Abstract
Over the past decades, Helicoverpa armigera nucleopolyhedrovirus (HearNPV) has been widely used for biocontrol of cotton bollworm, which is one of the most destructive pest insects in agriculture worldwide. However, the molecular mechanism underlying the interaction between HearNPV and host insects remains poorly understood. In this study, high-throughput RNA-sequencing was integrated with label-free quantitative proteomics analysis to examine the dynamics of gene expression in the fat body of H. armigera larvae in response to challenge with HearNPV. RNA sequencing-based transcriptomic analysis indicated that host gene expression was substantially altered, yielding 3,850 differentially expressed genes (DEGs), whereas no global transcriptional shut-off effects were observed in the fat body. Among the DEGs, 60 immunity-related genes were down-regulated after baculovirus infection, a finding that was consistent with the results of quantitative real-time RT-PCR. Gene ontology and functional classification demonstrated that the majority of down-regulated genes were enriched in gene cohorts involved in energy, carbohydrate, and amino acid metabolic pathways. Proteomics analysis identified differentially expressed proteins in the fat body, among which 76 were up-regulated, whereas 373 were significantly down-regulated upon infection. The down-regulated proteins are involved in metabolic pathways such as energy metabolism, carbohydrate metabolism (CM), and amino acid metabolism, in agreement with the RNA-sequence data. Furthermore, correlation analysis suggested a strong association between the mRNA level and protein abundance in the H. armigera fat body. More importantly, the predicted gene interaction network indicated that a large subset of metabolic networks was significantly negatively regulated by viral infection, including CM-related enzymes such as aldolase, enolase, malate dehydrogenase, and triose-phosphate isomerase. Taken together, transcriptomic data combined with proteomic data elucidated that baculovirus established systemic infection of host larvae and manipulated the host mainly by suppressing the host immune response and down-regulating metabolism to allow viral self-replication and proliferation. Therefore, this study provided important insights into the mechanism of host-baculovirus interaction.
Highlights
To obtain an overview of Helicoverpa armigera nucleopolyhedrovirus (HearNPV) genes at the transcription level, we performed statistical analysis of the percentage of baculovirus reads among the total reads in each library, and the results indicated that viral mRNA molecules increased sharply during the infection process, even accounting for 15% of the total reads at 72 hpi (Fig. 1B)
From the ‡State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101; §University of Chinese Academy of Sciences, Beijing 100049; ¶State Key Laboratory of Virology and Joint Laboratory of Invertebrate Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071; and ʈGuangzhou Medical University, Guangzhou 510182, China
Survival rate analysis indicated that the life span of Helicoverpa armigera nucleopolyhedrovirus (HearNPV)-infected larvae was significantly shorter than that of naive larvae, proving the potent virulence and lethality of NPV used in this study
Summary
To obtain an overview of HearNPV genes at the transcription level, we performed statistical analysis of the percentage of baculovirus reads among the total reads in each library, and the results indicated that viral mRNA molecules increased sharply during the infection process, even accounting for 15% of the total reads at 72 hpi (Fig. 1B). CM is one of the key processes producing ATP in insects; we characterized the expression dynamics of CM-related genes during infection in the fat body of H. armigera larvae.
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