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<p>Pheromones are key modulators of reproductive behavior in fish, and certain odorant receptors (ORs) expressed in the olfactory epithelium act as receptors for sex pheromones. The northern snakehead (<i>Channa argus</i>) exhibits distinctive parental care behaviors, such as nest construction and brood guarding. It is likely that hormonal regulation during the breeding season upregulates the expression of olfactory receptors, thereby enhancing the sensitivity of <i>C. argus</i> to pheromones released by the opposite sex and ultimately promoting the initiation of reproductive behaviors. A total of 256 functional OR genes were identified from the <i>C. argus</i> genome, and these were distributed across four chromosomes. Transcriptome sequencing of whole-brain and olfactory rosette tissues from males during and after the breeding season showed a marked upregulation of the olfactory receptor gene <i>caor67</i> in the olfactory rosettes, as well as increased expression of prolactin (PRL) in the brain. The open reading frames (ORFs) of <i>caor67</i>, <i>prl</i>, <i>prlra</i>, <i>prlrb</i>, <i>stat5a</i>, and <i>stat5b</i> from northern snakehead were cloned and characterized. The expression of <i>caor67</i> is highest in the olfactory rosettes. During the breeding season, the expression of <i>caor67</i> in the male olfactory rosettes is significantly higher than in females. <i>prl</i> expression is relatively high in the pituitary, while <i>prlra</i> shows the highest expression in the gills, followed by the olfactory rosettes. <i>prlrb</i> has the highest expression in the olfactory rosettes, followed by the gills and kidney. In situ hybridization results show that the mRNA of <i>caor67</i>, <i>prlra</i>, and <i>prlrb</i> is expressed in the sensory epithelium of the <i>C. argus</i> olfactory rosettes, with expression detected in both ciliated and microvillous olfactory receptor neurons (ORNs). Co-localization of <i>caor67</i> with <i>prlra</i> and <i>prlrb</i> was observed in the ORNs of the olfactory rosettes. Recombinant <i>C. argus</i> PRL (rPRL) was expressed and purified, and functional assays confirmed that it interacts with both PRLRa and PRLRb to enhance phosphorylated STAT5 (pSTAT5) activity. Overexpression of PRLRa/PRLRb or STAT5a/STAT5b significantly increased <i>caor67</i> promoter-driven luciferase activity in vitro. Treatment with the JAK2 inhibitor TG101348, which blocks the JAK2-STAT5 signaling pathway, significantly reduced luciferase activity, indicating that PRL regulates the transcription of <i>caor67</i> via the PRLR-JAK2-STAT5 signaling pathway.</p>

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Prolactin–PRLR–STAT5 signaling upregulates a candidate pheromone receptor caor67 in the olfactory epithelium of northern snakehead (Channa argus)

  • 期刊论文

  • 发表日期：

    2026年4月13日

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  • Tianyu Jiang,
  • Chenpeng Zuo,
  • Likang Lyu,
  • Xiaojie Wang,
  • Donglei Sun,
  • Xiao Jing,
  • Xinlin Yang,
  • Xin Qi

摘要

Pheromones are key modulators of reproductive behavior in fish, and certain odorant receptors (ORs) expressed in the olfactory epithelium act as receptors for sex pheromones. The northern snakehead (Channa argus) exhibits distinctive parental care behaviors, such as nest construction and brood guarding. It is likely that hormonal regulation during the breeding season upregulates the expression of olfactory receptors, thereby enhancing the sensitivity of C. argus to pheromones released by the opposite sex and ultimately promoting the initiation of reproductive behaviors. A total of 256 functional OR genes were identified from the C. argus genome, and these were distributed across four chromosomes. Transcriptome sequencing of whole-brain and olfactory rosette tissues from males during and after the breeding season showed a marked upregulation of the olfactory receptor gene caor67 in the olfactory rosettes, as well as increased expression of prolactin (PRL) in the brain. The open reading frames (ORFs) of caor67, prl, prlra, prlrb, stat5a, and stat5b from northern snakehead were cloned and characterized. The expression of caor67 is highest in the olfactory rosettes. During the breeding season, the expression of caor67 in the male olfactory rosettes is significantly higher than in females. prl expression is relatively high in the pituitary, while prlra shows the highest expression in the gills, followed by the olfactory rosettes. prlrb has the highest expression in the olfactory rosettes, followed by the gills and kidney. In situ hybridization results show that the mRNA of caor67, prlra, and prlrb is expressed in the sensory epithelium of the C. argus olfactory rosettes, with expression detected in both ciliated and microvillous olfactory receptor neurons (ORNs). Co-localization of caor67 with prlra and prlrb was observed in the ORNs of the olfactory rosettes. Recombinant C. argus PRL (rPRL) was expressed and purified, and functional assays confirmed that it interacts with both PRLRa and PRLRb to enhance phosphorylated STAT5 (pSTAT5) activity. Overexpression of PRLRa/PRLRb or STAT5a/STAT5b significantly increased caor67 promoter-driven luciferase activity in vitro. Treatment with the JAK2 inhibitor TG101348, which blocks the JAK2-STAT5 signaling pathway, significantly reduced luciferase activity, indicating that PRL regulates the transcription of caor67 via the PRLR-JAK2-STAT5 signaling pathway.