The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance

Abstract

Pandemics of vector-borne human and plant diseases often depend on the behaviors of their arthropod vectors. Arboviruses, including many bunyaviruses, manipulate vector behavior to accelerate their own transmission to vertebrates, birds, insects, and plants. However, the molecular mechanism underlying this manipulation remains elusive. Here, we report that the non-structural protein NSs of Tomato spotted wilt orthotospovirus, a prototype of the Tospoviridae family and the Orthotospovirus genus, is a key viral factor that indirectly modifies vector preference and increases vector performance. NSs suppresses the biosynthesis of plant volatile monoterpenes, which serve as repellents of the vector western flower thrips (WFT, Frankliniella occidentalis ). NSs directly interacts with MYC2, the jasmonate (JA) signaling master regulator and its two close homologs MYC3 and MYC4, to disable JA-mediated activation of terpene synthase genes. The dysfunction of the MYCs subsequently attenuates host defenses, increases the attraction of thrips, and improves thrips fitness. Moreover, MYC2 associated with NSs of Tomato zonate spot orthotospovirus, another Euro/Asian-type orthotospovirus, suggesting that MYC2 is an evolutionarily conserved target of Orthotospovirus species for suppression of terpene-based resistance to promote vector performance. These findings elucidate the molecular mechanism through which an orthotospovirus indirectly manipulates vector behaviors and therefore facilitates pathogen transmission. Our results provide insights into the molecular mechanisms by which Orthotospovirus NSs counteracts plant immunity for pathogen transmission.

Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors

“…The JAZ-MYC hub is one of the key nodes in JA signaling and MYC2-orchestrated transcriptional reprogramming during JA signaling [76]. Notably, during its long evolution history, JAZ-MYC hub has become a common target for both insect-borne plant DNA and RNA viruses [77][78][79][80].…”

“…The dysfunction of the MYCs in Arabidopsis thaliana leads to enhanced vector attraction and performance. Moreover, the association between MYC2 and NSs is conserved among different orthotospoviruses and plant hosts [79]. In addition, 2b of the Cucumber mosaic virus (CMV) also attenuated the JA signaling pathway.…”

“…A simple example of this relationship is the cooccurrence of whitefly and thrip insects and their transmitted TYLCV and TSWV on the same plant. These two persistently transmitted viruses both target the JAZ-MYC2 hub [77,79]. This process is supposed to benefit both vector and nonvector insects since JAZ-MYC2 is one of the key hubs to positively regulate defenses against multiple herbivores.…”

“…TYLCCNV associated with TYLCCNB (Tomato yellow leaf curl virus betasatellite) reduce the amount of this compound, thus resulting in an attraction of the insect vector [77]. TSWV also reduces the amount of linalool, whose function is to repel the thrip vector [79].…”

Herbivore-induced activation of viral phosphatase disarms plant antiviral immunities for pathogen transmission

“…For instance, mosquito-borne bunyaviruses and flaviviruses as well as thrip-borne tospoviruses promote virus transmission by directly increasing vector biting rates and by interfering with the ingestion process (Stafford et al, 2011; Liu et al, 2017). Furthermore, arboviruses may indirectly promote transmission by 1) manipulating the immune responses of both the vector and the host, 2) suppressing host immunity by vector salivary factors, 3) manipulating vector behavior, and 4) encoding transmission facilitators (Vasilakis and Tesh 2015; Wang et al, 2019; Wu et al 2019; Wu and Ye, 2020). Since plants are sessile, around 80% plant viruses are transmitted by insect vectors, especially whiteflies and aphids that transmit more than 50% of all vector-borne viruses.…”