PLANT-MEDIATED EFFECTS ON INSECT-VIRUS INTERACTIONS

Open Access
- Author:
- Plymale, Ruth
- Graduate Program:
- Entomology
- Degree:
- Doctor of Philosophy
- Document Type:
- Dissertation
- Date of Defense:
- June 23, 2006
- Committee Members:
- Kelli Hoover, Committee Chair/Co-Chair
Diana Lynn Cox Foster, Committee Member
Gary Felton, Committee Member
Kelly Johnson, Committee Member
A Daniel Jones, Committee Member - Keywords:
- Heliothis virescens
peritrophic matrix
tritrophic interactions
biological control
baculovirus
pathogenesis - Abstract:
- The effects of host plants on baculoviral efficacy have been well documented; consumption of particular host plants often renders insect herbivores less susceptible to viral disease. Ingestion of cotton (Gossypium hirsutum L.) foliage in the first through third instars prior to oral viral inoculation in the fourth instar significantly reduced mortality of Heliothis virescens F. by Autographa californica nucleopolyhedrovirus (AcNPV). A construct of AcNPV that expresses lacZ under the control of the hsp70 promoter of Drosophila (AcNPV-hsp70/lacZ) was used to examine viral infection in vivo. Larvae that consumed cotton foliage in the first 8 h of the fourth instar prior to viral inoculation experienced a significant reduction in both mortality and percentage of larvae with foci of infection, compared with larvae fed artificial diet. Although cotton ingested prior to inoculation significantly reduced the percentage of larvae with midgut infection foci (indicated by lacZ signaling), there was no difference in the percentage of larvae possessing systemic tracheal infection foci, compared with larvae fed artificial diet. These results support the hypothesis that ingested cotton foliage hinders establishment of midgut infections in H. virescens, perhaps by modifying midgut physiology or by direct antagonism between virions and foliage components. This effect may not be limited to cotton, since other host plants of H. virescens (tobacco and oakleaf lettuce) also significantly reduced larval susceptibility to AcNPV when consumed prior to viral inoculation. The peritrophic matrix (PM) of herbivorous insects lines the midgut, protecting it from damage by ingested plant material. A significantly thicker PM was observed in cotton-fed larvae compared with artificial diet-fed larvae, suggesting that this thickened PM protects the midgut cells from damage by ingested foliage and secondarily provides protection from ingested pathogens. Disruption of the PM by the metalloprotease enhancin in cotton-fed larvae restored larval susceptibility to the level of diet-fed larvae. When viral pathogenesis was examined using AcNPV-hsp70/lacZ to indicate AcNPV infection, lacZ signaling appeared in larvae fed artificial diet+enhancin significantly earlier and in a greater proportion of larvae, compared with larvae fed untreated artificial diet. Thus, the PM appears to be a barrier to baculoviral infection in cotton-fed H. virescens larvae and may be a significant factor determining pathogen success by influencing establishment of midgut infections. Although the ability of host plants to influence larval susceptibility to baculoviral infection is well-known, the influence on viral pathogenicity of inducing systemic acquired resistance in host plants has not been previously reported. SAR was induced in cotton foliage by the plant elicitor benzo-(1, 2, 3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH). BTH application significantly increased foliar peroxidase activity and total phenolic levels, but did not alter catecholic phenolic levels. Moreover, consumption of SAR-induced foliage did not affect H. virescens pupal mass or larval mortality by AcNPV as compared to consumption of untreated foliage. Thus, activators of SAR like BTH and baculoviruses are likely to be compatible components of an IPM system. Further, the colony source of H. virescens significantly influenced larval mortality. We examined the influence of food consumed prior to viral inoculation on larval mortality of H. virescens from three different lab colonies, designated as NCSU97, AGR and NCSU02. The NCSU97 colony had not had field-collected individuals added since its establishment five years prior. In contrast, the AGR and NCUS02 colonies had field-collected individuals added within a year of experimentation. Larvae from the AGR and NCSU02 colonies fed artificial diet were significantly less susceptible to AcNPV infection than artificial diet-fed NCSU97 larvae; the mechanism regulating this decreased susceptibility appears to be restricted to the midgut environment. This is the first report detailing the influence of ingested cotton foliage on baculoviral pathogenesis in H. virescens. The observations that ingestion of cotton foliage alters PM structure and reduces midgut viral infections suggest possible mechanisms of host plant influence on pathogens that infect through the midgut. Understanding the interactions between ingested foliage and insect pathogens is likely to become more important as pathogens are used more widely as biocontrol agents. Further, these results showcase the ability of the PM to protect insects from ingested pathogens and indicate that the PM is a potentially important pest control target.