Phosphoproteomic basis of neuroplasticity in the antennal lobes influences the olfactory differences between A. mellifera and A. cerana honeybees

The honeybee species A. mellifera and A. cerana have evolved substantial differences in olfactory-driven behaviors and in peripheral olfactory systems. Knowledge of the central nervous system regulating these olfaction differences is limited, however. We compared the phosphoproteome of the antennal lobes (ALs, the primary olfactory neuropil) of A. mellifera and A. cerana, and identified a total of 2812 phosphopeptides carrying 2971 phosphosites from 1265 phosphoproteins. Of these, 76% of the phosphoproteins were shared by both species, which were mainly presynapse and cytoskeleton components, and were involved in signal transduction and neurotransmitter secretion. This finding indicates the fundamental role of protein phosphorylation in regulating signal transduction in the ALs. The mTOR signaling pathway, the phagosome pathway, and the autophagy pathway, which are important in protein metabolism, were enriched, suggesting glomeruli plasticity and olfactory processing are intensively modulated by phosphorylation via these pathways. Compared with A. mellifera, 107 phosphoproteins associated with protein metabolism and transport were uniquely expressed in A. cerana, indicating the protein synthesis-dependent synaptic plasticity is enhanced in A. cerana to facilitate the processing of more complex floral odor clues in mountain foraging areas. This finding is further supported by the significantly upregulated key phosphoproteins of the mTOR signaling pathway in A. cerana ALs. These results provide insights into the phosphoproteomic basis of neuroplasticity that is coupled with the divergent evolution of bees in different environments.