Insect tissue-specific vitellogenin facilitates transmission of plant virus

Abstract

Insect vitellogenin (Vg) has been considered to be synthesized in the fat body. Here, we found that abundant Vg protein is synthesized in Laodelphax striatellus hemocytes as well. We also determined that only the hemocyte-produced Vg binds to Rice stripe virus (RSV) in vivo. Examination of the subunit composition of L. striatellus Vg (LsVg) revealed that LsVg was processed differently after its expression in different tissues. The LsVg subunit able to bind to RSV exist stably only in hemocytes, while fat body-produced LsVg lacks the RSV-interacting subunit. Nymph and male L. striatellus individuals also synthesize Vg but only in hemocytes, and the proteins co-localize with RSV. We observed that knockdown of LsVg transcripts by RNA interference decreased the RSV titer in the hemolymph, and thus interfered with systemic virus infection. Our results reveal the sex-independent expression and tissue-specific processing of LsVg and also unprecedentedly connect the function of this protein in mediating virus transmission to its particular molecular forms existing in tissues previously known as non-Vg producing.

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

“…A previous study showed that LsVg plays a pivotal role in mediating transovarial transmission of RSV . Recently, it was found that the only hemocyte‐produced Vg binding to RSV facilitated horizontal transmission in SBPH . Thus, we investigated the temporal expression profile of LsVg from naïve and RSV‐infected SBPH, and found that LsVg was highly expressed at the adult stage and had a higher expression in the viruliferous SBPH at 4 days post emergence.…”

“…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 …”

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

“…Building on our previous studies [28,29], we reveal that a plant arbovirus hitchhikes a well-defined insect ligandreceptor interaction pathway to achieve its cell entry. This represents a previously undescribed mechanism for the arboviral invasion of vector cells.…”

“…Thus, VgR is required for RSV to enter the nurse cells. When Vg is deficient and VgR remains normally expressed, RSV cannot efficiently invade the germarium [28,29], indicating that the influence of VgR on the ability of RSV to invade an ovary is dependent on Vg.…”

“…Based on our obtained data regarding Vg transport, the VgRmediated endocytic machine and RSV invasion of the insect ovarian germarium, we proposed a model in which RSV crosses the ovarian barrier to enter the nurse cells of the germarium, resulting in successful vertical transmission ( figure 4). Laodelphax striatellus fat body and haemocytes produce Vg in different molecular forms, but only the haemocyte-produced Vg is able to interact with RSV capsid protein [29]. When Vg is produced in haemocytes, RSV binds to Vg.…”