Abstract
Identifying proteome changes of honey bee embryogenesis is of prime importance for unraveling the molecular mechanisms that they underlie. However, many proteomic changes during the embryonic period are not well characterized. We analyzed the proteomic alterations over the complete time course of honey bee worker embryogenesis at 24, 48, and 72 h of age, using mass spectrometry-based proteomics, label-free quantitation, and bioinformatics. Of the 1460 proteins identified the embryo of all three ages, the core proteome (proteins shared by the embryos of all three ages, accounting for 40%) was mainly involved in protein synthesis, metabolic energy, development, and molecular transporter, which indicates their centrality in driving embryogenesis. However, embryos at different developmental stages have their own specific proteome and pathway signatures to coordinate and modulate developmental events. The young embryos (<24 h) stronger expression of proteins related to nutrition storage and nucleic acid metabolism may correlate with the cell proliferation occurring at this stage. The middle aged embryos (24-48 h) enhanced expression of proteins associated with cell cycle control, transporters, antioxidant activity, and the cytoskeleton suggest their roles to support rudimentary organogenesis. Among these proteins, the biological pathways of aminoacyl-tRNA biosynthesis, β-alanine metabolism, and protein export are intensively activated in the embryos of middle age. The old embryos (48-72 h) elevated expression of proteins implicated in fatty acid metabolism and morphogenesis indicate their functionality for the formation and development of organs and dorsal closure, in which the biological pathways of fatty acid metabolism and RNA transport are highly activated. These findings add novel understanding to the molecular details of honey bee embryogenesis, in which the programmed activation of the proteome matches with the physiological transition observed during embryogenesis. The identified biological pathways and key node proteins allow for further functional analysis and genetic manipulation for both the honey bee embryos and other eusocial insects.
Highlights
From the ‡Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Beijing, China
The identified biological pathways and key node proteins allow for further functional analysis and genetic manipulation for both the honey bee embryos and other eusocial insects
Western blotting analysis was performed to verify the expression of key node proteins in protein–protein interaction (PPI) networks-nucleoside diphosphate kinase (NDPK), lysyl-tRNA synthetase (LysRS), eEF1A, eukaryotic translation initiation factor 5A (eIF-5A), and ribosomal protein S11 (RPS11), the results showed that they weree consistent with the proteomics data (Fig. 9)
Summary
From the ‡Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, Beijing, China. Embryogenesis is an important period during which the body plan of adult honey bees (Apis mellifera L.) is formed This life stage, lasting 72 h, occurs during the egg laid by the queen before bees hatch as young larva. The honey bee has adapted an evolutionary strategy for better colony survival that makes it difficult to rear experimentally modified larvae and pupae within the colony [6, 7], nurse bees use acute judgment to identify and remove abnormal eggs or larvae [8]. Extending Embryonic Proteome of Honey Bee Worker much thinner than that of the fruit fly (Drosophila melonogastero) or the silk worm (Bombyx mori) (0.1– 0.25 m for honey bees compared with ϳ17 m for silk worm) [13, 14] These superiorities are quite promising for in vivo transgenic research on honey bee embryos
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