The intriguing success of helper components in vector-transmission of plant viruses.

International audienceAn intriguing aspect of vector-transmission of plant viruses is the frequent involvement of a helper component (HC). HCs are virus-encoded non-structural proteins produced in infected plant cells that are mandatory for the transmission success. Over five decades, all data collected on HCs from unrelated viral species transmitted by distinct vector species were consistent with a unique mode of action designated “the bridge hypothesis”: the HC has two functional domains, one binding the virus particle and the other binding a putative receptor in the vector, creating a reversible molecular bridge between the two. This hypothesis appeared fully satisfactory as HCs were reported solely in viruses transmitted non-circulatively -- i.e. the virus particle binds externally to the mouthpart of its vector, and can later be released therefrom and inoculated. Recently, however, HCs have also been reported in viruses transmitted circulatively, where the virus particles are internalized in gut cells and cycle within the body to reach the salivary glands. In this more complex scheme of virus-vector interaction, a simple mode of action of HC compatible with the bridge hypothesis becomes questionable. In addition, while it had consistently been shown that the sequential acquisition of HC and virus particles could only work when HC was acquired first, a recent report shows that the reverse acquisition sequence can work in some case, again questioning the bridge hypothesis as a universal mode of action. Because of the importance of HC molecules in the vector-transmission of plant viruses, we here propose an exhaustive review of the field, of its historical perspective and most recent development

The lifestyle of a multipartite virus challenges major paradigms in Virology

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Gene copy number variation impacts on gene expression in a multipartite virus

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Nonconcomitant host-to-host transmission of multipartite virus genome segments may lead to complete genome reconstitution

International audienceBecause multipartite viruses package their genome segments in different viral particles, they face a potentially huge cost if the entire genomic information, i.e., all genome segments, needs to be present concomitantly for the infection to function. Previous work with the octapartite faba bean necrotic stunt virus (FBNSV; family Nanoviridae , genus Nanovirus ) showed that this issue can be resolved at the within-host level through a supracellular functioning; all viral segments do not need to be present within the same host cell but may complement each other through intercellular trafficking of their products (protein or messenger RNA [mRNA]). Here, we report on whether FBNSV can as well decrease the genomic integrity cost during between-host transmission. Using viable infections lacking nonessential virus segments, we show that full-genome infections can be reconstituted and function through separate acquisition and/or inoculation of complementary sets of genome segments in recipient hosts. This separate acquisition/inoculation can occur either through the transmission of different segment sets by different individual aphid vectors or by the sequential acquisition by the same aphid of complementary sets of segments from different hosts. The possibility of a separate between-host transmission of different genome segments thus offers a way to at least partially resolve the genomic maintenance problem faced by multipartite viruses

On the mechanisms of circulative non-propagative transmission of nanoviruses

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Gene copy number variations at the within-host population level modulate gene expression in a multipartite virus

International audienceMultipartite viruses have a segmented genome, with each segment encapsidated separately. In all multipartite virus species for which the question has been addressed, the distinct segments reproducibly accumulate at a specific and host-dependent relative frequency, defined as the ‘genome formula’. Here, we test the hypothesis that the multipartite genome organization facilitates the regulation of gene expression via changes of the genome formula and thus via gene copy number variations. In a first experiment, the faba bean necrotic stunt virus (FBNSV), whose genome is composed of eight DNA segments each encoding a single gene, was inoculated into faba bean or alfalfa host plants, and the relative concentrations of the DNA segments and their corresponding messenger RNAs (mRNAs) were monitored. In each of the two host species, our analysis consistently showed that the genome formula variations modulate gene expression, the concentration of each genome segment linearly and positively correlating to that of its cognate mRNA but not of the others. In a second experiment, twenty parallel FBNSV lines were transferred from faba bean to alfalfa plants. Upon host switching, the transcription rate of some genome segments changes, but the genome formula is modified in a way that compensates for these changes and maintains a similar ratio between the various viral mRNAs. Interestingly, a deep-sequencing analysis of these twenty FBNSV lineages demonstrated that the host-related genome formula shift operates independently of DNA-segment sequence mutation. Together, our results indicate that nanoviruses are plastic genetic systems, able to transiently adjust gene expression at the population level in changing environments, by modulating the copy number but not the sequence of each of their genes

Co-Acquired Nanovirus and Geminivirus Exhibit a Contrasted Localization within Their Common Aphid Vector

International audienceSingle-stranded DNA (ssDNA) plant viruses belong to the families Geminiviridae and Nanoviridae. They are transmitted by Hemipteran insects in a circulative, mostly non-propagative, manner. While geminiviruses are transmitted by leafhoppers, treehoppers, whiteflies and aphids, nanoviruses are transmitted exclusively by aphids. Circulative transmission involves complex virus-vector interactions in which epithelial cells have to be crossed and defense mechanisms counteracted. Vector taxa are considered a relevant taxonomic criterion for virus classification, indicating that viruses can evolve specific interactions with their vectors. Thus, we predicted that, although nanoviruses and geminiviruses represent related viral families, they have evolved distinct interactions with their vector. This prediction is also supported by the non-structural Nuclear Shuttle Protein (NSP) that is involved in vector transmission in nanoviruses but has no similar function in geminiviruses. Thanks to the recent discovery of aphid-transmitted geminiviruses, this prediction could be tested for the geminivirus alfalfa leaf curl virus (ALCV) and the nanovirus faba bean necrotic stunt virus (FBNSV) in their common vector, Aphis craccivora. Estimations of viral load in midgut and head of aphids, precise localization of viral DNA in cells of insect vectors and host plants, and virus transmission tests revealed that the pathway of the two viruses across the body of their common vector differs both quantitatively and qualitatively

A mulicellular lifestyle for a multipartite virus

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