Royal jelly-like protein localization reveals differences in hypopharyngeal glands buildup and conserved expression pattern in brains of bumblebees and honeybees

Štefan Albert,Kornelia Grübel,Johannes Spaethe,Wolfgang Rössler

doi:10.1242/bio.20147211

Abstract

ABSTRACTRoyal jelly proteins (MRJPs) of the honeybee bear several open questions. One of them is their expression in tissues other than the hypopharyngeal glands (HGs), the site of royal jelly production. The sole MRJP-like gene of the bumblebee, Bombus terrestris (BtRJPL), represents a pre-diversification stage of the MRJP gene evolution in bees. Here we investigate the expression of BtRJPL in the HGs and the brain of bumblebees. Comparison of the HGs of bumblebees and honeybees revealed striking differences in their morphology with respect to sex- and caste-specific appearance, number of cells per acinus, and filamentous actin (F-actin) rings. At the cellular level, we found a temporary F-actin-covered meshwork in the secretory cells, which suggests a role for actin in the biogenesis of the end apparatus in HGs. Using immunohistochemical localization, we show that BtRJPL is expressed in the bumblebee brain, predominantly in the Kenyon cells of the mushroom bodies, the site of sensory integration in insects, and in the optic lobes. Our data suggest that a dual gland-brain function preceded the multiplication of MRJPs in the honeybee lineage. In the course of the honeybee evolution, HGs dramatically changed their morphology in order to serve a food-producing function.

Highlights

Glands serve manifold functions in insects ranging from reproduction, communication and food processing to defense and nest building (Chapman, 2012)
Honeybee Major royal jelly proteins (MRJPs) are recognized by anti-BtRJPL antibodies In the bumblebee hypopharyngeal glands (HGs), the antibody recognizes a polypeptide of 51–54 kDa, which is approximately the size found in immunoblots from head extracts of bumblebee queens and workers (Kupke et al, 2012)
BtRJPL is expressed in bumblebee brains We have previously shown that besides the HGs, BtMRJP mRNA is expressed in the brain of bumblebee workers, queens and drones, albeit to a lower extent (Kupke et al, 2012)

Summary

Introduction

Glands serve manifold functions in insects ranging from reproduction, communication and food processing to defense and nest building (Chapman, 2012). Hypopharyngeal glands (HGs) are specific to Hymenoptera (Cruz-Landim, 1998). It was hypothesized that the original function of HGs in food digestion and modification has been modified in the course of evolution into a nutritive, foodsecreting function in honeybees, which was accompanied by their growth (Kupke et al, 2012).

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