Potato leafroll virus in the aphid holobiont: Interactions shaping vector biology

Authors: PREISING, STEPHANIE - Cornell University; Heck, Michelle

Submitted to: Annual Review of Virology
Publication Type: Review Article
Publication Acceptance Date: 1/2/2025
Publication Date: 6/16/2025
Citation: Preising, S., Heck, M.L. 2025. Potato leafroll virus in the aphid holobiont: Interactions shaping vector biology. Annual Review of Virology. 12. https://doi.org/10.1146/annurev-virology-092623-103226.
DOI: https://doi.org/10.1146/annurev-virology-092623-103226

Interpretive Summary: Potato leafroll virus (PLRV) is a major threat to global potato production, causing significant yield losses and economic impact. This virus is transmitted exclusively by aphids, tiny insects that feed on plant sap. However, aphids are not just solitary insects—they exist as part of a complex community, or "holobiont," that includes bacteria and other microorganisms living inside them. Understanding how PLRV interacts with this holobiont is critical for developing new ways to manage the disease. Our research highlights how PLRV manipulates the biology of its aphid vector. Specifically, we found that PLRV affects the aphid's immune system and its interactions with other viruses that naturally infect aphids. This manipulation helps PLRV spread more effectively from plant to plant. Additionally, the virus alters the aphid's reproductive strategies, increasing the likelihood of winged aphids that can travel long distances to infect new plants. We also discovered that PLRV interacts with beneficial bacteria inside aphids, which are essential for aphid survival. By influencing these bacteria, PLRV changes how the aphids respond to stress and process nutrients. These findings reveal a previously unknown connection between plant viruses, their insect vectors, and the microbial communities within those insects. This review provides an overview of research on critical insights into the ecology of plant-virus-insect interactions and opens the door for innovative disease management strategies. For example, targeting the specific interactions between PLRV and aphid bacteria could lead to new ways to disrupt the virus's ability to spread, reducing its impact on potato crops without relying solely on chemical pesticides.

Technical Abstract: The aphid holobiont includes the aphid host and aphid-associated microorganisms, including plant pathogenic viruses. The polerovirus, potato leafroll virus (PLRV), is transmitted exclusively by aphids and is one of the most economically significant viruses infecting potatoes. In potato, PLRV infection results in stunting, leaf rolling, and net necrosis on tubers. PLRV threatens global potato cultivation, especially in regions where vector management options are limited. In this review, we delve into PLRV’s impact on the aphid holobiont and highlight literature showing the evolutionary and mechanistic ways in which PLRV influences the aphid holobiont during plant infection. We explore ideas to address the pressing need for aphid and PLRV management strategies by targeting interactions within the holobiont. Approaching PLRV-aphid interaction research through the lens of the holobiont allows a systems-level analysis of host, plant, and microbial effects that influence virus transmission - knowledge that can be leveraged to develop novel virus management strategies.