Phenotypic Plasticity through Transcriptional Regulation of the Evolutionary Hotspot Gene tan in Drosophila melanogaster

Phenotypic plasticity is the ability of a given genotype to produce different phenotypes in response to distinct environmental conditions. Phenotypic plasticity can be adaptive. Furthermore, it is thought to facilitate evolution. Although phenotypic plasticity is a widespread phenomenon, its molecular mechanisms are only beginning to be unravelled. Environmental conditions can affect gene expression through modification of chromatin structure, mainly via histone modifications, nucleosome remodelling or DNA methylation, suggesting that phenotypic plasticity might partly be due to chromatin plasticity. As a model of phenotypic plasticity, we study abdominal pigmentation of Drosophila melanogaster females, which is temperature sensitive. Abdominal pigmentation is indeed darker in females grown at 18°C than at 29°C. This phenomenon is thought to be adaptive as the dark pigmentation produced at lower temperature increases body temperature. We show here that temperature modulates the expression of tan (t), a pigmentation gene involved in melanin production. t is expressed 7 times more at 18°C than at 29°C in female abdominal epidermis. Genetic experiments show that modulation of t expression by temperature is essential for female abdominal pigmentation plasticity. Temperature modulates the activity of an enhancer of t without modifying compaction of its chromatin or level of the active histone mark H3K27ac. By contrast, the active mark H3K4me3 on the t promoter is strongly modulated by temperature. The H3K4 methyl-transferase involved in this process is likely Trithorax, as we show that it regulates t expression and the H3K4me3 level on the t promoter and also participates in female pigmentation and its plasticity. Interestingly, t was previously shown to be involved in inter-individual variation of female abdominal pigmentation in Drosophila melanogaster, and in abdominal pigmentation divergence between Drosophila species. Sensitivity of t expression to environmental conditions might therefore give more substrate for selection, explaining why this gene has frequently been involved in evolution of pigmentation.Author Summary: Environmental conditions can strongly modulate the phenotype produced by a particular genotype. This process, called phenotypic plasticity, has major implications in medicine and agricultural sciences, and is thought to facilitate evolution. Phenotypic plasticity is observed in many animals and plants but its mechanisms are only partially understood. As a model of phenotypic plasticity, we study the effect of temperature on female abdominal pigmentation in the fruit fly Drosophila melanogaster. Here we show that temperature affects female abdominal pigmentation by modulating the expression of tan (t), a gene involved in melanin production, in female abdominal epidermis. This effect is mediated at least partly by a particular regulatory sequence of t, the t_MSE enhancer. However we detected no modulation of chromatin structure of t_MSE by temperature. By contrast, the level of the active chromatin mark H3K4me3 on the t promoter is strongly increased at lower temperature. We show that the H3K4 methyl-transferase Trithorax is involved in female abdominal pigmentation and its plasticity and regulates t expression and H3K4me3 level on the t promoter. Several studies have linked t to pigmentation evolution within and between Drosophila species. Our results suggest that sensitivity of t expression to temperature might facilitate its role in pigmentation evolution.