Proteomic Analysis Reveals the Molecular Underpinnings of Mandibular Gland Development and Lipid Metabolism in Two Lines of Honeybees (Apis mellifera ligustica)

• Published in: Journal of proteome research 2016-09, Vol.15 (9), p.3342-3357
• Main Authors: Huo, Xinmei, Wu, Bin, Feng, Mao, Han, Bin, Fang, Yu, Hao, Yue, Meng, Lifeng, Wubie, Abebe Jenberie, Fan, Pei, Hu, Han, Qi, Yuping, Li, Jianke
• Format: Article
• Language: English
• Subjects: Animals; Bees - metabolism; Carbohydrate Metabolism; Insect Proteins - analysis; Life Cycle Stages; Lipid Metabolism; Pheromones; Proteome - analysis; Proteomics; Species Specificity; Submandibular Gland - growth & development; Submandibular Gland - metabolism
• ISSN: 1535-3893; 1535-3907
• DOI: 10.1021/acs.jproteome.6b00526

The mandibular glands (MGs) of honeybee workers are vital for the secretion of lipids, for both larval nutrition and pheromones. However, knowledge of how the proteome controls MG development and functionality at the different physiological stages of worker bees is still lacking. We characterized and compared the proteome across different ages of MGs in Italian bees (ITBs) and Royal Jelly (RJ) bees (RJBs), the latter being a line bred for increasing RJ yield, originating from the ITB. All 2000 proteins that were shared by differently aged MGs in both bee lines (>4000 proteins identified in all) were strongly enriched in metabolizing protein, nucleic acid, small molecule, and lipid functional groups. The fact that these shared proteins are enriched in similar groups in both lines suggests that they are essential for basic cellular maintenance and MG functions. However, great differences were found when comparing the proteome across different MG phases in each line. In newly emerged bees (NEBs), the unique and highly abundant proteins were enriched in protein synthesis, cytoskeleton, and development related functional groups, suggesting their importance to initialize young MG development. In nurse bees (NBs), specific and highly abundant proteins were mainly enriched in substance transport and lipid synthesis, indicating their priority may be in priming high secretory activity in lipid synthesis as larval nutrition. The unique and highly abundant proteins in forager bees (FBs) were enriched in lipid metabolism, small molecule, and carbohydrate metabolism. This indicates their emphasis on 2-heptanone synthesis as an alarm pheromone to enhance colony defense or scent marker for foraging efficiency. Furthermore, a wide range of different biological processes was observed between ITBs and RJBs at different MG ages. Both bee stocks may adapt different proteome programs to drive gland development and functionality. The RJB nurse bee has reshaped its proteome by enhancing the rate of lipid synthesis and minimizing degradation to increase 10-hydroxy-2-decenoic acid synthesis, a major component of RJ, to maintain the desired proportion of lipids in increased RJ production. This study contributes a novel understanding of MG development and lipid metabolism, and a potential starting point for lipid or pheromone biochemists as well as developmental geneticists.