Dataset Information

Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera.

ABSTRACT: Protecting genome integrity against transposable elements is achieved by intricate molecular mechanisms involving PIWI proteins, their associated small RNAs (piRNAs), and epigenetic modifiers such as DNA methylation. Eusocial bees, in particular the Western honeybee, Apis mellifera, have one of the lowest contents of transposable elements in the animal kingdom, and, unlike other animals with a functional DNA methylation system, appear not to methylate their transposons. This raises the question of whether the PIWI machinery has been retained in this species. Using comparative genomics, mass spectrometry, and expressional profiling, we present seminal evidence that the piRNA system is conserved in honeybees. We show that honey bee piRNAs contain a 2'-O-methyl modification at the 3' end, and have a bias towards a 5' terminal U, which are signature features of their biogenesis. Both piRNA repertoire and expression levels are greater in reproductive individuals than in sterile workers. Haploid males, where the detrimental effects of transposons are dominant, have the greatest piRNA levels, but surprisingly, the highest expression of transposons. These results show that even in a transposon-depleted species, the piRNA system is required to guard the vulnerable haploid genome and reproductive castes against transposon-associated genomic instability. This also suggests that dosage plays an important role in the regulation of transposons and piRNAs expression in haplo-diploid systems.

SUBMITTER: Wang W

PROVIDER: S-EPMC5452642 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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Publications

Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera.

Wang Weiwen W Ashby Regan R Ying Hua H Maleszka Ryszard R Forêt Sylvain S

Genome biology and evolution 20170501 5

Protecting genome integrity against transposable elements is achieved by intricate molecular mechanisms involving PIWI proteins, their associated small RNAs (piRNAs), and epigenetic modifiers such as DNA methylation. Eusocial bees, in particular the Western honeybee, Apis mellifera, have one of the lowest contents of transposable elements in the animal kingdom, and, unlike other animals with a functional DNA methylation system, appear not to methylate their transposons. This raises the question ...[more]

PMID: 28472327

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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.

Dataset Information

Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera.

Publications

Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera.

Similar Datasets

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