Proteome Analysis Unravels Mechanism Underling the Embryogenesis of the Honeybee Drone and Its Divergence with the Worker (Apis mellifera lingustica)

Abstract

The worker and drone bees each contain a separate diploid and haploid genetic makeup, respectively. Mechanisms regulating the embryogenesis of the drone and its mechanistic difference with the worker are still poorly understood. The proteomes of the two embryos at three time-points throughout development were analyzed by applying mass spectrometry-based proteomics. We identified 2788 and 2840 proteins in the worker and drone embryos, respectively. The age-dependent proteome driving the drone embryogenesis generally follows the worker's. The two embryos however evolve a distinct proteome setting to prime their respective embryogenesis. The strongly expressed proteins and pathways related to transcriptional-translational machinery and morphogenesis at 24 h drone embryo relative to the worker, illustrating the earlier occurrence of morphogenesis in the drone than worker. These morphogenesis differences remain through to the middle-late stage in the two embryos. The two embryos employ distinct antioxidant mechanisms coinciding with the temporal-difference organogenesis. The drone embryo's strongly expressed cytoskeletal proteins signify key roles to match its large body size. The RNAi induced knockdown of the ribosomal protein offers evidence for the functional investigation of gene regulating of honeybee embryogenesis. The data significantly expand novel regulatory mechanisms governing the embryogenesis, which is potentially important for honeybee and other insects.

Molecular insights into the enhanced performance of royal jelly secretion by a stock of honeybee (Apis mellifera ligustica) selected for increasing royal jelly production

“…Proteomics is becoming an important tool for describing bee biology at the molecular level (Zewdu Ararso et al 2018). The molecular basis of different organs and tissues that allow bees to perform their biological tasks has been explained on the proteome scale, for example in the brain (Hernandez et al 2012;Chan et al 2013;Han et al 2015;Han et al 2017;Meng et al 2018), hemolymph (Ararso et al 2018), embryo (Fang et al 2014;Fang et al 2015), antennae in Varroa resistance (Parker et al 2012;Hu et al 2016), and venom (Matysiak et al 2014;Matysiak et al 2016;Matysiak et al 2017).…”

Toward an Upgraded Honey Bee (Apis mellifera L.) Genome Annotation Using Proteogenomics

“…While this is no doubt a more accurate annotation, proteomics studies which utilize it still suffer from high rates of missed identifications relative to other model organisms. 17 Some recent honey bee proteomics publications that used modern instrumentation 18,19,20 have achieved identifications approaching the numbers reported in Chan et al (2013), 10 but have not exceeded them.…”

PROTEINS OF THE INTEGUMENTARY SYSTEM OF THE HONEYBEE, Apis mellifera

“…The association of these studies with protein analysis and identification, however, is needed to confirm the authenticity of the gene products. So far, to our knowledge, the following proteomic studies on Apis mellifera focused on hypopharyngeal glands (Feng et al., ; Jianke et al., ) and their secretion (Santos et al., ), royal jelly (Furusawa et al., ), brain (Hummon et al., ; Uno et al., ; Hernandez et al, ), body parts or the whole body of adult bees performing nursing or foraging tasks (Schippers et al., ; Wolschin and Amdam, , b), embryos (Li et al., ; Fang et al., , ), and during embryo–larva transition (Gala et al., ) have been developed. Here, we used two‐dimensional gel electrophoresis (2‐DE) and matrix‐assisted laser desorption (MALDI) time of flight (TOF) MS to identify proteins expressed in the developing integument of honeybee workers.…”