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.

The promises and challenges of research on plant–insect–microbe interactions

“…They also play a crucial role in more complex plant–microbe–insect vector interactions. For instance, depending on their transmission mode, viruses have evolved specific ways in which they manipulate VOCs and other plants traits to enhance their transmission by insect vectors (Mauck et al ., , Dáder et al ., ). Understanding the full interplay of how each of these three partners manipulates and responds to the other two in such vectored plant disease systems is perhaps the biggest challenge of all (Webster et al ., ; Zhou et al ., ).…”

“…Dáder et al . () compiled a large amount of published studies on plant pathogenic viruses and their interaction with host plants and described the transmission cycle of the viruses from the molecular level to the ecological level. Interestingly, many viruses are reported to alter infected plants and/or vectoring insects and influence the outcome of virus transmission.…”

“…This suggests that the modified CK profile in the infected plant tissue is the consequence of active hijacking of plant tissues by insect-bacteria system rather than a plant response to insect feeding, and reveals the important role of CK in the interaction of three organisms. Dáder et al (2017) compiled a large amount of published studies on plant pathogenic viruses and their interaction with host plants and described the transmission cycle of the viruses from the molecular level to the ecological level. Interestingly, many viruses are reported to alter infected plants and/or vectoring insects and influence the outcome of virus transmission.…”

Impact of Mutations in Arabidopsis thaliana Metabolic Pathways on Polerovirus Accumulation, Aphid Performance, and Feeding Behavior

“…Virus particles are then transported through the intestinal cells and released in the hemolymph. Finally, polerovirus particles cross the salivary gland cells and are released together with saliva into a new plant host during a subsequent feeding event [18].There is growing evidence that aphid-transmitted viruses can affect plant phenotypes and vector behaviors in ways that may ultimately facilitate virus acquisition and inoculation [19,20]. This concept of plant and aphid "manipulation" by the virus also applies to viruses in the Luteoviridae family.…”

“…There is growing evidence that aphid-transmitted viruses can affect plant phenotypes and vector behaviors in ways that may ultimately facilitate virus acquisition and inoculation [19,20]. This concept of plant and aphid "manipulation" by the virus also applies to viruses in the Luteoviridae family.…”