Integrative Proteomic and Phosphoproteomic Analyses Revealed Complex Mechanisms Underlying Reproductive Diapause in Bombus terrestris Queens

Abstract

Reproductive diapause is an overwintering strategy for Bombus terrestris, which is an important pollinator for agricultural production. However, the precise mechanisms underlying reproductive diapause in bumblebees remain largely unclear. Here, a combination analysis of proteomics and phosphoproteomics was used to reveal the mechanisms that occur during and after diapause in three different phases: diapause (D), postdiapause (PD), and founder postdiapause (FPD). In total, 4655 proteins and 10,600 phosphorylation sites of 3339 proteins were identified. Diapause termination and reactivation from D to the PD stage were characterized by the upregulation of proteins associated with ribosome assembly and biogenesis, transcription, and translation regulation in combination with the upregulation of phosphoproteins related to neural signal transmission, hormone biosynthesis and secretion, and energy-related metabolism. Moreover, the reproductive program was fully activated from PD to the FPD stage, as indicated by the upregulation of proteins related to fat digestion and absorption, the biosynthesis of unsaturated fatty acids, fatty acid elongation, protein processing in the endoplasmic reticulum, and the upregulation of energy-related metabolism at the phosphoproteome level. We also predicted a kinase–substrate interaction network and constructed protein–protein networks of proteomic and phosphoproteomic data. These results will help to elucidate the mechanisms underlying the regulation of diapause in B. terrestris for year-round mass breeding.

Comparative 4D Label-Free Quantitative Proteomic Analysis of Bombus terrestris Provides Insights into Proteins and Processes Associated with Diapause

“…Metabolic depression is heightened by inhibitions within mitochondria during diapause [33]. However, the sustained reduction in oxidative phosphorylation in the post-diapause phase compared to the diapause phase seems difficult to understand, but the same results have also been reported in our previous study, which may require further investigation [10].…”

“…B. terrestris has been mass-reared year-round and used commercially in greenhouses for crop pollination since the 1980s, and this species is used worldwide to increase the yield and quality of crops. A thorough understanding of the diapause mechanism is therefore of great significance for large-scale year-round breeding of bumblebees [ 10 , 11 ]. Changes in the B. terrestris transcriptome indicate that diapause is associated with nutrient storage, stress resistance, core metabolism, hormone signaling, and various cellular pathways [ 2 ].…”

“…ITRAQ proteomic analysis was employed to analyze the differentially abundant proteins (DAPs) during the pre-diapause, diapause, and post-diapause stages during summer diapause of adult Galeruca daurica [ 14 ]. Tandem mass tags labeling proteomic analysis was conducted to analyze the metabolic regulation of adult reproductive diapause in Drosophila suzukii females and B. terrestris [ 10 , 11 , 15 ]. Label-free quantitative proteomics revealed molecular evidence for the consequences and benefits of mating, as well as novel insights into preparation, survival, and recovering from diapause in B. terrestris queen hemolymph, but only 129 proteins were identified [ 16 ].…”

Transcriptome Analysis Provides Insights into Water Immersion Promoting the Decocooning of Osmia excavata Alfken

“…CO 2 is a ubiquitous sensory cue that affects the behavior, physiology, metabolism, and survival of insects [29,30]. For example, the increase in CO 2 concentration in the nests of honey bees and bumble bees causes their fanning activity [31,32]; CO 2 treatment induces postdiapause in bumble bees [33]; in Drosopbila melanogaster, CO 2 cues are thought to play a role in selecting food sources [34]. The larvae of cowpea bruchids respond to low oxygen by coordinating reduced energy requirements, strengthening cellular structure and muscle contraction [35].…”

Genomic basis of adaptation to climate and parasite prevalence and the importance of odorant perception in the ant Temnothorax longispinosus

“…This gene has previously been associated with cuticle-related functions in D. melanogaster and in the social bumblebee Bombus terrestris (Feng et al, 2022;Liu et al, 2022). While it remains speculative, it is plausible that this candidate gene could alter the cuticle of hosts, that is, lead to a harder cuticle with better defence abilities, favourable in highly parasitized areas.…”