Insect transmission of plant viruses: Multilayered interactions optimize viral propagation

Abstract By serving as vectors of transmission, insects play a key role in the infection cycle of many plant viruses. Viruses use sophisticated transmission strategies to overcome the spatial barrier separating plants and the impediment imposed by the plant cell wall. Interactions among insect vectors, viruses, and host plants mediate transmission by integrating all organizational levels, from molecules to populations. Best‐examined on the molecular scale are two basic transmission modes wherein virus–vector interactions have been well characterized. Whereas association of virus particles with specific sites in the vector's mouthparts or in alimentary tract regions immediately posterior to them is required for noncirculative transmission, the cycle of particles through the vector body is necessary for circulative transmission. Virus transmission is also determined by interactions that are associated with changes in vector feeding behaviors and with alterations in plant host's morphology and/or metabolism that favor the attraction or deterrence of vectors. A recent concept in virus–host–vector interactions proposes that when vectors land on infected plants, vector elicitors and effectors “inform” the plants of the confluence of interacting entities and trigger signaling pathways and plant defenses. Simultaneously, the plant responses may also influence virus acquisition and inoculation by vectors. Overall, a picture is emerging where transmission depends on multilayered virus–vector–host interactions that define the route of a virus through the vector, and on the manipulation of the host and the vector. These interactions guarantee virus propagation until one or more of the interactants undergo changes through evolution or are halted by environmental interventions.