The vitellogenin receptor has an essential role in vertical transmission of rice stripe virus during oogenesis in the small brown plant hopper

Abstract

BACKGROUND: The small brown plant hopper (SBPH), Laodelphax striatellus Fallén, is one of the most destructive pests on rice. This pest transmits rice stripe virus (RSV) both horizontally and vertically, leading to major yield and economic losses in rice production. However, the way that RSV particles enter oocytes of SBPH remains largely unknown. Thus, identification of key factors involved in the interaction between SBPH and RSV in the ovary is crucial. RESULTS: Transcriptome of non-viruliferous (NV) or high viruliferous (HV) SBPH ovaries at 24 and 48 h of emergence wassequenced. Differentially expressed genes analysis showed that vitellogenin receptor was significantly highly expressed in the ovary of the HV SBPH strains compared to NV strains. Quantitative real-time polymer chain reaction showed that the vitellogenin receptor in L. striatellus (LsVgR) was highly expressed in the ovaries of female adults and maintained a high level of expression at the early stage of ovary development. By using RNA interference, the expression of LsVgR in the ovaries of the HV strain was significantly decreased by 98.1%. RSV titer was reduced by 60.9% as quantified by viral RNA3 intergenic region and the transcripts of nucleocapsid protein gene (CP) reduced by 46.3%. The numbers of offspring hatched were significantly reduced in dsRNA-treated groups. The transcripts of CP were not affected by silencing LsVgR, whereas the abundance of RNA-dependent RNA polymerase increased by 15-fold in the member of surviving progenies. CONCLUSION: Our results suggest that vitellogenin receptor participates in regulating RSV replication during oogenesis.

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

“…RSV is believed to accumulate most in the ovaries, followed by the midgut lumen, epithelial cells and muscles . The RNA level of the CP gene or viral RNA3 segment is generally considered to reflect viral load and has been extensively used to quantify RSV titers in insect vectors . Thus, to investigate whether sublethal concentrations of triazophos affected RSV accumulations in the ovaries of SBPH, we measured the RNA levels of CP and RNA3 .…”

“…The small brown planthopper (SBPH), Laodelphax striatellus (Hemiptera: Delphacidae), is an economically important rice pest that transmits various plant viruses that cause serious crop diseases such as rice black‐streaked dwarf virus, barley yellow striate mosaic virus and rice stripe virus (RSV) . RSV is a single‐stranded RNA virus belonging to the Tenuivirus genus that causes chlorotic stripes, mottling and necrotic streaks of rice leaves, and is one of the most destructive rice diseases in East Asia, resulting in 50–100% grain yield losses . RSV contains four single‐strand RNA segments (RNA1–4) encoding seven proteins .…”

“…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 …”

“…[3][4][5][6][7] RSV is a single-stranded RNA virus belonging to the Tenuivirus genus that causes chlorotic stripes, mottling and necrotic streaks of rice leaves, 8 and is one of the most destructive rice diseases in East Asia, resulting in 50-100% grain yield losses. [9][10][11] RSV contains four single-strand RNA segments (RNA1-4) encoding seven proteins. 12,13 RNA1 is negative-sense to encode RNA-dependent RNA polymerase.…”

“…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.…”