Antennal Proteome Reveals Deep-insight Into Molecular Basis Driving Antennal Function And Royal Jelly Secretion

The honeybees have evolved a delicate system of chemical communication to regulate their complex social interactions.Antennae,the principal olfactory organs of the honeybees,are sensitive to varieties of chemical signals such as pheromones and odours,and play fundamental roles in stimulating nursing and foraging behaviours.This behavioural stimulation facilitates brood pheromone recognition during larval feeding,and increases pollen collecting behaviour,which in turn stimulate Royal Jelly(RJ)secretion by nurse bees(NBs).Although the olfactory system is crucial for nursing and foraging behaviours,an indepth molecular mechanism by which the olfactory system influences these behaviours during task transition across the adult ages and comparison between the different honeybee stocks is not fully explored.To gain deep-insight into the functionality and molecular details of the antennae in driving increased RJ production,we characterized and compared antennal proteomes across the adult ages of Italian bees(ITBs)and Royal Jelly bees(RJBs),a line selected from ITBs for increasing RJ production.Unprecedented depth of proteome was attained with the identification of 5692 antennal proteins in both bee lines.The antennal proteome of adult workers is to support the general functions to drive physiological and ageresolved behavioural developments of worker bees in both bee lines.However,age-specific proteome ground plans have adapted to prime the distinct olfactory physiology of worker bees during their development.In young bees,the proteome plays key roles to stimulate antennal neural cell development and differentiation to support the olfactory system maturation.In NBs,the proteome enhances antennal sensitivity for facilitating brood pheromone recognition and stimulating nursing behaviour to take care of young larvae.In forager bees(FBs),the proteome plays vital role in boosting intensive sensing and processing of diverse signal stimuli and regulating cellular homeostasis during foraging activity by supplying synthesized protein and metabolic fuel.Notably,between samples of the same age,RJB has tailored distinct antennal proteome programs to drive nursing and foraging behaviours to underline the elevated RJ production in response to decades of selection.In NBs,a large number of functional classes related to energy metabolism and cellular homeostasis,and the highly abundant proteins enriched in energy metabolism in RJB imply that it has adapted its proteome to initiate different olfactory system and high RJ secretion in response to selection for enhanced RJ production.In FBs,the enriched functional classes and pathways related to energy metabolism such as fatty acid degradation,pyruvate metabolism,nucleobase-containing compound metabolic process,pyridine nucleotide metabolic process,and glyoxylate and dicarboxylate metabolism in RJB suggest an enhanced olfactory system to prime the stronger foraging behaviour to pollen collection.Our data not only contribute to elucidating the relationship between olfactory and behaviour-related changes,but also portrait a new perspective into the molecular mechanism underlying high RJ production by RJBs.