bric à brac (bab), a central player in the gene regulatory network that mediates thermal plasticity of pigmentation in Drosophila melanogaster

Drosophila body pigmentation has emerged as a major Evo-Devo model. Using two Drosophila melanogaster lines, Dark and Pale, selected from a natural population, we analyse here the interaction between genetic variation and environmental factors to produce this complex trait. Indeed, pigmentation varies with genotype in natural populations and is sensitive to temperature during development. We demonstrate that the bric à brac (bab) genes, that are differentially expressed between the two lines and whose expression levels vary with temperature, participate in the pigmentation difference between the Dark and Pale lines. The two lines differ in a bab regulatory sequence, the dimorphic element (called here bDE). Both bDE alleles are temperature-sensitive, but the activity of the bDE allele from the Dark line is lower than that of the bDE allele from the Pale line. Our results suggest that this difference could partly be due to differential regulation by AbdB. bab has been previously reported to be a repressor of abdominal pigmentation. We show here that one of its targets in this process is the pigmentation gene tan (t), regulated via the tan abdominal enhancer (t_MSE). Furthermore, t expression is strongly modulated by temperature in the two lines. Thus, temperature sensitivity of t expression is at least partly a consequence of bab thermal transcriptional plasticity. We therefore propose that a gene regulatory network integrating both genetic variation and temperature sensitivity modulates female abdominal pigmentation. Interestingly, both bDE and t_MSE were previously shown to have been recurrently involved in abdominal pigmentation evolution in drosophilids. We propose that the environmental sensitivity of these enhancers has turned them into evolutionary hotspots.

果蝇躯体色素沉着已成为进化发育生物学（Evo-Devo）领域的主流研究模型之一。本研究以从自然种群中筛选获得的两个黑腹果蝇（Drosophila melanogaster）品系——深色系（Dark）与浅色系（Pale）——为实验材料，解析遗传变异与环境因子共同调控该复杂性状的分子机制。事实上，自然种群中的色素沉着性状随基因型差异而呈现多样性，且在个体发育过程中对温度敏感。我们证实，在两个品系间表达存在差异且表达水平随温度变化的bric à brac（bab）基因，参与了深色系与浅色系品系间的色素沉着差异调控。两个品系在bab基因的调控序列——二态元件（本文命名为bDE）——上存在序列差异。两个bDE等位基因均表现出温度敏感性，但深色系品系的bDE等位基因活性低于浅色系品系的bDE等位基因。本研究结果显示，该活性差异部分源于AbdB（Abdominal-B）的差异化调控。此前已有研究表明，bab基因是腹部色素沉着的负调控因子。本研究证实，该过程中bab的靶标基因之一为色素沉着相关基因tan（t），其调控依赖于tan基因的腹部特异性增强子（t_MSE）。此外，两个品系中t基因的表达均受温度的显著调控。由此可见，t基因表达的温度敏感性至少部分源于bab基因的温度依赖性转录可塑性。综上，我们提出：整合了遗传变异与温度敏感性的基因调控网络，共同调控雌性果蝇的腹部色素沉着性状。值得注意的是，此前研究已证实，bDE与t_MSE这两个增强子在果蝇类群的腹部色素沉着进化过程中被反复招募利用。我们据此推测，这些增强子的环境敏感性使其成为了进化热点区域。