Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum

Transcript patterns elicited in response to hosts can reveal how fungi recognize suitable hosts and the mechanisms involved in pathogenicity. These patterns could be fashioned by recognition of host-specific topographical features or by chemical components displayed or released by the host. We investigated this in the specific locust pathogen Metarhizium anisopliae var. acridum. Only host (Schistocerca gregaria) cuticle stimulated the full developmental program of germination and differentiation of infection structures (appressoria). Cuticle from beetles (Leptinotarsa decimlineata) repressed germination while cuticle from hemipteran bugs (Magicicada septendecim) allowed germination but only very low levels of differentiation, indicating that the ability to cause disease can be blocked at different stages. Using organic solvents to extract insects we identified a polar fraction from locusts that allowed appressorial formation against a flat plastic (hydrophobic) surface. Microarrays comprising 1,730 expressed sequence tags were used to determine if this extract elicits different transcriptional programs than whole locust cuticle or nonhost extracts. Of 483 differentially regulated genes, 97% were upregulated. These included genes involved in metabolism, utilization of host cuticle components, cell survival and detoxification, and signal transduction. Surprisingly, given the complex nature of insect epicuticle components and the specific response of M. anisopliae var. acridum to locusts, very similar transcript profiles were observed on locust and beetle extracts. However, the beetle extract cluster was enriched in genes for detoxification and redox processes, while the locust extract upregulated more genes for cell division and accumulation of cell mass. In addition, several signal transduction genes previously implicated in pathogenicity in plant pathogens were only upregulated in response to locust extract, implying similarities in the regulatory circuitry of these pathogens with very different hosts.