency of viral genes impacts both viral accumulation and symptom expression, and changes specifically in different hosts. We show that some viral genes accumulate at low frequency, whereas others dominate. Here, we investigate the segment frequency-related cost by monitoring the copy number of the eight single-gene segments composing the genome of a plant nanovirus. An evident cost for these viral systems, particularly if some segments are rare, is the difficulty of gathering one copy of each segment to ensure infection. Multipartite viruses have a genome divided into several nucleic acid segments, each encapsidated separately.
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