DNA methyltransferase 3 participates in behavioral phase change in the migratory locust

DNA methylation plays important roles in the behavioral plasticity of animals. The migratory locust, Locusta migratoria, displays striking density-dependent phenotypic plasticity that can reversely transit between solitarious and gregarious phases. However, the role and the mechanism through which DNA methylation is involved in locust phase change remain unknown. Here, we investigated the expression levels of three DNA methyltransferase genes and their roles in the regulation of locust phase changes. All three Dnmt genes, namely, Dnmt1, Dnmt2 and Dnmt3 showed high expression levels in the brains of gregarious locusts. By contrast, only Dnmt3 transcript rapidly responded to population density changes, decreasing during the isolation of gregarious locusts and steadily increasing upon the crowding of solitarious locusts. Dnmt3 knockdown significantly reduced the phase-related locomotor activity, rather than the attraction index, in gregarious and crowded solitarious locusts. Transcriptome analysis showed that Dnmt3 knockdown upregulated the genes related to metabolism and transporting activity and downregulated those associated with oxidative stress response. The expression level of the phase-core transcriptional factor, hormone receptor HR3, was significantly suppressed in the brain after Dnmt3 knockdown. Moreover, there was significant overlap in the differentially expressed genes between Dnmt3 RNAi and HR3 RNAi data sets, suggesting HR3 may act as key transcriptional factor mediating Dnmt3-controlled gene expression profiles in locust brains. These findings suggest that Dnmt3 transcription is involved in locust behavioral transition, implying the possible roles of DNA methylation in phase-related phenotypic plasticity in locusts.