Behind the scenes of Popillia japonica integrated pest management: differentially expressed gene analysis following different control treatments

Background: The Japanese beetle Popillia japonica is an invasive pest that is creating a major concern due to its spread and damaging potential. Native to Japan, it was introduced in the U.S.A. and the Azores during the twentieth century, and in mainland Europe in 2014. P. japonica is able to attack more than 400 plant species, including some of high economic importance, and the possible losses related to uncontrolled expansion in Europe are substantial. Numerous control measures are being developed to control this pest, with a specific focus on Integrated Pest Management and environmentally safe strategies. Aiming for a genetically informed optimization of the design of these control methods, we studied the gene expression response of the pest following exposure to three different treatments: deltamethrin-coated long lasting insecticidal nets, Bacillus thuringiensis and Metarhizium robertsii spores. Results: The treatment with insecticidal nets resulted in the differential expression of genes related to Ca2+ transport and CYP-based detoxification. Exposure to B. thuringiensis was associated with enrichment of gene ontology terms related to antimicrobial peptides and immune function, which suggested potential modulation of immune-related processes. Treatment with M. robertsii led to the production of antifungal peptides as well as an up-regulation of the Toll and MAPK pathways. Conclusions: These findings can be variously interpreted as a response of the insect to minimize the effects of the treatment at the molecular level (e.g. Ca2+ increase), as a direct attempt of the insect to combat the agent (e.g. antimicrobial peptides), or as part of a more complex interplay between the insect and the biological control agent (e.g. modulation of the immune system). In general terms, the response to the insecticidal nets and, partly, to B. thuringiensis, appears to arise from a direct interaction of the insecticide molecule, or toxin, with their targets at the molecular level. On the other hand, multiple gene pathways are modulated in the response to M. robertsii, suggesting a more diversified mode of action that impacts a broader spectrum of biological mechanisms, in line with the notion that the fungus actually grows and reproduces inside the insect host.