The Effect of Diet on Midgut and Resulting Changes in Infectiousness of AcMNPV Baculovirus in the Cabbage Looper, Trichoplusia ni

Abstract

Insecticide resistance has been reported in many important agricultural pests, and alternative management methods are required. Baculoviruses qualify as an effective, yet environmentally benign, biocontrol agent but their efficacy against generalist herbivores may be influenced by diet. However, few studies have investigated the tritrophic interactions of plant, pest, and pathogen from both a gene expression and physiological perspective. Here we use microscopy and transcriptomics to examine how diet affects the structure of peritrophic matrix (PM) in Trichoplusia ni larvae and consequently their susceptibility to the baculovirus, AcMNPV. Larvae raised on potato leaves had lower transcript levels for chitinase and chitin deacetylase genes, and possessed a thicker and more multi-layered PM than those raised on cabbage or artificial diet, which could contribute to their significantly lower susceptibility to the baculovirus. The consequences of these changes underline the importance of considering dietary influences on pathogen susceptibility in pest management strategies.

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

“…Transcript level inhibition of the juvenile hormone biosynthesis or alterations to its regulation is a common target attempted in recombinant baculoviruses developed as potential biopesticides [197,198]. Host genes associated with juvenile hormone regulation were noticeable among suppressed transcripts specially in the infected T. ni even when wild type AcMNPV strains were used [199] similar to observations made in our current study.…”

Susceptibility of the Gypsy Moth Lymantria dispar (Lepidoptera: Erebidae) to Nosema pyrausta (Microsporidia: Nosematidae)

“…Unfortunately, the sample size was not great enough to support the observations statistically, but we can speculate that insects in the rising phase are less susceptible to infection when fed with fresh birch leaves (resulting in microsporidia prevalence levels of 0–3.6%) as compared to artificial diet variants (4.3–9.5%). This suggestion fairly corresponds to the fact that feeding with an artificial diet suppresses insect resistance to alimentary infections, in particular, by decreasing the peritrophic membrane thickness [ 29 ]. Meanwhile, insects at the collapse phase display decreased fitness and their resistance to infections is lower in both cases, suggesting that diet type is not important in this case and optimal forage quality (exemplified by fresh birch leaves) does not facilitate resistance to the disease.…”

“…To induce depression of immune status, one half of both insect samples was pretreated with phenylthiourea (PTU; Merck, Darmstadt, Germany) which causes specific immunosuppression in insects by inhibition of the prophenoloxidase cascade [ 28 ]. Finally, all the experimental variants were split into two equal groups, one fed with natural forage (birch leaves) and another with an artificial diet, which is known to increase host susceptibility to alimentary infections [ 29 ].…”

Interaction of a Densovirus with Glycans of the Peritrophic Matrix Mediates Oral Infection of the Lepidopteran Pest Spodoptera frugiperda

“…Such developmental resistance of S. frugiperda has been also reported following baculovirus infections and a high synergism with Calcofluor was obtained at late instars (e.g., > 60-fold at 4th instar vs. 3 to 6-fold at 2nd and 3rd instars) [54]. The structure and the composition of the PM can vary as caterpillars grow and feed, or between populations, which might impact virus-PM interactions and consequently insect susceptibility [16,17,55]. Whether PM disruption results from mechanical stresses on chitin fibers similar to calcofluor and probably WGA lectins or from an enzymatic activity of the capsids (i.e., of VP4) remains to be analyzed more thoroughly.…”

“…The competition of the capsid with monosaccharides for binding the PM, suggests that food components could interfere with infection. Indeed, plants contain compounds that can interfere with PM synthesis, which has been shown to consequently affect baculovirus infection [55] (Chen et al, 2018). Regarding bacteria, it has been shown recently that the PM controls commensal bacteria, and conversely that its synthesis and integrity can be microbiota-dependent, i.e., the gut microbiota inducing the expression of components of the peritrophic matrix [62,63].…”