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Reprogramming in the adult honeybee mushroom body induces neonicotinoid-associated glia remodeling

ABSTRACT: Mushroom bodies play important roles in honeybee learning and memory, We performed the high-throughput single-cell sequencing analysis of honeybee mushroom body cells to investigate the effects of thiacloprid on mushroom body cell allocation in the honeybee brain.

ORGANISM(S): Apis mellifera

PROVIDER: GSE271402 | GEO | 2025/12/31

REPOSITORIES: GEO

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Project description:As a matter of fact, honeybees are vital for the pollination of more than 80 crops of agricultural interest. However, population decline has become an important global issue causing significant concerns among agricultural experts and the broader public. For this, parasites are known to be the major culprits responsible for the losses of millions of honeybee colonies so far. Among these parasites, Varroa destructor has been identified as a major cause for global losses in Western honeybee (Apis mellifera) colonies. Hygienic behavior (HB), on the other hand, is a collective response by adult honeybees to defend against parasites and diseases that is known to involve in resistance towards Varroosis. Even with the efforts made to elucidate the molecular mechanism underlying HB, it is still not understood. In our study, we have studied the proteomic correlates to HB using a honeybee line (selected for Varroa-specific HB for over a decade in Germany). We sampled individual worker bees from this line that showed HB after closer infrared video observations and compared the proteomes of their mushroom bodies and antennae with those of workers that came from the same set of colonies but didn't show the behaviour. Furthermore, we compared the pupal hemolymph for worker bees of the selected HB line and a control line using state-of-the art techniques of proteomics. We identified a total of 8609 proteins (covered >55% of the honeybee proteome) from these three honeybee tissues. This is the most comprehensive proteomic study of the honeybee HB to date, and the first to focus on individual bees expressing Varroa-specific HB. These results have significantly advanced our knowledge on the biology underlining HB to a new level. The uniquely found functional classes and pathways by the proteins identified in each tissue suggest that hygienic bees have shaped distinct proteome settings to underpin the HB. Moreover, during analysis of pupal hemolymph proteome, the HB-line has adapted a unique strategy to boost an individual and social immunity and drove pupal organogenesis via energy metabolism and protein biosynthesis. Moreover, in the mushroom bodies of different HB phenotypic worker bees, the hygienic bees have enhanced their neuronal sensitivity to promote the execution of HB by activation of synaptic vesicles and calcium channel activities. Moreover, in the antennae of two HB phenotypic worker bees, the hygienic bees have demonstrated strengthening of their sensitivity associated with olfactory senses and signal transmissions, which is important to input a strong signal to the mushroom bodies and initiate HB. In conclusion, our novel findings have significantly extended our understandings of the molecular mechanisms that underline the HB to combat Varroa infestation. Furthermore, we identified a wide array of novel markers that are useful for accelerating marker associated selection of HB to aid in the natural resistance to a parasite blamed for a global decline in honeybee health.

Project description:Purpose: In Drosophila, we tried to determine the neural activity-dependent transcription controlled by Kdm4B. We conducted nuclear RNA-seq analysis in mushroom body in Drosophila, either in naive state or after optogenetic activation. Methods: The nuclei of mushroom body were collected by immunoprecipitation-based method (Hirano Y., et al, 2016, Nature Communications, also see extraction protocol below). mRNA was purified from the mushroom body nuclei with oligo dT magnetic beads, and used to prepare library. After deep sequencing in triplicate using illumine Hiseq X, the adaptors were trimmed via Trimommatic, followed by mapping to the Drosophila reference genome, dm6 from UCSC using STAR. The reads with low mapping quality below 8 and the non-primary mapped reads were eliminated. The filtered reads were analyzed with HTSeq-count to obtain numbers of the reads mapped on exons, which was further analyzed on R using DESeq2 Results: Using an optimized data analysis workflow, we mapped about 9-18 million reads for ChIP-seq, and 30-40 million reads for nuclear RNA-seq to Drosophila reference genome, dm6 In ChIP-seq, binding of all proteins was enriched nearby the transcriptional start site (TSS). The binding sites determined were 1,237 for CoRest-C, 2,717 for Rpd3, and 6,684 for CBP. Importantly, among CoRest-C binding sites, overlapping sites of CoRest-C and CBP were 1,038/1,237 (83.9%), those of CoRest-C and Rpd3 were 789/1,237 (63.8%), and those of CoRest-C, Rpd3, and CBP were 704/1,237 (56.9%), suggesting that these three proteins colocalize on the specific genomic regions In nuclear RNA-seq, we found that upregulation of gene expression is robust at 10-min after 5-min optogenetic activation. The genes showing significant difference were 2,702 at this time point, in which 1,582 genes showed increase, and the rest showed decrease in the expression. Among the 1,582 increased genes, 1,055 genes were bound by CBP, supporting the idea that CBP is an important factor in activity-dependent transcription. Furthermore, 338 was bound by CoRest-C, 254 of which showed colocalization with CBP and Rpd3. Conclusions: Our study represents activity-dependent transcription in mushroom body in Drosophila, which is mediated by Kdm4B.

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	GSE271402_Apis_bee_metadata.h5ad	Other
	GSE271402_RAW.tar	Raw
	filelist.txt	Txt

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Reprogramming in the adult honeybee mushroom body induces neonicotinoid-associated glia remodeling

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