Transcriptomic analysis of the honey bee (Apis mellifera) queen spermathecae reveals genes that may be involved in sperm storage after mating

Rangel, Juliana; Shepherd, Tonya F.; González, Alejandra; Hillhouse, Andrew; Konganti, Kranti; Ing, Nancy H.

doi:10.1371/journal.pone.0244648

Cited by 17 publications

(23 citation statements)

References 69 publications

(106 reference statements)

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“…While the relationship among the other proteins and sperm viability is unclear (restin homolog, for example, is associated with the cytoskeleton filaments and Hodgkin’s disease in mammals, but the most similar Drosophila sequence is the uncharacterized protein Dmel_CG14354), melittin is the main protein component of honey bee venom and is negatively correlated with sperm viability, which would be consistent with contamination causing sperm death. However, melittin transcripts have been previously identified in the spermathecae of mated queens by an independent research group [ 23 ] and another group found melittin proteins in both virgin and mated queen spermathecal fluid [ 24 ]. We searched for melittin in our own previously published proteomics data (three independent datasets) and found that it was consistently present [ 8 , 20 , 25 ].…”

Section: Resultsmentioning

confidence: 99%

Queen honey bees exhibit variable resilience to temperature stress

McAfee

Foster

2021

PLoS ONE

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Extreme temperature exposure can reduce stored sperm viability within queen honey bees; however, little is known about how thermal stress may directly impact queen performance or other maternal quality metrics. Here, in a blind field trial, we recorded laying pattern, queen mass, and average callow worker mass before and after exposing queens to a cold temperature (4°C, 2 h), hot temperature (42°C, 2 h), and hive temperature (33°C, control). We measured sperm viability at experiment termination, and investigated potential vertical effects of maternal temperature stress on embryos using proteomics. We found that cold stress, but not heat stress, reduced stored sperm viability; however, we found no significant effect of temperature stress on any other recorded metrics (queen mass, average callow worker mass, laying patterns, the egg proteome, and queen spermathecal fluid proteome). Previously determined candidate heat and cold stress biomarkers were not differentially expressed in stressed queens, indicating that these markers only have short-term post-stress diagnostic utility. Combined with variable sperm viability responses to temperature stress reported in different studies, these data also suggest that there is substantial variation in temperature tolerance, with respect to impacts on fertility, amongst queens. Future research should aim to quantify the variation and heritability of temperature tolerance, particularly heat, in different populations of queens in an effort to promote queen resilience.

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Section: Resultsmentioning

confidence: 99%

Queen honey bees exhibit variable resilience to temperature stress

McAfee

Foster

2021

PLoS ONE

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“…Therefore, they also produce antioxidants to improve storage. Mated compared to unmated queens had higher upregulation of cytochrome p450 and the antioxidant proteins catalase, TXN2 (Thioredoxin, mitochondrial precursor), TXNRD1 (Thioredoxin reductase 1), GSTD1 (Glutathione S-transferase), and SOD1 (Superoxide dismutase 1) [95][96][97][98][99]. Thioredoxin has been confirmed multiple times and it plays an important role in the protection of sperm during storage.…”

Section: Sperm Storage By the Queenmentioning

confidence: 99%

Prospects in Connecting Genetic Variation to Variation in Fertility in Male Bees

Slater

Smith

Harpur

2021

Genes

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Bees are economically and ecologically important pollinating species. Managed and native bee species face increasing pressures from human-created stressors such as habitat loss, pesticide use, and introduced pathogens. There has been increasing attention towards how each of these factors impacts fertility, especially sperm production and maintenance in males. Here, we turn our attention towards another important factor impacting phenotypic variation: genetics. Using honey bees as a model, we explore the current understanding of how genetic variation within and between populations contributes to variation in sperm production, sperm maintenance, and insemination success among males. We conclude with perspectives and future directions in the study of male fertility in honey bees and non-Apis pollinators more broadly, which still remain largely understudied.

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“…Extensive studies, including proteomic, metabolomic, and transcriptomic analyses, have been conducted on the storage and survival of sperm in A. mellifera [1,2,4,5,[10][11][12][13][14]. A previous study identified >100 proteins as major spermathecal fluid constituents in A. mellifera queens and analyzed the association of spermathecal fluid proteins with energy metabolism and antioxidant defense [2].…”

Section: Introductionmentioning

confidence: 99%

“…A previous study identified >100 proteins as major spermathecal fluid constituents in A. mellifera queens and analyzed the association of spermathecal fluid proteins with energy metabolism and antioxidant defense [2]. Recent studies have identified >10,000 transcripts and 2778 proteins in the mated or virgin A. mellifera queen's spermathecae via transcriptomic and proteomic analyses, respectively [13,14]. The results from the transcriptomic analyses revealed the gene expression patterns during sperm storage after mating and showed that Kielin/chordin-like and trehalase transcripts are highly expressed in the spermathecae of the mated queens, in comparison with their levels in virgin queens [14].…”

Section: Introductionmentioning

confidence: 99%

“…Recent studies have identified >10,000 transcripts and 2778 proteins in the mated or virgin A. mellifera queen's spermathecae via transcriptomic and proteomic analyses, respectively [13,14]. The results from the transcriptomic analyses revealed the gene expression patterns during sperm storage after mating and showed that Kielin/chordin-like and trehalase transcripts are highly expressed in the spermathecae of the mated queens, in comparison with their levels in virgin queens [14]. The glycolytic metabolite glyceraldehyde-3-phosphate reportedly facilitates the long-term survival and energy (ATP) production of honeybee sperm during their storage in the spermathecae, because this metabolite functions independently of oxygen and prevents sperm damage caused by reactive oxygen species (ROS) [4].…”

Section: Introductionmentioning

confidence: 99%

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Upregulation of Transferrin and Major Royal Jelly Proteins in the Spermathecal Fluid of Mated Honeybee (Apis mellifera) Queens

Park

Kim

et al. 2021

Insects

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Sperm storage in the spermathecae of honeybee (Apis mellifera) queens is vital for reproduction of honeybees. However, the molecular mechanisms whereby queens store sperm in a viable state over prolonged periods in the spermatheca are not fully understood. Here, we conducted RNA sequencing analysis of the spermathecae in both virgin and mated A. mellifera queens 24 h after mating and observed that the genes encoding transferrin (Tf) and major royal jelly proteins (MRJPs) were differentially expressed in the spermathecae of mated queens. The concentrations of Tf and antioxidant proteins such as superoxide dismutase 1, catalase, and glutathione peroxidase as well as the levels of reactive oxygen species, H2O2, and iron were higher in the spermathecal fluid of the mated queens than in virgin queens. Tf upregulation is likely to perform a protective role against the Fenton reaction occurring between iron and H2O2 in the antioxidant pathway in the mated queen’s spermathecal fluid. Furthermore, MRJPs—especially MRJP1, MRJP4, and MRJP6—were upregulated in the mated queen’s spermathecal fluid, indicating that they may serve as antimicrobial and antioxidant agents as well as an energy source for stored sperm in the spermathecal fluid of honeybee queens. Together, our findings show that Tf and MRJPs are upregulated in the spermatheca and spermathecal fluid of mated honeybee queens.

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Transcriptomic analysis of the honey bee (Apis mellifera) queen spermathecae reveals genes that may be involved in sperm storage after mating

Cited by 17 publications

References 69 publications

Queen honey bees exhibit variable resilience to temperature stress

Queen honey bees exhibit variable resilience to temperature stress

Prospects in Connecting Genetic Variation to Variation in Fertility in Male Bees

Upregulation of Transferrin and Major Royal Jelly Proteins in the Spermathecal Fluid of Mated Honeybee (Apis mellifera) Queens

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