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

Abstract

Single-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.

Alfalfa leaf curl virus is efficiently acquired by its aphid vector Aphis craccivora but inefficiently transmitted

“…This study, together with previous results [10, 40], shows that barriers to gut exit or post-gut barriers were responsible not only for the non-transmission of ALCV by a non-vector population of A. craccivora but also for the low transmission of the vector population tested here. Interestingly, such barriers were detected in other virus–insect combinations in association with transmission defects.…”

“…This decrease may be due to hindrance to virus flow from the gut to these compartments and/or degradation of viral DNA in these post-gut compartments due to insect-defence mechanisms such as autophagy, already described in the whitefly B. tabaci for TYLCV [76, 77]. Based on a recent report, the excretion from the salivary glands is not expected to account for much of the virus decrease in the post-gut compartments [40]. Indeed, using the same Robinia population of A. craccivora as here and a nanovirus clone of faba bean necrotic stunt virus (FBNSV), this study showed that although the accumulation of the two viruses were similar in the head compartment, the excretion of ALCV was far lower than that of FBNSV.…”

“…ALCV was also tested for a possible impact on the fitness of the aphid vector and for vertical transmission. Particular attention was given to transmission efficiency because previous results showed that it was relatively low compared to other CNP viruses [10,40].…”

Vector acquisition and co-inoculation of two plant viruses influences transmission, infection, and replication in new hosts

“…Co-infections of plant viruses can be propagated by vectors that acquired virions from co-infected plants, sequentially from singly infected plants, or by multiple vector individuals that acquired different viruses. Vector acquisition of two viruses does not ensure both will be transmitted, and the presence of two viruses can alter transmission rates of one or both viruses 4,10,11,22–32,34–41,48–51 . Once acquired, two viruses may compete for binding sites required for retention in and transmission from their vectors 6,29,33,37,49,52 .…”

“…Once acquired, two viruses may compete for binding sites required for retention in and transmission from their vectors 6,29,33,37,49,52 . Order of acquisition sometimes has an antagonistic effect on virus transmission 4,10,34,36,38 and does not always benefit the virus acquired first 22,30,36 . Vector-plant interactions that occur during probing and feeding events can also induce host plant defenses that mediate infection dynamics.…”