The acquisition of a caulimovirus by different aphid species: comparison with a potyvirus

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.

Section: Discussionsupporting

confidence: 73%

Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector

Drucker

Froissart

Hébrard

et al. 2002

“…Although poorly efficient CaMV vector species have been reported, none of Ͼ30 aphid species tested thus far are strict CaMV nontransmitters (5,(10)(11)(12). While surveying P2-GFP binding to additional aphid species, a total absence of labeling was observed on 31 maxillary stylets from Acyrthosiphon lactucae (Fig.…”

Section: P2 Binding At the Tip Of The Maxillary Stylets Is Required Fmentioning

confidence: 99%

A protein key to plant virus transmission at the tip of the insect vector stylet

Uzest

Gargani

Drucker

et al. 2007

169

130

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.

“…Virions of these viruses are noncirculative and are retained or, in the case of CMV, thought to be retained on the stylets, but they differ in other regards. CMV and potyviruses are nonpersistently transmitted, with transmission occurring in seconds to minutes after acquisition (7), whereas CaMV is considered to be semipersistently transmitted, with transmission continuing over hours or days after acquisition (29). In contrast, all other semipersistently transmitted viruses whose retention sites have been investigated previously are retained in the foreguts of their vectors-the aphid-transmitted Anthriscus yellows virus (AYV) and Parsnip yellow fleck virus (PYFV) (17), and the leafhoppertransmitted Maize chlorotic dwarf virus (MCDV) (15,16).…”

Section: Discussionmentioning

confidence: 99%

A virus capsid component mediates virion retention and transmission by its insect vector

Chen¹,

Walker²,

Carter

et al. 2011

101

119

Numerous pathogens of humans, animals, and plants are transmitted by specific arthropod vectors. However, understanding the mechanisms governing these pathogen-vector interactions is hampered, in part, by the lack of easy-to-use analytical tools. We investigated whitefly transmission of Lettuce infectious yellows virus (LIYV) by using a unique immunofluorescent localization approach in which we fed virions or recombinant virus capsid components to whiteflies, followed by feeding them antibodies to the virions or capsid components, respectively. Fluorescent signals, indicating the retention of virions, were localized in the anterior foregut or cibarium of a whitefly vector biotype but not within those of a whitefly nonvector biotype. Retention of virions in these locations strongly corresponded with the whitefly vector transmission of LIYV. When four recombinant LIYV capsid components were individually fed to whitefly vectors, significantly more whiteflies retained the recombinant minor coat protein (CPm). As demonstrated previously and in the present study, whitefly vectors failed to transmit virions preincubated with anti-CPm antibodies but transmitted virions preincubated with antibodies recognizing the major coat protein (CP). Correspondingly, the number of insects that specifically retained virions preincubated with antiCPm antibodies were significantly reduced compared with those that specifically retained virions preincubated with anti-CP antibodies. Notably, a transmission-defective CPm mutant was deficient in specific virion retention, whereas the CPm-restored virus showed WT levels of specific virion retention and transmission. These data provide strong evidence that transmission of LIYV is determined by a CPm-mediated virion retention mechanism in the anterior foregut or cibarium of whitefly vectors.arthropod vector transmission | crinivirus | noncirculative transmission | semipersistent transmission | Bemisia tabaci