Circulative, “Nonpropagative” Virus Transmission: An orchestra of virus, insect and plant derived instruments

Authors: Gray, Stewart; Heck, Michelle; GHANIM, MURAD - Volcani Center (ARO)

Submitted to: Advances in Virus Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/28/2014
Publication Date: 4/1/2014
Citation: Gray, S.M., Cilia, M., Ghanim, M. 2014. Circulative, “Nonpropagative” Virus Transmission: An orchestra of virus, insect and plant derived instruments. Advances in Virus Research. 89:141-99.

Interpretive Summary: Insects such as aphids and whiteflies use their piercing-sucking mouthparts to feed on the vascular tissues of plants. Although their feeding can directly damage plants, a more important problem is that during their feeding they can transmit plant viruses that cause disease leading to significant crop yield and quality losses. One mode of virus spread, called circulative transmission, requires the insect to feed on a virus-infected plant for several hours to ingest virus and then have the virus circulate through the body of the insect. This is required before the insect can spread virus to a new plant. This paper is a comprehensive treatise of decades of research conducted in our laboratories and those of colleagues around the globe on the subject of circulative transmission of plant viruses. While aphids and whiteflies differ in the specifics of anatomy and physiology as it pertains to virus transmission, they share many commonalities in the actual mechanisms of how the plant viruses circulate through the insect and are transmitted to new plants. For example, many of the insect proteins that interact with virus and facilitate transmission are similar in both aphids and whiteflies. Similarly, both types of insects harbor bacteria that also play a role in virus transmission. Finally, the circulative viruses can directly and indirectly manipulate the plant and the insect to better ensure the virus is transmitted to new host plants. These commonalities can be exploited to provide the means to develop virus disease control strategies that are useful for many different virus diseases affecting many different crops. Many of the unifying principles described in this paper apply to all insects that transmit viruses in a circulative manner, even those insects that transmit animal viruses.

Technical Abstract: The many species of plant viruses within the Luteoviridae, Geminiviridae and Nanoviridae are all transmitted by phloem feeding insects in a circulative, nonpropagative manner. The precise route of virus movement through the vector can differ across and within virus families, but these viruses all share many biological, biochemical and ecological features. All share temporal and spatial constraints with respect to transmission efficiency. The viruses also induce physiological changes in their plant hosts resulting in behavioral changes in the insects that optimize the transmission of virus to new hosts. Virus proteins interact with insect, endosymbiont and plant proteins to orchestrate directly and indirectly virus movement in insects and plants to facilitate transmission. Knowledge of these complex interactions allows for the development of new tools to reduce or prevent transmission, to quickly identify important vector populations, and to improve the management of these economically important viruses affecting agricultural and natural plant populations.