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Sequence and expression characteristics of long noncoding RNAs in honey bee caste development--potential novel regulators for transgressive ovary size.

Humann FC, Tiberio GJ, Hartfelder K - PLoS ONE (2013)

Bottom Line: Recent genomics approaches on honey bee developmental biology revealed a set of genes that are differentially expressed genes in larval ovaries and associated with transgressive ovary size in queens and massive cell death in workers.Genomically, both map within a previously identified QTL on chromosome 11, associated with transgressive ovary size in honey bee workers.With only four lncRNAs known so far in honey bees, two expressed in the ovaries, these findings open a novel perspective on regulatory factors acting in the fine tuning of developmental processes underlying phenotypic plasticity related to social life histories.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil.

ABSTRACT
Division of labor in social insect colonies relies on a strong reproductive bias that favors queens. Although the ecological and evolutionary success attained through caste systems is well sketched out in terms of ultimate causes, the molecular and cellular underpinnings driving the development of caste phenotypes are still far from understood. Recent genomics approaches on honey bee developmental biology revealed a set of genes that are differentially expressed genes in larval ovaries and associated with transgressive ovary size in queens and massive cell death in workers. Amongst these, two contigs called special attention, both being over 200 bp in size and lacking apparent coding potential. Herein, we obtained their full cDNA sequences. These and their secondary structure characteristics placed in evidence that they are bona fide long noncoding RNAs (lncRNA) differentially expressed in larval ovaries, thus named lncov1 and lncov2. Genomically, both map within a previously identified QTL on chromosome 11, associated with transgressive ovary size in honey bee workers. As lncov1 was over-expressed in worker ovaries we focused on this gene. Real-time qPCR analysis on larval worker ovaries evidenced an expression peak coinciding with the onset of autophagic cell death. Cellular localization analysis through fluorescence in situ hybridization revealed perinuclear spots resembling omega speckles known to regulate trafficking of RNA-binding proteins. With only four lncRNAs known so far in honey bees, two expressed in the ovaries, these findings open a novel perspective on regulatory factors acting in the fine tuning of developmental processes underlying phenotypic plasticity related to social life histories.

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Fluorescence in situ hybridization (FISH) revealing the localization of lncov1 transcripts in ovaries of fifth instar worker larvae.(A) Detection of an Alexa 594-labeled lncov1 probe (red) in ovary whole mounts; nuclei are counterstained with DAPI (blue). White arrows indicate some of the lncov1 agglomerates, showing their distribution throughout the developing ovarioles. (B) High resolution image of (A) evidencing lncov1 RNA agglomerates in perinuclear positions. The images were captured by confocal microscopy. Scale bars represent 20 and 5 µm, respectively.
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pone-0078915-g005: Fluorescence in situ hybridization (FISH) revealing the localization of lncov1 transcripts in ovaries of fifth instar worker larvae.(A) Detection of an Alexa 594-labeled lncov1 probe (red) in ovary whole mounts; nuclei are counterstained with DAPI (blue). White arrows indicate some of the lncov1 agglomerates, showing their distribution throughout the developing ovarioles. (B) High resolution image of (A) evidencing lncov1 RNA agglomerates in perinuclear positions. The images were captured by confocal microscopy. Scale bars represent 20 and 5 µm, respectively.

Mentions: The FISH assays revealed distinct focal spots of lncov1 RNA (Figure 5). Through comparison with DAPI stained nuclei in the single image series of optical 0.5 µm sections, these lncov1 spots turned out to be of primarily cytoplasmic localization. Their perinuclear localization is indicative of an omega speckle-like structure.


Sequence and expression characteristics of long noncoding RNAs in honey bee caste development--potential novel regulators for transgressive ovary size.

Humann FC, Tiberio GJ, Hartfelder K - PLoS ONE (2013)

Fluorescence in situ hybridization (FISH) revealing the localization of lncov1 transcripts in ovaries of fifth instar worker larvae.(A) Detection of an Alexa 594-labeled lncov1 probe (red) in ovary whole mounts; nuclei are counterstained with DAPI (blue). White arrows indicate some of the lncov1 agglomerates, showing their distribution throughout the developing ovarioles. (B) High resolution image of (A) evidencing lncov1 RNA agglomerates in perinuclear positions. The images were captured by confocal microscopy. Scale bars represent 20 and 5 µm, respectively.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3814967&req=5

pone-0078915-g005: Fluorescence in situ hybridization (FISH) revealing the localization of lncov1 transcripts in ovaries of fifth instar worker larvae.(A) Detection of an Alexa 594-labeled lncov1 probe (red) in ovary whole mounts; nuclei are counterstained with DAPI (blue). White arrows indicate some of the lncov1 agglomerates, showing their distribution throughout the developing ovarioles. (B) High resolution image of (A) evidencing lncov1 RNA agglomerates in perinuclear positions. The images were captured by confocal microscopy. Scale bars represent 20 and 5 µm, respectively.
Mentions: The FISH assays revealed distinct focal spots of lncov1 RNA (Figure 5). Through comparison with DAPI stained nuclei in the single image series of optical 0.5 µm sections, these lncov1 spots turned out to be of primarily cytoplasmic localization. Their perinuclear localization is indicative of an omega speckle-like structure.

Bottom Line: Recent genomics approaches on honey bee developmental biology revealed a set of genes that are differentially expressed genes in larval ovaries and associated with transgressive ovary size in queens and massive cell death in workers.Genomically, both map within a previously identified QTL on chromosome 11, associated with transgressive ovary size in honey bee workers.With only four lncRNAs known so far in honey bees, two expressed in the ovaries, these findings open a novel perspective on regulatory factors acting in the fine tuning of developmental processes underlying phenotypic plasticity related to social life histories.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil.

ABSTRACT
Division of labor in social insect colonies relies on a strong reproductive bias that favors queens. Although the ecological and evolutionary success attained through caste systems is well sketched out in terms of ultimate causes, the molecular and cellular underpinnings driving the development of caste phenotypes are still far from understood. Recent genomics approaches on honey bee developmental biology revealed a set of genes that are differentially expressed genes in larval ovaries and associated with transgressive ovary size in queens and massive cell death in workers. Amongst these, two contigs called special attention, both being over 200 bp in size and lacking apparent coding potential. Herein, we obtained their full cDNA sequences. These and their secondary structure characteristics placed in evidence that they are bona fide long noncoding RNAs (lncRNA) differentially expressed in larval ovaries, thus named lncov1 and lncov2. Genomically, both map within a previously identified QTL on chromosome 11, associated with transgressive ovary size in honey bee workers. As lncov1 was over-expressed in worker ovaries we focused on this gene. Real-time qPCR analysis on larval worker ovaries evidenced an expression peak coinciding with the onset of autophagic cell death. Cellular localization analysis through fluorescence in situ hybridization revealed perinuclear spots resembling omega speckles known to regulate trafficking of RNA-binding proteins. With only four lncRNAs known so far in honey bees, two expressed in the ovaries, these findings open a novel perspective on regulatory factors acting in the fine tuning of developmental processes underlying phenotypic plasticity related to social life histories.

Show MeSH
Related in: MedlinePlus