Comparison of Transcriptome Responses between Sogatella furcifera Females That Acquired Southern Rice Black-Streaked Dwarf Virus and Not

SIMPLE SUMMARY: The southern rice black-streaked dwarf virus (SRBSDV) is transmitted horizontally by the planthopper, Sogatella furcifera. During feeding on virus-infected plants, S. furcifera may acquire or fail to acquire SRBSDV. In this study, the responses were compared among the S. furcifera successfully acquiring the virus, those failing to acquire the virus, and those not exposed to SRBSDV (the control). A total of 1043 and 2932 differentially expressed genes (DEGs) were obtained in S. furcifera females that acquired SRBSDV and that failed to, in comparison with the control, respectively. Functionally, these DEGs are primarily involved in diverse signaling pathways related to primary metabolism and innate immunity, such as apoptosis. Additional bioassays confirmed the activation of apoptosis in S. furcifera by SRBSDV exposure. Interestingly, we also found that six female-specific genes were also upregulated in S. furcifera females exposed to SRBSDV. Our results further the understanding of the interactions between the vector S. furcifera females and SRBSDV at the molecular level. ABSTRACT: The southern rice black-streaked dwarf virus (SRBSDV) is transmitted horizontally by Sogatella furcifera in a persistent, propagative manner. Exposure of S. furcifera females to SRBSDV-infected rice plants may trigger transcriptomic changes in the insects, the transcriptomes of females that acquired SRBSDV and those that failed to, as well as females fed on healthy rice plants as control, were sequenced and compared. Nine transcriptomic libraries were constructed, from which a total of 53,084 genes were assembled. Among the genes, 1043 and 2932 were differentially expressed genes (DEGs) in S. furcifera females that acquired SRBSDV and that failed to, in comparison with the control, respectively. Functional enrichment analysis showed that DEGs identified in S. furcifera females exposed to SRBSDV are primarily involved in diverse signaling pathways related to primary metabolism and innate immunity. The DEGs in the S. furcifera females that failed to acquire the virus significantly outnumbered that in the insects that acquired the virus, and the virus exposure activated the humoral and cellular immune responses of the vectors, especially the apoptosis. The key gene in apoptosis encoding caspase 1 was upregulated by SRBSDV exposure, especially in S. furcifera females that failed to acquire the virus. Analysis of caspase 1 activity validated that SRBSDV exposure induced caspase 1 accumulation. Surprisingly, the expression of six female-specific genes was also upregulated by SRBSDV exposure, which was confirmed by RT-qPCR analysis. This study provides evidence to explain the differential virus acquisition at the transcriptome level.