Poleroviruses are restricted to vascular phloem tissues from which they are transmitted by their aphid vectors and are not transmissible mechanically. Phloem limitation has been attributed to the absence of virus proteins either facilitating movement or counteracting plant defense. The polerovirus capsid is composed of two forms of coat protein, the major P3 protein and the minor P3/P5 protein, a translational readthrough of P3. P3/P5 is required for insect transmission and acts in trans to facilitate long-distance virus movement in phloem tissue. Specific potato leafroll virus mutants lacking part or all of the P5 domain moved into and infected nonvascular mesophyll tissue when the source-sink relationship of the plant (Solanum sarrachoides) was altered by pruning, with the progeny virus now being transmissible mechanically. However, in a period of months, a phloem-specific distribution of the virus was reestablished in the absence of aphid transmission. Virus from the new phloem-limited infection showed compensatory mutations that would be expected to restore the production of full-length P3/P5 as well as the loss of mechanical transmissibility. The data support our hypothesis that phloem limitation in poleroviruses presumably does not result from a deficiency in the repertoire of virus genes but rather results from P3/P5 accumulation under selection in the infected plant, with the colateral effect of facilitating transmission by phloem-feeding aphid vectors.
Members of the Luteoviridae are transmitted by aphids in a circulative, nonpropagative manner that requires the virus to be acquired through gut tissue into the aphid hemocoel and then exit through salivary tissues. This process is aphid species-specific and involves specific recognition of the virus by unidentified components on the membranes of gut and salivary tissues. Transport through the tissues is an endocytosis/exocytosis process. Both structural proteins of the virus are involved in the transmission process, with multiple protein domains regulating the movement and survival of the virus in the aphid and plant. Here we review what is known about the genetic, cellular, and molecular mechanisms regulating these complex and specific virus-aphid interactions.
The coat protein (CP) of potato leafroll virus (PLRV) is the primary component of the capsid, and is a multifunctional protein known to be involved in vector transmission and virus movement within plant hosts, in addition to particle assembly. Thirteen mutations were generated in various regions of the CP and tested for their ability to affect virus-host and virus-vector interactions. Nine of the mutations prevented the assembly of stable virions. These mutants were unable to infect systemically four different host species. Furthermore, although virus replication and translation of the CP were similar for the mutants and wild-type virus in individual plant cells, the translation of the CP readthrough product was affected in several of the mutants. Four of the mutants were able to assemble stable particles and infect host plants systemically, similarly to the wild-type virus; however, two of the mutants were transmitted less efficiently by aphid vectors. Based on a computer-generated model of the PLRV CP, the mutations that prevented virion assembly were associated with subunit interfaces, while the amino acid alterations in the assembly-competent mutants were associated with surface loops. This and previous work indicates that the CP structural model has value in predicting the structural architecture of the virion.
Cereal yellow dwarf virus-RPV (CYDV-RPV) is transmitted specifically by the aphids Rhopalosiphum padi andSchizaphis graminum in a circulative nonpropagative manner. The high level of vector specificity results from the vector aphids having the functional components of the receptor-mediated endocytotic pathways to allow virus to transverse the gut and salivary tissues. Studies of F 2 progeny from crosses of vector and nonvector genotypes of S. graminum showed that virus transmission efficiency is a heritable trait regulated by multiple genes acting in an additive fashion and that gut-and salivary gland-associated factors are not genetically linked. Utilizing two-dimensional difference gel electrophoresis to compare the proteomes of vector and nonvector parental and F 2 genotypes, four aphid proteins (S4, S8, S29, and S405) were specifically associated with the ability of S. graminum to transmit CYDV-RPV. The four proteins were coimmunoprecipitated with purified RPV, indicating that the aphid proteins are capable of binding to virus. Analysis by mass spectrometry identified S4 as a luciferase and S29 as a cyclophilin, both of which have been implicated in macromolecular transport. Proteins S8 and S405 were not identified from available databases. Study of this unique genetic system coupled with proteomic analysis indicated that these four virus-binding aphid proteins were specifically inherited and conserved in different generations of vector genotypes and suggests that they play a major role in regulating polerovirus transmission.Viruses in the family Luteoviridae, including Barley yellow dwarf virus (BYDV), Cereal yellow dwarf virus (CYDV), Potato leafroll virus, and Beet western yellows virus, are collectively referred to in this paper as luteovirids. They are transmitted in a circulative persistent nonpropagative manner only by aphids (Aphididae: Hemiptera) (20). Ultrastructural studies indicate that all luteovirids follow a similar pathway through their aphid vectors (12). Aphids acquire the viruses from infected phloem cells while feeding with their piercing-sucking stylets. Virions are drawn up the food canal of the stylets and into the gut lumen within the aphid. Subsequently, virions traverse the lining of the midgut, hindgut, or both (7,8,25) and are released into the body cavity (hemocoel) to circulate in the hemolymph. Virions suspended in hemolymph that contact the paired accessory salivary glands (ASG) are actively transported by endocytosis into the ASG cells and then transported into the salivary duct to be transmitted into potential host plants. Interestingly, each luteovirid species is transmitted most efficiently only by a specific set of aphid species or populations within an aphid species, thus demonstrating a high level of vector specificity. The cellular mechanisms responsible for vector specificity are regulated by distinct interactions between the two virus structural proteins and unknown proteins in the aphid (12).The discovery of Gildow and Rochow (9) that competition occurred between se...
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