The brain is a vital organ in regulating complex social behaviors of honeybees including learning and memory. Knowledge of how brain membrane proteins and their phosphorylation underlie the age-related behavioral polyethism is still lacking. A hitherto age-resolved brain membrane proteome and phosphoproteome were reported in adult worker bees from two strains of honeybee (Apis mellifera ligustica): Italian bee (ITB) and Royal Jelly bee (RJB), a line selected from ITB for increased RJ outputs over 4 decades. There were 1079 membrane protein groups identified, and 417 unique phosphosites were located in 179 membrane protein groups mainly phosphorylated by kinase families of MAPKs, CDKs, and CK2. Age-resolved dynamics of brain membrane proteome and phosphoproteome are indicative of their correlation with the neurobiological requirements during the adult life of honeybee workers. To stimulate immature brain cell development in newly emerged bees (NEBs), the enriched functional classes associated with metabolism of carbohydrates, nucleosides, and lipids by the up-regulated proteins suggest their enhanced role in driving cell maturity of the brain. In nurse bees (NBs) and forager bees (FBs), a higher number of membrane proteins and phosphoproteins were expressed as compared to in the young stages, and the enriched signal transduction related pathways by the up-regulated proteins suggest their significances in sustaining the intensive information processing during nursing and foraging activities. Notably, RJB has shaped unique membrane proteome and phosphoproteome settings to consolidate nursing and foraging behaviors in response to decades of selection underpinning the elevated RJ yields. In RJB NBs, the enriched pathways of phosphatidylinositol signaling and arachidonic acid metabolism indicate a stronger olfaction sensation in response to larval pheromone stimulation. In RJB FBs, the enriched pathways related to signal processing such as SNARE interactions in vesicular transport, wnt signaling, TGF-beta signaling, and taurine and hypotaurine metabolism suggest an enhanced nerve sensitivity to prime the stronger tendency to pollen collection. Our data gain a novel insight into membrane proteome and phosphoproteome driven cerebral regulation of honeybee behaviors, which is potentially useful for further neurobiological investigation in both honeybees and other social insects.

中文翻译：

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脑膜蛋白质组和磷酸化蛋白质组揭示了与蜜蜂工人的护理和觅食行为有关的分子基础

大脑是调节蜜蜂复杂的社交行为（包括学习和记忆）的重要器官。仍然缺少关于脑膜蛋白及其磷酸化如何与年龄相关的行为多种族主义基础的知识。据报道，成年工蜂使用两种蜜蜂（Apis mellifera ligustica）：意大利蜂（ITB）和蜂王浆（RJB），迄今已解决年龄的脑膜蛋白质组和磷酸化蛋白质组。 4年。鉴定出1079个膜蛋白组，在179个膜蛋白组中有417个独特的磷酸位点，主要被MAPK，CDK和CK2的激酶家族磷酸化。脑膜蛋白质组和磷酸化蛋白质组的年龄分辨动力学表明它们与蜜蜂工人成年后的神经生物学需求相关。为了刺激新出现的蜜蜂（NEB）中未成熟的脑细胞发育，上调的蛋白质与碳水化合物，核苷和脂质的代谢相关的丰富的功能类别表明它们在驱动脑细胞成熟中的作用增强。与年轻阶段相比，在护理蜂（NBs）和觅食蜂（FBs）中表达了更高数量的膜蛋白和磷蛋白，并且上调的蛋白丰富的信号转导相关途径表明它们在维持高脂血症蜜蜂的过程中具有重要意义。在护理和觅食活动中进行密集的信息处理。尤其，RJB塑造了独特的膜蛋白质组和磷酸化蛋白质组设置，以巩固护理和觅食行为，以响应数十年的选择，从而提高RJ产量。在RJB NB中，磷脂酰肌醇信号传导和花生四烯酸代谢的丰富途径表明，响应幼虫信息素刺激，嗅觉更强。在RJB FBs中，与信号处理有关的丰富途径，例如囊泡运输中的SNARE相互作用，wnt信号传导，TGF-β信号传导以及牛磺酸和低牛磺酸代谢，提示神经敏感性增强，从而引发了更强的花粉收集趋势。我们的数据获得了对膜蛋白质组和磷酸化蛋白质组驱动的蜜蜂行为的大脑调节的新颖见解，