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

Abstract

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.

Plant paleopathology and the roles of pathogens and insects

“…Phytophagous hemipteran insects disproportionately transmit viruses, particularly as their elongate, stylate mouthparts are involved in piercing and sucking deep-seated plant tissues with the accompanying injection of viruses into plants (Uzest et al, 2007). One common entry point for plant viruses is the xylem and phloem of a host's vasculature, of which Barley Yellow Dwarf Disease is a prominent example (Table 1, Fig.…”

Evolution of Plant Viruses: Adaptation to Hosts and Vectors

“…However, there are recent break-through findings in mapping genetic loci controlling virus transmission in aphids (Gray et al, 2007) and identification of aphid receptors that interact with other viral proteins required for transmission (Uzest et al, 2007). Analysis of the CP sequences from a broad range of viruses suggests that the virus-vector interaction dominates over the virus-host interactions as a selective force in virus evolution (Chare and Holmes, 2004).…”

Plant virus transmission from the insect point of view

“…Uzest et al (1) found, by imaging using GVP-fused ATF and microscopy, that ATF binds to the very tip of the maxillary stylet (Fig. 1).…”

“…In this issue of PNAS, Uzest et al (1) tackle that problem and trace the receptor for the cauliflower mosaic virus (CaMV) movement protein to a protein imbedded into the chitin matrix at the tip of the stylet of the aphid vector.…”