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. 2018 Oct 4;18(1):219.
doi: 10.1186/s12870-018-1438-7.

Rice stripe virus-derived siRNAs play different regulatory roles in rice and in the insect vector Laodelphax striatellus

Meiling Yang  1 , Zhongtian Xu  2   3 , Wan Zhao  1 , Qing Liu  1   3 , Qiong Li  1   3 , Lu Lu  1 , Renyi Liu  4 , Xiaoming Zhang  5 , Feng Cui  6
Affiliations

Rice stripe virus-derived siRNAs play different regulatory roles in rice and in the insect vector Laodelphax striatellus

Meiling Yang et al. BMC Plant Biol. .

Abstract

Background: Most plant viruses depend on vector insects for transmission. Upon viral infection, virus-derived small interfering RNAs (vsiRNAs) can target both viral and host transcripts. Rice stripe virus (RSV) is a persistent-propagative virus transmitted by the small brown planthopper (Laodelphax striatellus, Fallen) and can cause a severe disease on rice.

Results: To investigate how vsiRNAs regulate gene expressions in the host plant and the insect vector, we analyzed the expression profiles of small RNAs (sRNAs) and mRNAs in RSV-infected rice and RSV-infected planthopper. We obtained 88,247 vsiRNAs in rice that were predominantly derived from the terminal regions of the RSV RNA segments, and 351,655 vsiRNAs in planthopper that displayed relatively even distributions on RSV RNA segments. 38,112 and 80,698 unique vsiRNAs were found only in rice and planthopper, respectively, while 14,006 unique vsiRNAs were found in both of them. Compared to mock-inoculated rice, 273 genes were significantly down-regulated genes (DRGs) in RSV-infected rice, among which 192 (70.3%) were potential targets of vsiRNAs based on sequence complementarity. Gene ontology (GO) analysis revealed that these 192 DRGs were enriched in genes involved in kinase activity, carbohydrate binding and protein binding. Similarly, 265 DRGs were identified in RSV-infected planthoppers, among which 126 (47.5%) were potential targets of vsiRNAs. These planthopper target genes were enriched in genes that are involved in structural constituent of cuticle, serine-type endopeptidase activity, and oxidoreductase activity.

Conclusions: Taken together, our results reveal that infection by the same virus can generate distinct vsiRNAs in different hosts to potentially regulate different biological processes, thus reflecting distinct virus-host interactions.

Keywords: Rice; Rice stripe virus; Small RNA sequencing; Small brown planthopper; Transcriptome; Virus-derived small interfering RNAs.

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Figures

Fig. 1
Fig. 1
Host-derived sRNAs in rice and small brown planthopper. (a, b) Size distribution of host-derived sRNAs in rice (a) and small brown planthopper (b). Host-derived sRNAs are 18–30-nt sRNAs with perfect match to the host genome minus those derived from structural RNAs. Numbers of sRNAs of the same size but with different 5′ terminal nucleotides were drawn in different colors. c, d 5′ terminal nucleotide frequency of host-derived sRNAs in rice (c) and small brown planthopper (d). e, f Volcano plot of differentially expressed sRNAs between mock-inoculated and RSV infected samples in rice (e) and small brown planthopper (f). Green dots represent differentially expressed unique sRNAs with significance cutoffs being fold change > 2 and adjusted p-value < 0.05
Fig. 2
Fig. 2
vsiRNAs in rice and small brown planthopper. a Venn diagram showing number of unique vsiRNAs that were specific to rice or planthopper and those found in both hosts. b, c Size distribution of vsiRNAs in rice (b) and small brown planthopper (c). vsiRNAs are 18–30-nt sRNAs in RSV-infected rice and planthopper with up to one mismatch to the RSV genome. Numbers of vsiRNAs of the same size but with different 5′ terminal nucleotides are drawn in different colors. d 5′ terminal nucleotide frequency of vsiRNAs in RSV-infected rice and planthopper. e, f Distribution of vsiRNAs along the RSV genome in RSV-infected rice (e) and small brown planthopper (f). Four segments of the RSV genome were arranged along the X-axis with length drawn to scale. vsiRNAs that were derived from the sense and antisense strand were shown above and below the horizontal line, respectively. Numbers of vsiRNAs with the most abundant size class (21-nt in rice and 22-nt in planthopper) were separated from those of other size classes
Fig. 3
Fig. 3
RT-PCR validation of the expressions of vsiRNAs in RSV-infected rice (a) and small brown planthopper (b). RT-PCR assays were conducted with three independent biological replicates. U6 was used as internal control
Fig. 4
Fig. 4
Rice genes that are potentially targeted by rice-specific vsiRNAs. a GO enrichment analysis of the down-regulated genes in rice after RSV infection. b GO enrichment analysis of the down-regulated genes that are potentially targeted by vsiRNAs. c Selected rice-specific vsiRNAs that potentially interact with rice genes involved in kinase activity, carbohydrate binding and pollen-pistil interaction. d Six predicted target genes of vsiRNA were selected to verify downregulation using qRT–PCR. qPCR data are shown as the means ± SEM (n = 6). *p < 0.05; **p < 0.01; ***p < 0.001
Fig. 5
Fig. 5
Planthopper genes that are potentially targeted by planthopper-specific vsiRNAs. (A) GO enrichment analysis of the down-regulated genes in small brown planthopper after RSV infection. (B) GO enrichment analysis of the down-regulated genes that are potentially targeted by vsiRNAs. (C) Selected planthopper-specific vsiRNAs that potentially target planthopper genes encoding secretion proteins or involved in serine-type endopeptidase activity. (D) Six predicted target genes of vsiRNA were selected to verify downregulation using qRT–PCR. qPCR data are shown as the means ± SEM (n = 6). *p < 0.05; **p < 0.01; ***p < 0.001
Fig. 6
Fig. 6
Common vsiRNAs in RSV-infected rice and planthopper potentially target genes with different functionalities. a, b Gene ontology (GO) enrichment analysis of the down-regulated genes that were potentially targeted by the 50 most highly expressed common vsiRNAs in RSV-infected rice (a) and viruliferous planthopper (b). c Target genes of common vsiRNA in the two hosts that show sequence homology. Blue circles represents common vsiRNAs. Black arrows represent vsiRNA-target relationship. Colored boxes with “A”-“D” labels represent predicted target genes. The genes targeted by the same vsiRNA in the two hosts are labeled by the same letter because they show sequence homology, the level of which is indicated above the black arrow
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References

    1. Soosaar JL, Burch-Smith TM, Dinesh-Kumar SP. Mechanisms of plant resistance to viruses. Nat Rev Microbiol. 2005;3(10):789–798. doi: 10.1038/nrmicro1239. - DOI - PubMed
    1. Ng JC, Perry KL. Transmission of plant viruses by aphid vectors. Mol Plant Pathol. 2004;5(5):505–511. doi: 10.1111/j.1364-3703.2004.00240.x. - DOI - PubMed
    1. Power AG. Insect transmission of plant viruses: a constraint on virus variability. Curr Opin Plant Biol. 2000;3(4):336–340. doi: 10.1016/S1369-5266(00)00090-X. - DOI - PubMed
    1. Hohn T. Plant virus transmission from the insect point of view. Proc Natl Acad Sci U S A. 2007;104(46):17905–17906. doi: 10.1073/pnas.0709178104. - DOI - PMC - PubMed
    1. Ding SW. RNA-based antiviral immunity. Nat Rev Immunol. 2010;10(9):632–644. doi: 10.1038/nri2824. - DOI - PubMed

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