In-depth Proteome of the Hypopharyngeal Glands of Honeybee Workers Reveals Highly Activated Protein and Energy Metabolism in Priming the Secretion of Royal Jelly

Hu, Han; Bezabih, Gebreamlak; Mao, Feng; Wei, Qiaohong; Zhang, Xufeng; Wu, Fan; Meng, Lifeng; Yu, Fang; Han, Bin; Ma, Chuan; Li, Jianke

doi:10.1074/mcp.ra118.001257

Cited by 47 publications

(54 citation statements)

References 75 publications

(139 reference statements)

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“…Indeed, for MRJP5 all scenarios were described: significantly higher in foragers than nurses (Hernández et al, (brain)), no difference between nurses and foragers (Buttstedt et al, (heads); Ji et al, (HGs)), or being higher in nurses than in foragers (Drapeau et al, (heads)). MRJP1 ‐ 4 and MRJP7 are in the majority of studies described as being higher in nurse bees than in foragers with some studies detecting the proteins exclusively in nurses (Feng, Fang, & Li, (HG); Garcia et al, (brain); Hernández et al, (brain); Hu et al, (HG); Ji et al, (HG) Klaudiny et al, (head); Kubo et al, (HG); Liu et al, (HG); Ohashi et al, (HG); Peixoto et al, (brain)).…”

Section: Discussionmentioning

confidence: 99%

The rise and fall of major royal jelly proteins during a honeybee (Apis mellifera) workers' life

Dobritzsch

Aumer

Fuszard

et al. 2019

Ecology and Evolution

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The genome of the western honeybee ( Apis mellifera ) harbors nine transcribed major royal jelly protein genes ( mrjp1‐9 ) which originate from a single‐copy precursor via gene duplication. The first MRJP was identified in royal jelly, a secretion of the bees' hypopharyngeal glands that is used by young worker bees, called nurses, to feed developing larvae. Thus, MRJPs are frequently assumed to mainly have functions for developing bee larvae and to be expressed in the food glands of nurse bees. In‐depth knowledge on caste‐ and age‐specific role and abundance of MRJPs is missing. We here show, using combined quantitative real‐time PCR with quantitative mass spectrometry, that expression and protein amount of mrjp1‐5 and mrjp7 show an age‐dependent pattern in worker's hypopharyngeal glands as well as in brains, albeit lower relative abundance in brains than in glands. Expression increases after hatching until the nurse bee period and is followed by a decrease in older workers that forage for plant products. Mrjp6 expression deviates considerably from the expression profiles of the other mrjps , does not significantly vary in the brain, and shows its highest expression in the hypopharyngeal glands during the forager period. Furthermore, it is the only mrjp of which transcript abundance does not correlate with protein amount. Mrjp8 and mrjp9 show, compared to the other mrjps, a very low expression in both tissues. Albeit mrjp8 mRNA was detected via qPCR, the protein was not quantified in any of the tissues. Due to the occurrence of MRJP8 and MRJP9 in other body parts of the bees, for example, the venom gland, they might not have a hypopharyngeal gland‐ or brain‐specific function but rather functions in other tissues. Thus, mrjp1‐7 but not mrjp8 and mrjp9 might be involved in the regulation of phenotypic plasticity and age polyethism in worker honeybees.

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Section: Discussionmentioning

confidence: 99%

The rise and fall of major royal jelly proteins during a honeybee (Apis mellifera) workers' life

Dobritzsch

Aumer

Fuszard

et al. 2019

Ecology and Evolution

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“…In addition, phosphorylation has been shown to regulate the protein activity of HG at all ages of worker bees, suggesting that phosphorylation optimizes the biochemical activity of worker bees HG (Qi et al 2015). In RJB NB, the pathways of protein synthesis and energy metabolism are functionally induced to consolidate enhanced RJ secretion compared to ITB (Hu et al 2019). Also, in RJBs enhanced levels of neuropeptides are involved in regulating water homeostasis, brooder pheromone recognition, foraging ability, and pollen collection to regulate RJ secretion behavior (Han et al 2015).…”

Section: Molecular Insights Into the R J B S A C H I E V I N G H I Gmentioning

confidence: 99%

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

Altaye

Meng

2019

Apidologie

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The genetic selection of a high royal jelly (RJ)-producing strain of bees (RJBs) from Italian bees (ITBs) has been conducted for nearly four decades in China since the 1980s. RJBs are the most important producers of RJ in the world and produce > 90% of the total output with an annual market value of > $40 million. With technological advancements in proteomics, the mechanism underpinning the high RJ production by RJBs has been explored to new depths in the last decades. Here, we give an overview that the mechanism driving the enhanced performance of RJ secretion by RJBs. First, the selection of RJBs, high-efficiency technology for RJ production, and advances in genetic characterization of RJBs are reviewed. Then, proteome and phosphoproteome characterization that decipher the augmented RJ production using honeybee organs and tissues are summarized. This may be potentially useful in gaining a complete mechanistic insight into the high performance of RJ yields in honeybees, and expands understanding of the honeybee biology. Italian bees / royal jelly bees / royal jelly production / molecular basis-proteome

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“…Hypopharyngeal gland size, morphology, and activity are known to be affected by a variety of pesticides, including herbicides, fungicides, and insecticides (Table 1). Reductions in gland size and function can lead to decreased royal jelly secretion 43 and consequent colony failure through diminished brood production, premature transition from nursing to foraging behaviors, shortened worker life span, and reduced colony size. 38 Moreover, pesticides, including fungicides, herbicides, 6 and insecticides, 44 can alter nurse food consumption patterns and increase the risk of transmission of unmetabolized pesticides to larvae via royal or worker jelly.…”

Section: Implications Of Honeybee Eusociality On Toxicologic Pathologymentioning

confidence: 99%

Honey Bees and Environmental Stress: Toxicologic Pathology of a Superorganism

Berenbaum

Liao

2019

Toxicol Pathol

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As a eusocial species, Apis mellifera, the European honey bee, is effectively a superorganism—a group of genetically related individuals functioning as a collective unit. Because the unit of selection is the colony and not the individual, standard methods for assessing toxicologic pathology can miss colony-level responses to stress. For over a decade, US populations of honeybees have experienced severe annual losses attributed to a variety of environmental stressors varying temporally and geographically; differentiating among those stressors is accordingly a high priority. Social interactions among individuals in this social species, however, mean that the “footprint” of stressors such as pesticides, phytochemicals, pathogens, and parasites may be most discernible in individuals that did not themselves directly encounter the stressor. For example, neurotoxic effects of pesticides on nurse bees may impair their behavioral responses to queen-destined larvae, which may then emerge as adults with altered anatomy or physiology. Similarly, pesticide-induced size alterations in nurse hypopharyngeal glands, which produce royal jelly, the exclusive food of larval and adult queens, may disproportionately affect the queen’s (and thus colony) health. Thus, evaluating toxicologic pathology in the honeybee requires a new perspective and development of assays that preserve the social context that ultimately determines colony health.

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In-depth Proteome of the Hypopharyngeal Glands of Honeybee Workers Reveals Highly Activated Protein and Energy Metabolism in Priming the Secretion of Royal Jelly

Cited by 47 publications

References 75 publications

The rise and fall of major royal jelly proteins during a honeybee (Apis mellifera) workers' life

The rise and fall of major royal jelly proteins during a honeybee (Apis mellifera) workers' life

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

Honey Bees and Environmental Stress: Toxicologic Pathology of a Superorganism

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