Data from: 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.表型可塑性（Phenotypic plasticity）指特定基因型（genotype）响应不同环境条件产生多种表型（phenotype）的能力。表型可塑性可具有适应性，且被认为可促进进化进程。尽管表型可塑性是一种广泛存在的现象，但其分子机制仅处于逐步解析的初始阶段。 环境条件可通过修饰染色质结构（chromatin structure）影响基因表达，主要通过组蛋白修饰（histone modifications）、核小体重塑（nucleosome remodelling）或DNA甲基化（DNA methylation），这提示表型可塑性可能部分源于染色质可塑性（chromatin plasticity）。 我们以黑腹果蝇（Drosophila melanogaster）雌性腹部色素沉着（abdominal pigmentation）为表型可塑性研究模型，该性状具有温度敏感性。在18℃环境下培养的雌性个体，其腹部色素沉着较29℃时更深。该现象被认为具有适应性：低温下产生的深色色素沉着可提升机体体温。 本研究证实，温度可调控色素沉着相关基因tan（t）的表达，该基因参与黑色素（melanin）生成过程。在雌性腹部表皮中，该基因在18℃下的表达量为29℃下的7倍。 遗传实验表明，温度对tan基因表达的调控，是雌性腹部色素沉着可塑性的必要条件。 温度可调控tan基因增强子（enhancer）的活性，却不会改变其染色质的压缩状态，亦不会影响活性组蛋白标记H3K27ac的水平。 与之相反，tan基因启动子区域的活性组蛋白标记H3K4me3则会受到温度的显著调控。 参与该过程的组蛋白H3K4甲基转移酶（H3K4 methyl-transferase）大概率为Trithorax：我们证实该酶可调控tan基因的表达，以及其启动子区域的H3K4me3水平，同时也参与雌性腹部色素沉着及其可塑性的调控。 值得注意的是，此前已有研究证实，tan基因参与黑腹果蝇雌性腹部色素沉着的个体间差异，以及不同果蝇物种间腹部色素沉着的演化分化。因此，tan基因表达对环境条件的敏感性，可为自然选择提供更多作用底物，这也解释了为何该基因频繁参与色素沉着相关的演化过程。