Abstract

Sogatella furcifera, the white-backed planthopper (WBPH), has become one of the most destructive pests in rice production owing to its plant sap-sucking behavior and efficient transmission of Southern rice black-streaked dwarf virus (SRBSDV) in a circulative, propagative and persistent manner. The dynamic and complex SRBSDV-WBPH-rice plant interaction is still poorly understood. In this study, based on a homology-based genome-wide analysis, 348 immune-related genes belonging to 28 families were identified in WBPH. A transcriptome analysis of non-viruliferous (NVF) and viruliferous groups with high viral titers (HVT) and median viral titers (MVT) revealed that feeding on SRBSDV-infected rice plants has a significant impact on gene expression, regardless of viral titers in insects. We identified 278 up-regulated and 406 down-regulated genes shared among the NVF, MVT, and HVT groups and detected significant down-regulation of primary metabolism-related genes and oxidoreductase. In viruliferous WBPH with viral titer-specific transcriptome changes, 1,906 and 1,467 genes exhibited strict monotonically increasing and decreasing expression, respectively. The RNAi pathway was the major antiviral response to increasing viral titers among diverse immune responses. These results clarify the responses of immune genes and the transcriptome of WBPH to SRBSDV and improve our knowledge of the functional relationship between pathogen, vector, and host.

Highlights

  • Sogatella furcifera, the white-backed planthopper (WBPH), has become one of the most destructive pests in rice production owing to its plant sap-sucking behavior and efficient transmission of Southern rice black-streaked dwarf virus (SRBSDV) in a circulative, propagative and persistent manner

  • A total of 348 manually curated immune genes were identified in the WBPH genome based on a homology search of WBPH protein-coding genes against immune-related genes of model species (Drosophila melanogaster and Anopheles gambiae) and ImmunoDB

  • Among the 348 immune genes identified in WBPH, 231 were classified into 28 families and 4 functional groups (Fig. 1 and Fig. S1), which mainly included immune recognition families (PGRPs, GRPs, C-type lectins, SCRs, etc.), immune signaling pathways (Toll, IMD, Janus kinase (JAK)-signal transducer and activator of transcription (STAT) signaling pathways, RNA interference (RNAi) pathway), immune response effectors (PPO, thioester-containing protein (TEP), antimicrobial peptide (AMP), etc.), and others (SOD, catalases, peroxidases, etc.) (Tables S1 and S2), representing a relatively complete immune gene set for the species

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Summary

Introduction

The white-backed planthopper (WBPH), has become one of the most destructive pests in rice production owing to its plant sap-sucking behavior and efficient transmission of Southern rice black-streaked dwarf virus (SRBSDV) in a circulative, propagative and persistent manner. The RNAi pathway was the major antiviral response to increasing viral titers among diverse immune responses These results clarify the responses of immune genes and the transcriptome of WBPH to SRBSDV and improve our knowledge of the functional relationship between pathogen, vector, and host. There were more immune system genes and cytoskeleton organization genes among MIEGs and MDEGs than DEGs in general, and the RNAi pathway was one of the major antiviral pathways Taking together, this informative integrated immune analysis provides a deeper understanding of the innate immune system of WBPH, the biology of the virus within the insect host, and the host response to the virus

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