The bunyavirus nonstructural protein NSs suppresses plant immunity to facilitate its own transmission by improving vector insect performance

Abstract

15Pandemics of vector-borne human and plant pathogens often rely on the behaviors of 16 their arthropod vectors. Arboviruses, including many bunyaviruses, manipulate vector 17 behavior to accelerate their own transmission to vertebrates, birds, insects, and plants. 18 However, the molecular mechanism underlying this manipulation remains elusive. 19 Here, we report that the non-structural protein NSs of orthotospovirus (order 20 Bunyavirales, family Tospoviridae), is a key viral factor that indirectly modifies 21 vector preference and increases vector performance. NSs suppresses the biosynthesis 22 of volatile monoterpenes, which serve as repellents of the vector Western flower 23 thrips (WFT, Frankliniella occidentalis) instead of using its known silencing 24 suppressor activity. NSs directly interacts with and relocalizes the jasmonate (JA) 25 signaling master regulator MYC2 and its two close homologs, MYC3 and MYC4, to 26 disable JA-mediated activation of terpene synthase genes. The dysfunction of the 27 MYCs subsequently attenuates host defenses, increases the attraction of thrips, and 2 28 improves thrips fitness. These findings elucidate the molecular mechanism through 29 which a bunyavirus manipulates vector behaviors and therefore facilitate disease 30 transmission. Our results provide important insights into the molecular mechanisms 31 by which tospoviruses NSs counteracts host immunity for pathogen transmission. 32 Author summary 33 Most bunyaviruses are transmitted by insect vectors, and some of them can modify 34 the behaviors of their arthropod vectors to increase transmission to mammals, birds, 35 and plants. NSs is a non-structural bunyavirus protein with multiple functions that 36 acts as an avirulence determinant and silencing suppressor. In this study, we identified 37 a new function of NSs as a manipulator of vector behavior, independent of its 38 silencing suppressor activity. NSs manipulates jasmonate-mediated immunity against 39 thrips by directly interacting with several homologs of MYC transcription factors, the 40 core regulators of the jasmonate-signaling pathway. This hijacking by NSs enhances 41 thrips preference and performance. Many human-and animal-infecting members of 42the Bunyaviridales also encode NSs and could manipulate vector behavior to 43 accelerate their own transmission. Therefore, our data support the hypothesis that the 44 NSs protein may play conserved roles among various members of the Bunyaviridales 45 in the modification of vector feeding behavior that evolved as a mechanism to 46 enhance virus transmission. 47 48 Arthropod-borne viruses (arboviruses) are virulent causal agents of diseases in 49 humans, animals, and plants. Vector behaviors have critical ecological and 50 evolutionary consequences for arboviruses, which rely exclusively on their arthropod 51 vectors for dispersal to (and survival in) new hosts. Therefore, it is of evolutionary 3 52 significance for an arbovirus to alter its vector's behavior to facilitate its own 53 transmission. Interestingly,...