Proteomics Reveals the Molecular Underpinnings of Stronger Learning and Memory in Eastern Compared to Western Bees

Yu Fang,Fan Wu,Jianke Li,Lifeng Meng,Xinmei Huo,Han Hu,Mao Feng,Bin Han

doi:10.1074/mcp.ra117.000159

Abstract

The eastern (Apis cerana cerana, Acc) and western (Apis mellifera ligustica, Aml) honeybee are two major honeybee species. Surprisingly, little is known about the fundamental molecular neurobiology of brain suborgans of Acc and Aml. We characterized and compared the proteomes of mushroom bodies (MBs), antennal lobes (ALs) and optical lobes (OLs) in the brain of both species, and biologically validated the functions related to learning and memory. Acc and Aml have evolved similar proteome signatures in MBs and OLs to drive the domain-specific neural activities. In MBs of both species, commonly enriched and enhanced functional groups related to protein metabolism and Ca2+ transport relative to ALs and OLs, suggests that proteins and Ca2+ are vital for consolidating learning and memory via modulation of synaptic structure and signal transduction. Furthermore, in OLs of both species, the mainly enriched ribonucleoside metabolism suggests its vital role as second messenger in promoting phototransduction. Notably, in ALs of both species, distinct proteome settings have shaped to prime olfactory learning and memory. In ALs of Acc, this is supported by the enriched cytoskeleton organization to sustain olfactory signaling through modulation of plasticity in glomeruli and intracellular transport. In ALs of Aml, however, the enriched functional groups implicated in hydrogen ion transport are indicative of their importance in supporting olfactory processes by regulation of synaptic transmission. The biological confirmation of enhanced activities of protein metabolism and signal transduction in ALs and MBs of Acc relative to in Aml demonstrates that a stronger sense of olfactory learning and memory has evolved in Acc. The reported first in-depth proteome data of honeybee brain suborgans provide a novel insight into the molecular basis of neurobiology, and is potentially useful for further neurological studies in honeybees and other insects.

Highlights

The honeybee brain, a very small organ in size comprising 960,000 neurons, is a part of the central nervous system (CNS) that regulates social biology including social behavior, From the ‡Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Science, Beijing 100093, China
Mushroom bodies (MBs) are the highest-order in the CNS, which integrates massive information streams from various sensory organs to form associated memory [14], whereas antennal lobes (ALs) and optical lobes (OLs) are primary centers where olfactory information detected by the antennae is processed and visual cues are received from the compound eyes [15]
Similar region-specific proteomic settings of mushroom bodies (MBs) and OLs have been developed in both honeybee species to achieve their distinct roles in driving neuronal biology

Summary

Introduction

The honeybee brain, a very small organ in size comprising 960,000 neurons, is a part of the central nervous system (CNS) that regulates social biology including social behavior, From the ‡Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Science, Beijing 100093, China. In the case of neuropeptides, tachykinin-related peptide is preferentially expressed in MBs and some ALs and OLs neurons, where it is implicated in regulating the activity of neuronal circuits [24, 25] These observations are a manifestation that the honeybee brain has a ‘module-functionalization’ which is like the tuning of regular neural activity in the human brain [26, 27]. Several large-scale proteome works have been performed on honeybee brain to reveal the molecular mechanisms that drive the neural activity in Aml (28 –30). They were performed only in mushroom body and whole brain tissue. This work, we believe will be used as a potentially important resource and new knowledge for further neuronal activity functional investigations in more specific anatomical regions of honeybee and other insects’ brain

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