Midgut-based resistance of Heliothis virescens to baculovirus infection mediated by phytochemicals in cotton

The decrease in susceptibility to polyhedrosis disease when Heliothis virescens larvae feed on cotton is profound, limiting the utility of baculoviruses for controlling noctuids on this important crop. We observed that the mortalities of H. virescens larvae challenged with a reporter-gene construct of Autographa californica M nucleopolyhedrovirus (AcMNPV-hsp70/lacZ) and fed either lettuce or artificial diet were ≈2.5-fold higher than that of cotton-fed insects. This decrease in susceptibility on cotton was observed following oral but not intrahemocoelic inoculation of virus, and it was negatively correlated with levels of foliar peroxidase. The rates of development of both infected and uninfected larvae also were correlated negatively with levels of foliar peroxidase, and hence, were significantly lower for insects fed cotton. When Calcofluor White M2R, an optical brightener reported to enhance the retention of AcMNPV-infected midgut cells, was included in inoculum administered orally to larvae, mortality levels were equivalent regardless of diet. These results suggest that sloughing of infected midgut cells occurred at a higher rate in insects that fed on cotton compared to the other two diets, and that midgut cell sloughing is the mechanism whereby susceptibility to mortal infection by AcMNPV-hsp70/lacZ is decreased on cotton. This conclusion is consistent with previous reports that ingestion of cotton can generate reactive oxygen species within the midgut lumen that may damage midgut epithelial cells. As far as we know, this is the first study to link resistance intrinsic to the physiology of the insect (e.g., developmental resistance) and resistance conferred by host plant chemistry to a single mechanism, i.e., midgut cell sloughing.