NS3 Protein from Rice stripe virus affects the expression of endogenous genes in Nicotiana benthamiana

Abstract

BackgroundRice stripe virus (RSV) belongs to the genus Tenuivirus. It is transmitted by small brown planthoppers in a persistent and circulative-propagative manner and causes rice stripe disease (RSD). The NS3 protein of RSV, encoded by the viral strand of RNA3, is a viral suppressor of RNA silencing (VSR). NS3 plays a significant role in viral infection, and NS3-transgenic plants manifest resistance to the virus.MethodsThe stability and availability of NS3 produced by transgenic Nicotiana benthamiana was investigated by northern blot analysis. The accumulation of virus was detected by western blot analysis. Transcriptome sequencing was used to identify differentially expressed genes (DEGs) in NS3-transgenic N. benthamiana.ResultsWhen the host plants were inoculated with RSV, symptoms and viral accumulation in NS3-transgenic N. benthamiana were reduced compared with the wild type. Transcriptome analysis identified 2533 differentially expressed genes (DEGs) in the NS3-transgenic N. benthamiana, including 597 upregulated genes and 1936 downregulated genes. These DEGs were classified into three Gene Ontology (GO) categories and were associated with 43 GO terms. KEGG pathway analysis revealed that these DEGs were involved in pathways associated with ribosomes (ko03010), photosynthesis (ko00195), photosynthesis-antenna proteins (ko00196), and carbon metabolism (ko01200). More than 70 DEGs were in these four pathways. Twelve DEGs were selected for RT-qPCR verification and subsequent analysis. The results showed that NS3 induced host resistance by affecting host gene expression.ConclusionNS3, which plays dual roles in the process of infection, may act as a VSR during RSV infection, and enable viral resistance in transgenic host plants. NS3 from RSV affects the expression of genes associated with ribosomes, photosynthesis, and carbon metabolism in N. benthamiana. This study enhances our understanding of the interactions between VSRs and host plants.

The Bunyavirales: The Plant-Infecting Counterparts

“…Mutants that lost siRNA binding activity are compromised in their ability to suppress RNAi [ 166 , 167 ]. The protein also modifies the expression of plant endogenous genes [ 168 ] via interaction with OsDRB1, an indispensable component of the rice miRNA-processing complex. It acts as a scaffold between OsDRB1 and pri-miRNAs to regulate their association and aid to in vivo processing of pri-miRNAs.…”

The small brown planthopper (Laodelphax striatellus) as a vector of the rice stripe virus

“…Jiang et al, 2021;Kong et al, 2014;J. Li et al, 2015;Lu et al, 2019;G. Wu et al, 2018;Yang et al, 2020;X.…”

Crystal Structure of the Disease-Specific Protein of Rice Stripe Virus

“…2 Transcriptome analyses of the p3 gene silencing suppressor protein overexpressed in Nicotiana benthamiana revealed significantly altered genes related to the ribosome and photosynthesis. 17 NbP3IP interacts with the autophagy-related ATG8 to direct p3 degradation through the autophagy pathway. 18 RSV pc3 interacts with SP during the formation of inclusion complexes that are important for viral spread in the body of vector insects.…”

“…RNA3 encodes nonstructural protein 3 (NS3; p3) from the vRNA and NSvc3 (coat protein; pc3) in the vcRNA . Transcriptome analyses of the p3 gene silencing suppressor protein overexpressed in Nicotiana benthamiana revealed significantly altered genes related to the ribosome and photosynthesis . NbP3IP interacts with the autophagy-related ATG8 to direct p3 degradation through the autophagy pathway .…”