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

Xiaofang Chen,Feng Cui,Jinting Yu,Wei Wang,Le Kang,Hong Lu,Bruno Lemaitre

doi:10.1128/mbio.01453-20

Xiaofang Chen, Feng Cui + Show 5 more

Open Access

https://doi.org/10.1128/mbio.01453-20

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Journal: mBio	Publication Date: Aug 18, 2020
Citations: 20	License type: CC BY 4.0

Affiliation: University of Chinese Academy of Sciences

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.

Highlights

IntroductionViral stability in the hemolymph of vector insects is a prerequisite for successful transmission of persistent plant viruses
Most plant viruses require vector insects for transmission
The gene response of the PPO activation pathway to rice stripe virus (RSV) was checked in the fat body and hemocytes of viruliferous and nonviruliferous planthoppers using quantitative real-time PCR (Fig. 2; see Fig. S1)

Summary

Introduction

Viral stability in the hemolymph of vector insects is a prerequisite for successful transmission of persistent plant viruses. 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. 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. PO catalyzes the conversion of monophenols to quinones, which form melanins restricting the activity of or killing pathogens [10] This pathway is negatively regulated by serpins, which maintain the PPO cascade in an inactive state when there is no immune challenge [11]. Pathogenic bacteria and fungi usually induce the activation of PPO cascade, and some of them, such as Enterobacter cloacae or Micrococcus luteus, are frequently used as activators of this cascade in studies [12, 13]

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