A viral movement protein targets host catalases for 26S proteasome-mediated degradation to facilitate viral infection and aphid transmission in wheat.

The infection of host plants by many different viruses causes reactive oxygen species (ROS) accumulation and yellowing symptoms, but the mechanisms through which plant viruses counteract ROS-mediated immunity to facilitate infection and symptom development has not been fully elucidated. Most plant viruses are also transmitted by insect vectors in the field, but the molecular mechanisms underlying virus‒host-insect interactions are unclear. In this study, we investigated the interactions among wheat, barley yellow dwarf virus (BYDV) and its aphid vector and found that the BYDV movement protein (MP) interacts with both wheat catalases (CATs) and the 26S proteasome ubiquitin receptor PSMD2 to facilitate the 26S proteasome-mediated degradation of CATs, facilitating viral infection, disease symptom development and aphid transmission. Overexpression of the BYDV MP gene in wheat promoted the degradation of CATs to increase the accumulation of ROS, leading to enhanced viral infection. Interestingly, transgenic wheat lines overexpressing BYDV MP induced significantly reduced proliferation of wingless aphids and an increased number of winged aphids. Consistently, the silencing of CATs also enhanced viral accumulation and reduced the proliferation of wingless aphids but increased the occurrence of winged aphids. In contrast, transgenic wheat plants overexpressing TaCAT1 exhibited the opposite changes and increases in grain size and weight upon infection with BYDV. Biochemical assays demonstrated that BYDV MP interacts with PSMD2 and may promotes the 26S proteasome-mediated degradation of TaCAT1 in a ubiquitination-independent manner. Overall, our study reveals the mechanism by which a plant virus manipulates the ROS production system of the host plant to facilitate infection and transmission, shedding new light on the sophisticated interactions among viruses, host plants and insect vectors.

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