Rice stripe virus hitchhikes the vector insect vitellogenin ligand-receptor pathway for ovary entry

Abstract

It is known that plant arboviruses infect insect vector cells by endocytosis; however, the cellular receptors that mediate endocytosis have not been well defined. In our recently published work and this study, by clarifying the vertical transmission mechanism of Rice stripe virus (RSV) in Laodelphax striatellus , we provide a novel paradigm for how arboviruses enter insect germ-line cells. Instead of direct interaction with a viral receptor, the virus binds to a secreted ligand protein, hitchhiking the ligand-receptor pathway to achieve cell entry. Vitellogenin (Vg) is an indispensable protein for embryo development that is synthesized extra-ovarially and taken up by germ-line cells through Vg receptor (VgR)-mediated endocytosis. After revealing that RSV invades L. striatellus ovary by a specific molecular interaction with the insect Vg in haemolymph, this study addressed VgR's function in mediating the RSV invasion of the germarium nurse cells, further confirming the ligand's receptor-mediated viral cell-invasion mechanism. Understanding the viral ovary-entry pathways in vectors will help to find suitable measures to block the trans-generation transmission of the viruses. This article is part of the theme issue ‘Biotic signalling sheds light on smart pest management’.

Triazophos‐induced vertical transmission of rice stripe virus is associated with host vitellogenin in the small brown planthopper Laodelphax striatellus

“…The results indicate that LsVg mRNA expression in the ovaries is significantly reduced by 84.1% and LsVgR is significantly decreased by 47.3%. VgR‐mediated endocytosis facilitates Vg entry into ovaries . Hence, we inferred that silencing of Vg suppressed VgR expression due to disrupted VgR‐mediated Vg uptake into ovary.…”

“…VgR-mediated endocytosis facilitates Vg entry into ovaries. 38 Hence, we inferred that silencing of Vg suppressed VgR expression due to disrupted VgR-mediated Vg uptake into ovary. Meanwhile, knockdown of LsVg significantly decreased the expression levels of CP and RNA3 in the ovaries, suggesting that RSV accumulation is seriously suppressed.…”

“…The Vg ligand‐receptor pathway is considered critical for the mediation of RSV entry into SBPH ovaries. Knockdown of Vg or VgR transcript significantly decreased RSV titers and thus interfered with systemic virus infection . In addition, Vg or VgR was found to participate in the transmission of other pathogens …”

“…Knockdown of Vg or VgR transcript significantly decreased RSV titers and thus interfered with systemic virus infection. 11,35,37,38 In addition, Vg or VgR was found to participate in the transmission of other pathogens. [39][40][41] Our previous study first reported that sublethal doses of triazophos increased RSV vertical transmission ability in SBPH.…”

Overview: biotic signalling for smart pest management

“…Cellular receptor determines the cell type that a virus invades; however, no insect receptor for arbovirus has been characterized. Huo et al demonstrated that a plant arbovirus hitchhikes a well-defined insect ligand-receptor interaction pathway to achieve its cell entry, representing an undescribed mechanism for arbovirus to invade vector cells [25]. Salivary effector proteins present in viruliferous insects play an important role in the tripartite interaction.…”