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Dimorphic ovary differentiation in honeybee (Apis mellifera) larvae involves caste-specific expression of homologs of ark and buffy cell death genes.

ABSTRACT: The establishment of the number of repeated structural units, the ovarioles, in the ovaries is one of the critical events that shape caste polyphenism in social insects. In early postembryonic development, honeybee (Apis mellifera) larvae have a pair of ovaries, each one consisting of almost two hundred ovariole primordia. While practically all these ovarioles continue developing in queen-destined larvae, they undergo massive programmed cell death (PCD) in worker-destined larvae. So as to gain insight into the molecular basis of this fundamental process in caste differentiation we used quantitative PCR (qPCR) and fluorescent in situ hybridization (FISH) to investigate the expression of the Amark and Ambuffy genes in the ovaries of the two honeybee castes throughout the fifth larval instar. These are the homologs of ark and buffy Drosophila melanogaster genes, respectively, involved in activating and inhibiting PCD. Caste-specific expression patterns were found during this time-window defining ovariole number. Amark transcript levels were increased when ovariole resorption was intensified in workers, but remained at low levels in queen ovaries. The transcripts were mainly localized at the apical end of all the worker ovarioles, but appeared in only a few queen ovarioles, thus strongly suggesting a function in mediating massive ovariolar cell death in worker larvae. Ambuffy was mainly expressed in the peritoneal sheath cells covering each ovariole. The levels of Ambuffy transcripts increased earlier in the developing ovaries of queens than in workers. Consistent with a protective role against cell death, Ambuffy transcripts were localized in practically all queen ovarioles, but only in few worker ovarioles. The results are indicative of a functional relationship between the expression of evolutionary conserved cell death genes and the morphological events leading to caste-specific ovary differentiation in a social insect.

SUBMITTER: Dallacqua RP

PROVIDER: S-EPMC4028266 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Dimorphic ovary differentiation in honeybee (Apis mellifera) larvae involves caste-specific expression of homologs of ark and buffy cell death genes.

Dallacqua Rodrigo Pires RP Bitondi Márcia Maria Gentile MM

PloS one 20140520 5

The establishment of the number of repeated structural units, the ovarioles, in the ovaries is one of the critical events that shape caste polyphenism in social insects. In early postembryonic development, honeybee (Apis mellifera) larvae have a pair of ovaries, each one consisting of almost two hundred ovariole primordia. While practically all these ovarioles continue developing in queen-destined larvae, they undergo massive programmed cell death (PCD) in worker-destined larvae. So as to gain i ...[more]

PMID: 24844304

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Project description:Honeybee (Apis mellifera) exhibits divisions in both morphology and reproduction. The queen is larger in size and fully developed sexually, while the worker bees are smaller in size and nearly infertile. To better understand the specific time and underlying molecular mechanisms of caste differentiation, the proteomic profiles of larvae intended to grow into queen and worker castes were compared at 72 and 120 hours using two dimensional electrophoresis (2-DE), network, enrichment and quantitative PCR analysis. There were significant differences in protein expression between the two larvae castes at 72 and 120 hours, suggesting the queen and the worker larvae have already decided their fate before 72 hours. Specifically, at 72 hours, queen intended larvae over-expressed transketolase, aldehyde reductase, and enolase proteins which are involved in carbohydrate metabolism and energy production, imaginal disc growth factor 4 which is a developmental related protein, long-chain-fatty-acid CoA ligase and proteasome subunit alpha type 5 which metabolize fatty and amino acids, while worker intended larvae over-expressed ATP synthase beta subunit, aldehyde dehydrogenase, thioredoxin peroxidase 1 and peroxiredoxin 2540, lethal (2) 37 and 14-3-3 protein epsilon, fatty acid binding protein, and translational controlled tumor protein. This differential protein expression between the two caste intended larvae was more pronounced at 120 hours, with particular significant differences in proteins associated with carbohydrate metabolism and energy production. Functional enrichment analysis suggests that carbohydrate metabolism and energy production and anti-oxidation proteins play major roles in the formation of caste divergence. The constructed network and validated gene expression identified target proteins for further functional study. This new finding is in contrast to the existing notion that 72 hour old larvae has bipotential and can develop into either queen or worker based on epigenetics and can help us to gain new insight into the time of departure as well as caste trajectory influencing elements at the molecular level.

Project description:BackgroundIn honeybees, differential feeding of female larvae promotes the occurrence of two different phenotypes, a queen and a worker, from identical genotypes, through incremental alterations, which affect general growth, and character state alterations that result in the presence or absence of specific structures. Although previous studies revealed a link between incremental alterations and differential expression of physiometabolic genes, the molecular changes accompanying character state alterations remain unknown.ResultsBy using cDNA microarray analyses of >6,000 Apis mellifera ESTs, we found 240 differentially expressed genes (DEGs) between developing queens and workers. Many genes recorded as up-regulated in prospective workers appear to be unique to A. mellifera, suggesting that the workers' developmental pathway involves the participation of novel genes. Workers up-regulate more developmental genes than queens, whereas queens up-regulate a greater proportion of physiometabolic genes, including genes coding for metabolic enzymes and genes whose products are known to regulate the rate of mass-transforming processes and the general growth of the organism (e.g., tor). Many DEGs are likely to be involved in processes favoring the development of caste-biased structures, like brain, legs and ovaries, as well as genes that code for cytoskeleton constituents. Treatment of developing worker larvae with juvenile hormone (JH) revealed 52 JH responsive genes, specifically during the critical period of caste development. Using Gibbs sampling and Expectation Maximization algorithms, we discovered eight overrepresented cis-elements from four gene groups. Graph theory and complex networks concepts were adopted to attain powerful graphical representations of the interrelation between cis-elements and genes and objectively quantify the degree of relationship between these entities.ConclusionWe suggest that clusters of functionally related DEGs are co-regulated during caste development in honeybees. This network of interactions is activated by nutrition-driven stimuli in early larval stages. Our data are consistent with the hypothesis that JH is a key component of the developmental determination of queen-like characters. Finally, we propose a conceptual model of caste differentiation in A. mellifera based on gene-regulatory networks.

Project description:The reproductive division of labor, based on caste differentiation in social insects, is of great significance in evolution. Generally, a healthy bee colony consists of a queen and numerous workers and drones. Despite being genetically identical, the queen and workers exhibit striking differences in morphology, behavior, and lifespan. The fertilized eggs and larvae selectively develop into queen and worker bees depending on the local nutrition and environment. Bee worker larvae that are transplanted within 3 days of age to queen cells of a bee colony can develop into queens with mature ovaries. This phenomenon is important to understand the regulatory mechanisms of caste differentiation. In this study, we transplanted worker larvae (Apis mellifera) at the age of 1 (L1), 2 (L2), and 3 days (L3) into queen cells until the age of 4 days. Subsequently, genetic changes in these larvae were evaluated. The results revealed that the number of differentially expressed genes (DEGs) in L1 vs. L3 was more than that in L1 vs. L2. Furthermore, many of the genes that were downregulated are mostly involved in metabolism, body development, reproductive ability, and longevity, indicating that these functions decreased with the age of transplantation of the larvae. Moreover, these functions may be critical for worker larvae to undergo the developmental path to become queens. We also found that the DEGs of L1 vs. L2 and L1 vs. L3 were enriched in the MAPK, FoxO, mTOR, Wnt, TGF-beta Hedgehog Toll and Imd, and Hippo signaling pathways. Gene ontology analysis indicated that some genes are simultaneously involved in different biological pathways; through these genes, the pathways formed a mutual regulatory network. Casein kinase 1 (CK 1) was predicted to participate in the FoxO, Wnt, Hedgehog, and Hippo signaling pathways. The results suggest that these pathways cross talked through the network to modify the development of larvae and that CK 1 is an important liaison. The results provide valuable information regarding the regulatory mechanism of environmental factors affecting queen development, thus, amplifying the understanding of caste differentiation in bees.

Dataset Information

Dimorphic ovary differentiation in honeybee (Apis mellifera) larvae involves caste-specific expression of homologs of ark and buffy cell death genes.

Publications

Dimorphic ovary differentiation in honeybee (Apis mellifera) larvae involves caste-specific expression of homologs of ark and buffy cell death genes.

Similar Datasets

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