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Transcriptome analysis of Apis mellifera antennae reveals molecular divergence underlying the division of labor in worker bees

ABSTRACT: Olfaction system plays a fundamental role in mediating insect behavior. Besides, the division of queen, worker and drone, honeybee also exhibit an age-dependent division of labor. Worker bees perform discrete sets of behaviors throughout their lifespan. These behavioral states rely on the sense of the environments and chemical communications via their olfactory system - antennae. However, the olfactory adaption mechanism of workers in these processes of behavioral development is still unclear. In this study, we conducted a comprehensive and quantitative analysis of gene expression in Apis mellifera antenna of newly emerged workers, nurses, foragers, and defenders using RNA-seq. We found that antennae tissues continue to develop after transformation from pupae to adult. Additionally, we identified both developmental and labor-division specific expressed genes. We validated the unexpected discovery of major royal jelly protein genes, which are highly and specifically expressed in nurse honeybee workers. We further identified and validated that significant alternative splicing events are also involved in the development and division of labor. These findings provided a comprehensive transcriptome profile and new perspective into the molecular mechanism underlying honeybee division of labor.

ORGANISM(S): Apis mellifera

PROVIDER: GSE221246 | GEO | 2024/10/24

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:Olfaction and chemical communication are fundamental for coordination in insect societies, especially in species forming large colonies. Reproductive and task partitioning suggest that colony members belonging to different castes or subcastes or performing different tasks during their life (polyethism) may produce different semiochemicals and be differently sensitive to the variety of pheromones and/or environmental odours. The main peripheral olfactory organs are the antennal chemosensilla, where the early olfactory processes take place. At this stage, members of two different families of soluble chemosensory proteins (Odorant Binding Proteins -OBPs-, Chemosensory Proteins -CSPs-) show a remarkable affinity for different odorants and act as carriers while a further family, the Niemann Pick type C2 proteins (NPC2) may have a similar function, although this has not been fully demonstrated. Sensillar lymph also contains Odorant degrading enzymes (ODEs) which are involved in inactivation through degradation of the chemical signals, once the message is conveyed. Despite their importance in chemical communication, poor is known about how proteins involved in peripheral olfaction and, more generally antennal proteins, differ in honeybees of different caste, task and age. Here we investigate for the first time, using a shotgun proteomic approach, the antennal profile of honeybee of different castes (queens and workers) and of workers performing different tasks (nursers, guards and foragers) by controlling for the potential confounding effect of age. Regarding olfactory proteins, major differences were observed between queens and workers, some of which were found to be more abundant in queens (OBP3, OBP18, NPC2-1) and others to be more abundant in workers (OBP15, OBP21, CSP1, CSP3); while between workers performing different tasks, OBP14 was more abundant in nurses with respect to guards and foragers, and two ODEs were more abundant in guards with respect to workers of 2nd week. Apart from proteins involved in olfaction, we have found that the antennal proteomes are mainly characterized by castes and tasks, while age has a limited effect on antennal protein profile.

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Transcriptome analysis of Apis mellifera antennae reveals molecular divergence underlying the division of labor in worker bees

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