A Plant Virus Ensures Viral Stability in the Hemolymph of Vector Insects through Suppressing Prophenoloxidase Activation

Abstract

Most plant viruses require vector insects for transmission. Viral stability in the hemolymph of vector insects is a prerequisite for successful transmission of persistent plant viruses. However, knowledge of whether the proteolytic activation of prophenoloxidase (PPO) affects the stability of persistent plant viruses remains elusive. Here, we explored the interplay between rice stripe virus (RSV) and the PPO cascade of the vector small brown planthopper. Phenoloxidase (PO) activity was suppressed by RSV by approximately 60%. When the PPO cascade was activated, we found distinct melanization around RSV particles and serious damage to viral stability in the hemolymph. Viral suppression of PO activity was derived from obstruction of proteolytic cleavage of PPOs by binding of the viral nonstructural protein NS3. These results indicate that RSV attenuates the PPO response to ensure viral stability in the hemolymph of vector insects. Our research provides enlightening cues for controlling the transmission of vector-borne viruses. IMPORTANCE Large ratios of vector-borne plant viruses circulate in the hemolymph of their vector insects before entering the salivary glands to be transmitted to plants. The stability of virions in the hemolymph is vital in this process. Activation of the proteolytic prophenoloxidase (PPO) to produce active phenoloxidase (PO) is one of the major innate immune pathways in insect hemolymph. How a plant virus copes with the PPO immune reaction in its vector insect remains unclear. Here, we report that the PPO affects the stability of rice stripe virus (RSV), a notorious rice virus, in the hemolymph of a vector insect, the small brown planthopper. RSV suppresses PPO activation using viral nonstructural protein. Once the level of PO activity is elevated, RSV is melanized and eliminated from the hemolymph. Our work gives valuable clues for developing novel strategies for controlling the transmission of vector-borne plant viruses.

Roles of Bacterial Symbionts in Transmission of Plant Virus by Hemipteran Vectors

“…The insect hemolymph, which is critical in persistent viral transmissions by insect vectors, can be used as a bridge to the salivary glands (Liu et al, 2015;Chen X. et al, 2020). Besides, it is well-defended by the immune system, which can effectively remove microorganisms (such as bacteria, fungi, and viruses) (Lavine and Strand, 2002;Blow and Douglas, 2019).…”

“…After viral particles are released from the midgut to the hemolymph, they can be recognized, targeted and cleared by the host immune system. Therefore, survival of virions within the hemolymph is vital for systemic dissemination of persistent viruses before entry into salivary glands (Liu et al, 2015;Chen X. et al, 2020). Van den Heuvel et al (1994) reported that chaperone proteins of endosymbionts may be involved in maintenance of plant viruses in the hemolymph.…”

The Bunyavirales: The Plant-Infecting Counterparts

“…Phenoloxidase is involved in the melanization pathway, one of the major innate immune responses of insects. RSV p3 binds cleavage sites of prephenoloxidase, preventing phenoloxidase activation by a cascade of clip-domain serine proteases and ensuring viral stability in the hemolymph [ 242 ].…”

Hemipteran-Transmitted Plant Viruses: Research Progress and Control Strategies

“…Additionally, the prophenoloxidase cascade is one of the major innate immune pathways that can restrict virus infection. Chen et al reported that RSV attenuates the prophenoloxidase response of the host to ensure virus stability in the hemolymph of vector insects [32] . Some animal viruses employ the mitogen-activated protein kinases of the host to establish successful infection.…”