Transcriptional analysis of physiological pathways in a generalist herbivore: responses to different host plants and plant structures by the cotton bollworm, Helicoverpa armigera

The generalist cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae), can consume host plants in more than 40 families, and often utilizes several tissues of a single plant. It is believed that generalists owe their success to the deployment of various members of multigene families of detoxification and digestive enzymes, a strategy that may also be responsible for rapid evolution of insecticide resistance. However, studies of generalist adaptations have been limited to specific genes or gene families, and an overview of how these adaptations are orchestrated at the transcriptional level is lacking. We used Drosophila melanogaster Meigen gene homology to H. armigera-expressed sequence tags to identify key groups of genes and pathways differentially regulated in the gut of fifth instars after 2 days of feeding on a variety of food sources. A series of microarray hybridizations was performed following two alternating loop designs, one comparing the gut gene expression upon feeding on various hosts (cotton, bean, tobacco, and chickpea) and two artificial diets (pinto bean and wheat germ-based), whereas the second design compared the gut expression toward feeding on various plant structures within cotton (leaf, square, and boll). The transcriptional responses toward bean and tobacco feeding treatments were more closely related in comparison with the rest of the diets, whereas the gene expression profiles toward cotton leaf and square-feeding were highly similar. We furthermore found significant changes in several pathways not directly responsible for detoxification mechanisms. Genes involved in primary and secondary metabolism, environmental information processing, and cellular processes were found to be differentially expressed. In addition, regulation of xenobiotic metabolism and the extracellular matrix-receptor pathways appeared differentially regulated across feeding treatments. Three cytochrome P450 genes CYP6AE17, CYP6B6, and CYP9A17 grouped as part of a xenobiotic metabolism pathway, were up-regulated in the bean-feeding treatment, and down-regulated in both tobacco and cotton-feeding treatments. CYP4L11, CYP4L5, and CYP4S13 were differentially expressed upon feeding on different cotton plant structures. The present work provides host plant and plant structure-specific transcriptional responses in a lepidopteran herbivore, including pathways and gene candidates for future studies of H. armigera physiology under a more integrative ecologically meaningful framework.