A plant virus, TYLCV, up-regulates an endocrine oxylipin signal in its insect vector, Bemisia tabaci, via the viral C2 virulence factor for viral transmission

Abstract

To survive and efficiently transit between plant and insect hosts, circulative plant viruses have evolved sophisticated strategies to exploit insect vector factors. Tomato yellow leaf curl virus (TYLCV) is transmitted by Bemisia tabaci through a circulative and replicative pathway. In insects, C20 oxylipin (eicosanoid) and C18 oxylipin (EpOME) antagonistically regulate antiviral responses. Upon TYLCV infection, the intestinal apoptosis of B. tabaci facilitated the viral multiplication. The apoptosis was suppressed by eicosanoid but induced by EpOME. EpOME treatment also upregulated other proviral factors, including defensin, PGRP, and cathepsins, while eicosanoid signaling exerted opposite effects. TYLCV infection suppressed eicosanoid biosynthetic enzymes but induced a cytochrome P450 gene involved in EpOME biosynthesis, consistent with elevated EpOME levels in the viruliferous B. tabaci detected by LC-MS/MS. Individual RNA interference treatments specific to each of the TYLCV genes in the viruliferous insects revealed that only silencing of the viral C2 gene abolished EpOME-mediated proviral effects. These findings uncover a lipid-mediated mechanism by which TYLCV enhances vector competence to promote transmission. IMPORTANCEVarious plant viruses depend on insect vectors for their horizontal transfer. Some of them exhibit a circulative and propagative transmission by multiplying the viral titers within the insects using the host machinery. Here is a fascinating manipulation of the host immunity by a plant virus, tomato yellow leaf curl virus (TYLCV), which uses the insect endocrine signals associated with immunity of its vector, Bemisia tabaci. Two types of oxylipins, eicosanoid and EpOME, antagonistically act to insect immunity, in which eicosanoid induces immune responses while EpOME, as an insect immune resolvin, suppresses them. TYLCV uses its C2 gene component as a virulent factor to induce the EpOME biosynthesis of B. tabaci. The elevated EpOME levels in the vector insect led to proviral responses by inducing intestinal apoptosis and selectively suppressing the immune-associated genes. These findings demonstrate the viral manipulation of the host endocrine signal for inducing proviral responses.