Viral silencing suppressor activity in plants modifies aphid antiviral immunity and fecundity

Authors: PREISING, STEPHANIE - Cornell University; Wilson, Jennifer; PARKER, GLENN - Cornell University; Deblasio, Stacy; Reeve, Domenica; Chappie, Joshua; Heck, Michelle

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 5/13/2025
Publication Date: 5/13/2025
Citation: Preising, S., Wilson, J., Parker, G., Deblasio, S.L., Reeve, D.M., Chappie, J.S., Heck, M.L. 2025. Viral silencing suppressor activity in plants modifies aphid antiviral immunity and fecundity. bioRxiv. 2025. https://doi.org/10.1101/2025.05.13.653761.
DOI: https://doi.org/10.1101/2025.05.13.653761

Interpretive Summary: Economically, plant poleroviruses such as potato leafroll virus (PLRV) and other related poleroviruses are costly. In some areas, PLRV can cut potato yields by 50–60%, costing $100 million annually and contributing to global losses of 20 million tons. New strategies to reduce virus transmission are needed. Plants defend against viral infections using RNA interference (RNAi), an immunity mechanism that destroys viral RNA. However, viruses such as PLRV, produce proteins to block this defense. PLRV’s P0 protein disrupts a key plant protein (ARGONATE 1), enabling PLRV to spread in the plant. PLRV is spread by aphids, and P0 also affects these insects by weakening the aphid’s immune response to aphid-specific viruses, and increases aphid reproduction, leading to more virus-carrying offspring. In this work, we show that a specific motif of P0 is required to suppress aphid immunity but not for boosting aphid reproduction. We also show that other plant viruses similarly influence aphid reproduction, suggesting a complex interplay where plant viruses, aphid viruses, plants, and aphids co-evolve, each adapting to the others’ defenses and strategies. New strategies targeting proteins like P0 to reduce aphid populations or virus transmission could mitigate losses due to poleroviruses.

Technical Abstract: Plants defend themselves from viral infection using RNA interference (RNAi), an evolutionary conserved mechanism that degrades viral RNA through the production of small interfering RNAs. As a counter defense, plant viruses evolved suppressors of RNA silencing (VSRs) to inhibit plant RNAi machinery, aiding viral replication and transmission. P0, a VSR encoded by the potato leafroll virus (PLRV), family Polerovirus, suppresses RNAi by targeting the plant protein ARGONATE 1 for degradation through its F-box motif interaction with a Skp1 subunit of the family of E3 ubiquitin ligases. Our previous work shows PLRV P0 suppresses antiviral immunity in its aphid vector Myzus persicae, leading to an increase in aphid infection by the insect virus Myzus persicae densovirus (MpDNV). Here, we expand on these findings and show that the P0 protein also regulates aphid fecundity. Using a series of F-box mutants, we demonstrate that a functional P0 F-box motif is required for inhibition MpDNV antiviral immunity but not modulation of aphid fecundity. We further show that silencing suppressors from non-aphid-borne plant viruses that target other components of the plant’s RNAi machinery also modulate aphid fecundity but MpDNV titer. Collectively, the results show that aphids have been favored by selection to modulate their anti-viral immunity and fecundity in response to changes in the plant RNAi pathways induced by plant viral infection. These data highlight the intricate co-evolution of plant viruses, their vectors, and host defenses. This knowledge may open new avenues for managing vector-borne plant diseases by targeting viral proteins to manipulate insect vectors.