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. 2015 Jan 20:5:7883.
doi: 10.1038/srep07883.

Rice stripe virus affects the viability of its vector offspring by changing developmental gene expression in embryos

Shuo Li  1 , Shijuan Wang  1 , Xi Wang  1 , Xiaoli Li  1 , Jinyan Zi  1 , Shangshu Ge  1 , Zhaobang Cheng  1 , Tong Zhou  1 , Yinghua Ji  1 , Jinhua Deng  1 , Sek-Man Wong  2 , Yijun Zhou  1
Affiliations

Rice stripe virus affects the viability of its vector offspring by changing developmental gene expression in embryos

Shuo Li et al. Sci Rep. .

Abstract

Plant viruses may affect the viability and development process of their herbivore vectors. Small brown planthopper (SBPH) is main vector of Rice stripe virus (RSV), which causes serious rice stripe disease. Here, we reported the effects of RSV on SBPH offspring by crossing experiments between viruliferous and non-viruliferous strains. The life parameters of offspring from different cross combinations were compared. The hatchability of F1 progeny from viruliferous parents decreased significantly, and viruliferous rate was completely controlled by viruliferous maternal parent. To better elucidate the underlying biological mechanisms, the morphology of eggs, viral propagation and distribution in the eggs and expression profile of embryonic development genes were investigated. The results indicated that RSV replicated and accumulated in SBPH eggs resulting in developmental stunt or delay of partial eggs; in addition, RSV was only able to infect ovum but not sperm. According to the expression profile, expression of 13 developmental genes was regulated in the eggs from viruliferous parents, in which two important regulatory genes (Ls-Dorsal and Ls-CPO) were most significantly down-regulated. In general, RSV exerts an adverse effect on SBPH, which is unfavourable for the expansion of viruliferous populations. The viewpoint is also supported by systematic monitoring of SBPH viruliferous rate.

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Figures

Figure 1
Figure 1. The numbers of SBPH F1 progeny from the different cross groups on major developmental stages.
Major developmental stages included the egg, 1st-instar, 4th-instar and adult stages. V and N are viruliferous and non-viruliferous strains, respectively. All date are shown as the mean (± SE), and the different letters above the error bars indicate significant difference with a statistical analysis system (SAS) followed by Tukey's honest significant difference (HSD) test (P < 0.01 and P < 0.05).
Figure 2
Figure 2. The hatching period and nymph stage of the F1 progeny from the 4 cross groups.
All date are shown as the mean (± SE), and the different letters above the error bars indicate significant difference with a statistical analysis system (SAS) followed by Tukey's honest significant difference (HSD) test (P < 0.01 and P < 0.05).
Figure 3
Figure 3. The morphology of delayed and stunted eggs.
A–I: The stunted or delayed eggs from viruliferous SBPH parents. Some eggs became malformations (A, B and D) or wizened (C), some were already dead, rotten and blackening (E–H), and some eggs were developmentally delayed that their egg-eyes had not yet formed until the 10th day after spawning (I); J–L: non-viruliferous normal eggs in the 2nd (J), 5th (K) and 7th (L) day after spawning. Scale bars: 200 μm.
Figure 4
Figure 4. RSV propagation in the eggs.
(A) The variations of RSV transcripts in the viruliferous SBPH eggs during the egg development. The expression levels of RNP and SP genes were normalized relative to β-actin transcript, and the resulting 2−ΔCt values were used to plot with the developmental stages as the abscissa, including the prenatal (forthcoming) stage, postpartum 4th and 7th day. Each histogram bar represents the mean (± SE) from four repeats, and the different letters above the error bars indicate significant difference by Tukey's honest significant difference (HSD) test (P < 0.01 and P < 0.05). (B) Western-blot analysis of SP protein. Proteins from SBPH eggs were probed with the polyclonal antibody against SP. Protein markers were indicated on the left, and the detected bands were indicated by arrows. Lane M: relative molecular weight markers; lane 1: proteins from RSV-free SBPH eggs; lane 2: proteins from viruliferous SBPH eggs.
Figure 5
Figure 5. Immunolabelling micrographs showing the distribution of RSV RNP particles in SBPH germ cells.
A–D are transmission electron micrographs, and E and F are confocal laser micrographs. A: RSV RNP particles on the eggshell; B: RSV RNPs in the interior of ovum; C and D: the sperms of viruliferous SBPH without virus infection; the transverse section of sperms was approximately circular, and the longitudinal section was cylindrical shape; E and F: RSV RNPs in the interior of eggs after spawning. Virus RNPs were indicated by arrows. Scale bars: 0.2 μm (A, B), 1 μm (C, D) and 100 μm (E, F).
Figure 6
Figure 6. Expression profile of the embryonic development genes in SBPH eggs from different crosses.
The expression levels of target genes were normalized relative to β-actin transcript. Each histogram bar represents the mean (± SE) from triplicate repeats, and the different letters above the error bars indicate significant difference within the same gene by Tukey's honest significant difference (HSD) test (P < 0.01 and P < 0.05). A: relative expression quantity of the 10 genes (Ls-Atpα, Ls-Bx42, Ls-CtBP, Ls-drk, Ls-Hsc70-4, Ls-Mo25, Ls-Sema-1b, Ls-vib, Ls-tlk and Ls-Tll-1); B: relative expression quantity of the 5 genes (Ls-fd64A, Ls-Ddx1, Ls-Eip63E, Ls-InR and Ls-CPO); C: relative expression quantity of Ls-αTub67C, Ls-Lar and Ls-Dorsal genes.
Figure 7
Figure 7. The dynamics of the viruliferous rate of SBPH natural populations in Jiangsu between 2001–2013.
All date are shown as the mean values (± SD). The dynamics of SBPH's VR can be divided into three stages, including the rapid rise phase (RRP, 2001–2003), the stationary phase with high VR (SP, 2003–2007) and the slow decline phase (SDP, 2007–2013).
Figure 8
Figure 8. The monitoring of VR generation fluctuations of SBPH natural populations in Jiangsu.
All date are shown as the mean values (± SD). A: the monitoring VR results of SBPH from Guanyun, Haian, Jiangyan, Jingjiang and Wujin counties in 2003; B: VR fluctuations of SBPH from Changshu, Gaoyou, Hongze and Jianhu counties in 2004.
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