Transcriptional Responses of the Trichoplusia ni Midgut to Oral Infection by the Baculovirus Autographa californica Multiple Nucleopolyhedrovirus

Abstract

Baculoviruses are large double-stranded DNA viruses that are virulent pathogens of certain insect species. In a natural host, Trichoplusia ni, infection by the model baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) begins when the occluded form of the virus disassembles in the midgut and virions infect midgut epithelial cells to establish the primary phase of the infection. To better understand the primary phase of the AcMNPV infection cycle, newly molted 5th-instar T. ni larvae were orally infected with AcMNPV occlusion bodies and the transcriptional responses of the T. ni midgut were analyzed at various times from 0 to 72 h postinfection, using transcriptome sequencing analysis and a T. ni reference genome. The numbers of differentially expressed host genes increased as the infection progressed, and we identified a total of 3,372 differentially expressed T. ni transcripts in the AcMNPV-infected midgut. Genes encoding orthologs of HMG176, atlastin, and CPH43 were among the most dramatically upregulated in response to AcMNPV infection. A number of cytochrome P450 genes were downregulated in response to infection. We also identified the effects of AcMNPV infection on a large variety of genes associated with innate immunity. This analysis provides an abundance of new and detailed information on host responses to baculovirus infection during the primary phase of the infection in the midgut and will be important for understanding how baculoviruses establish productive infections in the organism. IMPORTANCE Baculoviruses are virulent pathogens of a number of important insect pest species. In the host Trichoplusia ni, infection begins in the midgut when infectious virions of the occlusion-derived virus (ODV) phenotype enter and subsequently replicate in cells of the midgut epithelium. A second virion phenotype (budded virus [BV]) is produced there, and BV mediates systemic infection of the animal. Most prior detailed studies of baculovirus infections have focused on BV infections of cultured cells. In this study, we examined the transcriptional responses of the T. ni midgut to infection by ODV of the baculovirus AcMNPV and identified a variety of host genes that respond dramatically to viral infection. Understanding the transcriptional responses of the host midgut to viral infection is critically important for understanding the biphasic infection in the animal as a whole.

A tale of two transcriptomic responses in agricultural pests via host defenses and viral replication

“…5b). Contrasting to the overall observations made by Shrestha et al, (2019) during the midgut infection, the hemolymph of both hosts in our study during systemic infection appear to clearly induce transcripts associated with oxidative stress while suppressing those related to hemostatis, chitin metabolism, and tracheal development.…”

“…2). This is consistent with the trend observed in previous transcriptomic studies in cell cultures of AcMNPV-infected S. frugiperda and T. ni [33,34,36,45,46]. Interestingly, we see extensive similarities across multiple biological processes as deduced from the functional attributes of DETs in each species, suggesting a shared host response to the AcMNPV pathogen.…”

Resource quality determines the evolution of resistance and its genetic basis

“…The first was that a single class of protein was overrepresented for the genes that were significantly associated with resistance on the common garden diet. This was an oxygenase and is of interest as many oxidoreductases have been previously linked to insect resistance (Chen et al, 2014;Nguyen, Nielsen, & Reid, 2013;Shrestha et al, 2019;Sun et al, 2012 Cory, 2017;Gebhardt, Eberle, Radtke, & Jehle, 2014).…”

“…The first was that a single class of protein was overrepresented for the genes that were significantly associated with resistance on the common garden diet. This was an oxygenase and is of interest as many oxidoreductases have been previously linked to insect resistance (Chen et al., 2014; Nguyen, Nielsen, & Reid, 2013; Shrestha et al., 2019; Sun et al., 2012). Oxidative stress induced by tissue damage during viral infection appears to be a ubiquitous pathology, implicating antioxidant enzymes in modulating immune function and resistance to viruses including influenza A infection in humans (reviewed in Camini, da Silva Caetano, Almeida, & de Brito Magalhães, 2017; Liu et al., 2017).…”

“…However, a single protein class (oxygenase) was highly enriched (12.16-fold, adjusted p-value = .021). This is of note as a recent finding associated a down regulation of cytochrome P450 with baculovirus infection, suggesting a key role of oxygenase enzymes in baculovirus resistance(Shrestha et al, 2019). A full list of all significantly associated genes is provided(Table S4).…”