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<p>Animal behavior is linked to the gene regulatory network (GRN) coordinating gene expression in the brain. Eusocial honeybees, with their natural behavioral plasticity, provide an excellent model for exploring the connection between brain activity and behavior. Using single-nucleus RNA sequencing and spatial transcriptomics, we analyze the expression patterns of brain cells associated with the behavioral maturation from nursing to foraging. Integrating spatial and cellular data uncovered cell-type and spatial heterogeneity in GRN organization. Interestingly, the stripe regulon is explicitly activated in foragers’ small Keyon cells, which are implicated in spatial learning and navigation. When worker age is controlled in artificial colonies, <i>stripe</i> and its key targets remained highly expressed in the KC regions of bees performing foraging tasks. These findings suggest that specific GRNs coordinate individual brain cell activity during behavioral transitions, shedding light on GRN-driven brain heterogeneity and its role in the division of labor of social life.</p>

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Single-nucleus and spatial transcriptomics identify brain landscape of gene regulatory networks associated with behavioral maturation in honeybees

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年4月8日

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  • Xiaohuan Mu,
  • Zijing Zhang,
  • Qun Liu,
  • Jie Ma,
  • Yating Qin,
  • Haoyu Lang,
  • Yingying Zhang,
  • Nannan Zhang,
  • Qunfei Guo,
  • Pei Zhang,
  • Denghui Li,
  • Ruihua Zhang,
  • Qianyue Ji,
  • Aijun Jiang,
  • Yang Wang,
  • Shanshan Pan,
  • Xiawei Liu,
  • Xuemei Liu,
  • Jiahui Sun,
  • Yan Liu,
  • Hao Chen,
  • Li Zheng,
  • Liang Meng,
  • Haorong Lu,
  • He Zhang,
  • Yifan Zhai,
  • Qiye Li,
  • Junnian Liu,
  • Huanming Yang,
  • Jian Wang,
  • Xiaosong Hu,
  • Xun Xu,
  • Shanshan Liu,
  • Hao Zheng

摘要

Animal behavior is linked to the gene regulatory network (GRN) coordinating gene expression in the brain. Eusocial honeybees, with their natural behavioral plasticity, provide an excellent model for exploring the connection between brain activity and behavior. Using single-nucleus RNA sequencing and spatial transcriptomics, we analyze the expression patterns of brain cells associated with the behavioral maturation from nursing to foraging. Integrating spatial and cellular data uncovered cell-type and spatial heterogeneity in GRN organization. Interestingly, the stripe regulon is explicitly activated in foragers’ small Keyon cells, which are implicated in spatial learning and navigation. When worker age is controlled in artificial colonies, stripe and its key targets remained highly expressed in the KC regions of bees performing foraging tasks. These findings suggest that specific GRNs coordinate individual brain cell activity during behavioral transitions, shedding light on GRN-driven brain heterogeneity and its role in the division of labor of social life.