BackgroundThe prevailing paradigm of host-parasite evolution is that arms races lead to increasing specialisation via genetic adaptation. Insect herbivores are no exception and the majority have evolved to colonise a small number of closely related host species. Remarkably, the green peach aphid, Myzus persicae, colonises plant species across 40 families and single M. persicae clonal lineages can colonise distantly related plants. This remarkable ability makes M. persicae a highly destructive pest of many important crop species.ResultsTo investigate the exceptional phenotypic plasticity of M. persicae, we sequenced the M. persicae genome and assessed how one clonal lineage responds to host plant species of different families. We show that genetically identical individuals are able to colonise distantly related host species through the differential regulation of genes belonging to aphid-expanded gene families. Multigene clusters collectively upregulate in single aphids within two days upon host switch. Furthermore, we demonstrate the functional significance of this rapid transcriptional change using RNA interference (RNAi)-mediated knock-down of genes belonging to the cathepsin B gene family. Knock-down of cathepsin B genes reduced aphid fitness, but only on the host that induced upregulation of these genes.ConclusionsPrevious research has focused on the role of genetic adaptation of parasites to their hosts. Here we show that the generalist aphid pest M. persicae is able to colonise diverse host plant species in the absence of genetic specialisation. This is achieved through rapid transcriptional plasticity of genes that have duplicated during aphid evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1145-3) contains supplementary material, which is available to authorized users.

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aphid ͉ receptor N early all plant viruses that cause extensive agricultural damage use specific vectors to spread between hosts. The most common vectors are arthropods, especially aphids (1), and the most widely adopted strategy for virus-vector interaction is noncirculative transmission, in which the virus is taken up by a vector feeding on an infected plant, adsorbed somewhere on the cuticle lining the inner part of the feeding apparatus, and subsequently released to inoculate a new host plant. The viral components involved in this interaction are relatively well established, in particular for the genus Cucumovirus, where domains of the coat protein directly recognize unknown retention sites in the vector mouthparts (capsid strategy), and for the genera Potyvirus and Caulimovirus, where a nonstructural viral protein, HC (helper component), creates the link between virion and vector (helper strategy) (reviewed in refs. 2 and 3). However, no putative binding sites for viral components in the insect vector have ever been chemically characterized or even precisely localized. This question is of major importance, because numerous noncirculative viruses may use the same vector attachment sites, and identification of putative receptor molecules could lead to new strategies to combat viral spread.A distinguishing feature of noncirculative transmission is that several virus species can be transmitted by the same vector, and, conversely, several vector species can transmit the same virus. Hence, although some degree of noncirculative virus/vector specificity exists (4, 5), it is often so broad that the very existence of actual viral receptors remains questionable, because their existence has never been directly demonstrated.Here we report evidence for the existence, precise location, and chemical nature of the receptor for a noncirculative virus, cauliflower mosaic virus (CaMV), in its insect vector. A novel in vitro system allowed rapid visualization of the interaction between dissected aphid stylets and the HC of CaMV. The CaMV retention sites are concentrated exclusively in a tiny and previously unknown anatomical zone located at the extreme tip of the aphid maxillary stylets. Virus/vector binding at this specific zone is mandatory for successful CaMV transmission. Pretreatment of dissected stylets with various chemicals and enzymes demonstrated that the molecule used by CaMV as a specific receptor for vector transmission is a nonglycosylated protein deeply embedded in the chitin matrix.

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Most noncirculative plant viruses transmitted by insect vectors bind to their mouthparts. They are acquired and inoculated within seconds when insects hop from plant to plant. The receptors involved remain totally elusive due to a long-standing technical bottleneck in working with insect cuticle. Here we characterize the role of the two first cuticular proteins ever identified in arthropod mouthparts. A domain of these proteins is directly accessible at the surface of the cuticle of the acrostyle, an organ at the tip of aphid stylets. The acrostyle has been shown to bind a plant virus, and we consistently demonstrated that one of the identified proteins is involved in viral transmission. Our findings provide an approach to identify proteins in insect mouthparts and point at an unprecedented gene candidate for a plant virus receptor.

Interactions between Cauliflower mosaic virus (CaMV) and its aphid vector are regulated by the viral protein P2, which binds to the aphid stylets, and protein P3, which bridges P2 and virions. By using baculovirus expression of P2 and P3, electron microscopy, surface plasmon resonance, affinity chromatography, and transmission assays, we demonstrate that P3 must be previously bound to virions in order that attachment to P2 will allow aphid transmission of CaMV. We also show that a P2:P3 complex exists in the absence of virions but is nonfunctional in transmission. Hence, unlike P2, P3 and virions cannot be sequentially acquired by the vector. Immunogold labeling revealed the predominance of spatially separated P2:P3 and P3:virion complexes in infected plant cells. This specific distribution indicates that the transmissible complex, P2:P3:virion, does not form primarily in infected plants but in aphids. A model, describing the regulating role of P3 in the formation of the transmissible CaMV complex in planta and during acquisition by aphids, is presented, and its consequences are discussed.

The mechanisms and impacts of the transmission of plant viruses by insect vectors have been studied for more than a century. The virus route within the insect vector is amply documented in many cases, but the identity, the biochemical properties, and the structure of the actual molecules (or molecule domains) ensuring compatibility between them remain obscure. Increased efforts are required both to identify receptors of plant viruses at various sites in the vector body and to design competing compounds capable of hindering transmission. Recent trends in the field are opening questions on the diversity and sophistication of viral adaptations that optimize transmission, from the manipulation of plants and vectors ultimately increasing the chances of acquisition and inoculation, to specific "sensing" of the vector by the virus while still in the host plant and the subsequent transition to a transmission-enhanced state.

Viral recombination can dramatically impact evolution and epidemiology. In viruses, the recombination rate depends on the frequency of genetic exchange between different viral genomes within an infected host cell and on the frequency at which such co-infections occur. While the recombination rate has been recently evaluated in experimentally co-infected cell cultures for several viruses, direct quantification at the most biologically significant level, that of a host infection, is still lacking. This study fills this gap using the cauliflower mosaic virus as a model. We distributed four neutral markers along the viral genome, and co-inoculated host plants with marker-containing and wild-type viruses. The frequency of recombinant genomes was evaluated 21 d post-inoculation. On average, over 50% of viral genomes recovered after a single host infection were recombinants, clearly indicating that recombination is very frequent in this virus. Estimates of the recombination rate show that all regions of the genome are equally affected by this process. Assuming that ten viral replication cycles occurred during our experiment—based on data on the timing of coat protein detection—the per base and replication cycle recombination rate was on the order of 2 × 10−5 to 4 × 10−5. This first determination of a virus recombination rate during a single multi-cellular host infection indicates that recombination is very frequent in the everyday life of this virus.