Summary auto-generated
This study examined how the accessory salivary gland (ASG) basal lamina regulates barley yellow dwarf luteovirus (BYDV) transmission by aphids. Researchers microinjected five aphid species with purified BYDV isolates (RPV, PAV, and MAV) and used transmission electron microscopy to visualize virus-basal lamina interactions. Results revealed that BYDV particles specifically associate with the ASG basal lamina of vector species but not non-vector species. For example, PAV and RPV particles never associated with Rhopalosiphum maidis basal laminae, while they readily penetrated those of Rhopalosiphum padi and Sitobion avenae. Notably, in S. avenae, RPV accumulated in the basal lamina but failed to penetrate the plasmalemma, preventing transmission—indicating separate mechanisms control each barrier. In vitro experiments with charged and differently-sized colloidal gold particles revealed the basal lamina has a net negative charge and a size exclusion limit of approximately 20 nm based on charge interactions. Dissected salivary gland experiments confirmed MAV specifically attached only to S. avenae basal laminae, not R. maidis, suggesting recognition involves specific basal lamina components. These findings demonstrate that luteovirus transmission specificity involves two independent mechanisms: selective virus attachment to basal lamina and charge-dependent penetration through it.
Key findings
- BYDV attachment to and penetration of the ASG basal lamina are virus-species and aphid-species specific, with different isolates showing distinct interaction patterns with different aphid species
- The basal lamina and plasmalemma represent independent selective barriers; viruses can penetrate one but not the other, with transmission requiring passage through both
- The ASG basal lamina has a net negative charge and functions as a molecular sieve with size-exclusion limits (~20 nm) that depend on particle charge, allowing small anionic particles to penetrate while blocking cationic particles
- Non-aphid-transmitted viruses like cowpea mosaic virus do not specifically associate with the ASG basal lamina, indicating the interaction is specific to luteoviruses
- In vitro dissected salivary gland experiments confirmed that virus-basal lamina attachment is reproducible without intact insect physiology, suggesting recognition involves specific molecular components in the basal lamina
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Abstract
Barley yellow dwarf luteovirus (BYDV) particles are transmitted by aphids in a species-specific manner. Transmission to plants requires that the virus particles be transported across the basal lamina and plasmalemma of the accessory salivary gland (ASG). To characterize the role of the ASG basal lamina in regulating BYDV transmission, five aphid species were microinjected with purified New York isolates BYDV- PAV or -RPV. Both viruses associated specifically only with the ASG basal lamina. The ability of virions to penetrate the basal lamina was separate from the ability to penetrate the plasmalemma. When the salivary glands of vector, Sitobion avenae, or non-vector, Rhopalosiphum maidis, aphids were incubated in vitro with New York isolate BYDV-MAV, virions only attached to the ASG basal lamina of S. avenae. When anionic and cationic ferritin were microinjected into aphids, only cationic ferritin aggregated on the surface of the ASG basal lamina and at openings of plasmalemma invaginations into the cytoplasm, suggesting that these sites had a net negative charge. In vitro studies of anionic and cationic gold penetration of ASG basal laminae indicated a macromolecular size exclusion limit of approximately 20 nm that depended on charge. Anionic gold particles did not accumulate in the basal lamina as densely as the 25 nm BYDV particles, suggesting that the virus particles have a greater affinity for the ASG basal lamina. These results indicate that both the ASG basal lamina and plasmalemma contain specific components independently involved in the recognition and transmission of luteoviruses.