Abstract
The Toll pathway plays an important role in defense against infection of various pathogenic microorganisms, including viruses. However, current understanding of Toll pathway was mainly restricted in mammal and some model insects such as Drosophila and mosquitoes. Whether plant viruses can also activate the Toll signaling pathway in vector insects is still unknown. In this study, using rice stripe virus (RSV) and its insect vector (small brown planthopper, Laodelphax striatellus) as a model, we found that the Toll pathway was activated upon RSV infection. In comparison of viruliferous and non-viruliferous planthoppers, we found that four Toll pathway core genes (Toll, Tube, MyD88, and Dorsal) were upregulated in viruliferous planthoppers. When the planthoppers infected with RSV, the expressions of Toll and MyD88 were rapidly upregulated at the early stage (1 and 3 days post-infection), whereas Dorsal was upregulated at the late stage (9 days post-infection). Furthermore, induction of Toll pathway was initiated by interaction between a Toll receptor and RSV nucleocapsid protein (NP). Knockdown of Toll increased the proliferation of RSV in vector insect, and the dsToll-treated insects exhibited higher mortality than that of dsGFP-treated ones. Our results provide the first evidence that the Toll signaling pathway of an insect vector is potentially activated through the direct interaction between Toll receptor and a protein encoded by a plant virus, indicating that Toll immune pathway is an important strategy against plant virus infection in an insect vector.
Highlights
In invertebrates, host defense against pathogens, including bacteria, fungi, and viruses, is known to rely on innate immunity, while in vertebrates, the innate immune system provides the first defense line against pathogens before activation of acquired immune response [1]
The activation of Toll pathway in vertebrate is initiated by Toll-like receptors (TLRs) binding to various pathogen associated molecular patterns (PAMPs), whereas in invertebrate, it is activated indirectly by Toll receptors binding to the cytokine-like molecule Spätzle (Spz) [7]
Our results revealed that the Toll signaling pathway in L. striatellus is potentially induced through the direct interaction between Toll and rice stripe virus (RSV)-nucleocapsid protein (NP)
Summary
Host defense against pathogens, including bacteria, fungi, and viruses, is known to rely on innate immunity, while in vertebrates, the innate immune system provides the first defense line against pathogens before activation of acquired immune response [1]. Various evolutionarily conserved signaling pathways mediate antiviral immunity, including small RNA interference (RNAi), Toll, the immune deficiency (IMD), and JAK-STAT [2, 3]. Toll Immune Pathway in Planthopper mainly rely on different pattern recognition receptors (PRRs), which recognize signature molecules of pathogens, known as pathogen associated molecular patterns (PAMPs) and induce downstream effectors against viral infection [4, 5]. The activation of Toll pathway in vertebrate is initiated by TLRs binding to various PAMPs, whereas in invertebrate, it is activated indirectly by Toll receptors binding to the cytokine-like molecule Spätzle (Spz) [7]. In Drosophila, the complex further trigger the phosphorylation and degradation of Cactus, freeing Dorsal or Dif (Dorsalrelated immunity factor) to transfer from the cytoplasm into the nucleus for the regulation of different antibacterial peptides (AMPs) expressions [12]
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