Apicultural Research Institute, College of Animal Science and Technology, Yangzhou University, Yangzhou, 225009, China.
Yunnan Animal Husbandry Station, Kunming, 650225, China.
BMC Genomics. 2024 Sep 30;25(1):912. doi: 10.1186/s12864-024-10817-x.
Hygienic behavior, a specialized form of immune response evolved in social insects, plays a crucial role in safeguarding colonies from disease spread. In honeybee colonies, such behavior typically entails the dual steps of uncapping and removal of unhealthy and deceased brood. Although in recent years, numerous studies have examined the development of hygienic behavior, the mechanisms underlying the division in the performance of uncapping and removal have yet to be sufficiently elucidated. In this regard, long non-coding RNAs (lncRNAs) have been evidenced to be engaged in regulating the physiological activities of honeybees; however, whether lncRNAs are likewise involved in the uncapping and removal tasks has not been clarified.
In this study, the strong hygienic Apis cerana worker bees were used and the processes of uncapping and removal behaviors in three colonies were assayed with freeze-killed brood in the field. We then sequenced the antennal RNAs of honeybees to identify differentially expressed lncRNAs and performed lncRNA-mRNA association analysis to establish the differences between uncapping and removal. We detected 1,323 differentially expressed lncRNAs in the antennae, and the findings of lncRNA-mRNA association analyses revealed that the target genes of differentially expressed lncRNAs between uncapping and removal worker bees were predominantly linked to response to stimulus, receptor activity, and synapse. Notably, among the lncRNAs enriched in cellular response to stimulus, XR_001766094.2 was exclusively expressed in the uncapping worker bees. Based on these findings, we hypothesize that XR_001766094.2 plays a key role in distinguishing uncapping from removal behaviors by responding to external stimulus, thereby suggesting that the division of hygienic behaviors is governed by differential thresholds of responsiveness to environmental cues.
We characterized differences in the uncapping and removal behaviors of worker bees from a perspective of lncRNAs. Uncapping bees may be equipped with a more rapid stimulatory response and more acute olfactory sensitivity, contributing to the rapid hygienic behavior in honeybee colonies. Our results thus establish a foundation for potential lncRNA-mediated gene expression regulation in hygienic behavior.
卫生行为是一种在社会性昆虫中进化而来的特殊免疫反应形式，对于保护群体免受疾病传播起着至关重要的作用。在蜜蜂群体中，这种行为通常包括双重步骤，即揭开和清除不健康和死亡的幼虫。尽管近年来，许多研究都检查了卫生行为的发展，但对于揭开和清除行为表现的分工机制尚未得到充分阐明。在这方面，长链非编码 RNA（lncRNA）已被证明参与调节蜜蜂的生理活动；然而，lncRNA 是否同样参与揭开和清除任务尚不清楚。
本研究中，使用了具有强烈卫生习性的中华蜜蜂工蜂，并在野外利用冷冻杀死的幼虫检测了三个群体中揭开和清除行为的过程。然后，我们对蜜蜂的触角 RNA 进行了测序，以鉴定差异表达的 lncRNA，并进行了 lncRNA-mRNA 关联分析，以确定揭开和清除之间的差异。我们在触角中检测到 1323 个差异表达的 lncRNA，lncRNA-mRNA 关联分析的结果表明，揭开和清除工蜂之间差异表达 lncRNA 的靶基因主要与对刺激的反应、受体活性和突触有关。值得注意的是，在对刺激的细胞反应中富集的 lncRNA 中，XR_001766094.2 仅在揭开工蜂中表达。基于这些发现，我们假设 XR_001766094.2 通过对外界刺激的反应在区分揭开和清除行为中起着关键作用，这表明卫生行为的分工是由对环境线索的响应差异决定的。
我们从 lncRNA 的角度描述了工蜂揭开和清除行为的差异。揭开蜜蜂可能具有更快的刺激反应和更敏锐的嗅觉敏感性，有助于蜜蜂群体中快速的卫生行为。我们的研究结果为卫生行为中潜在的 lncRNA 介导的基因表达调控奠定了基础。
