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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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Related in: MedlinePlus

Schematic representation of the lncov1 and lncov2 gene positions in the chromosome 11 region containing a QTL for transgressive ovary size in workers.The dotted and dashed LOD score lines represent the 95% and 99% QTL thresholds, respectively, above which ovariole number is significantly influenced [4], [6]. The orange bar indicates the location of Group 11.31 scaffold and the green one the Group 11.35 scaffold (genome version 4.0). Black vertical lines indicate the respective positions of lncov1 and lncov2 within these scaffolds.
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pone-0078915-g003: Schematic representation of the lncov1 and lncov2 gene positions in the chromosome 11 region containing a QTL for transgressive ovary size in workers.The dotted and dashed LOD score lines represent the 95% and 99% QTL thresholds, respectively, above which ovariole number is significantly influenced [4], [6]. The orange bar indicates the location of Group 11.31 scaffold and the green one the Group 11.35 scaffold (genome version 4.0). Black vertical lines indicate the respective positions of lncov1 and lncov2 within these scaffolds.

Mentions: The fact that lncov1 and lncov2 both map to a relatively narrow genomic region on chromosome 11 made us take a closer look at this region, and a fortuitous finding was the report of a Quantitative Trait Locus (QTL) for variation in ovariole number of honey bee workers [6], [35]. This QTL on chromosome 11 was identified in backcrosses of Africanized with European honey bees, which exhibit different worker ovariole phenotypes. The QTL is above the 99% genome-wide threshold, with a 95% confidence interval covering the map interval between positions 8.9 and 12.2 Mb on chromosome 11. Strikingly, a genome browser analysis in BeeBase revealed that lncov1 maps right in the center of this interval, while lncov2 is located close to the 12.2 Mb border of the QTL (Figure 3).


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)

Schematic representation of the lncov1 and lncov2 gene positions in the chromosome 11 region containing a QTL for transgressive ovary size in workers.The dotted and dashed LOD score lines represent the 95% and 99% QTL thresholds, respectively, above which ovariole number is significantly influenced [4], [6]. The orange bar indicates the location of Group 11.31 scaffold and the green one the Group 11.35 scaffold (genome version 4.0). Black vertical lines indicate the respective positions of lncov1 and lncov2 within these scaffolds.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0078915-g003: Schematic representation of the lncov1 and lncov2 gene positions in the chromosome 11 region containing a QTL for transgressive ovary size in workers.The dotted and dashed LOD score lines represent the 95% and 99% QTL thresholds, respectively, above which ovariole number is significantly influenced [4], [6]. The orange bar indicates the location of Group 11.31 scaffold and the green one the Group 11.35 scaffold (genome version 4.0). Black vertical lines indicate the respective positions of lncov1 and lncov2 within these scaffolds.
Mentions: The fact that lncov1 and lncov2 both map to a relatively narrow genomic region on chromosome 11 made us take a closer look at this region, and a fortuitous finding was the report of a Quantitative Trait Locus (QTL) for variation in ovariole number of honey bee workers [6], [35]. This QTL on chromosome 11 was identified in backcrosses of Africanized with European honey bees, which exhibit different worker ovariole phenotypes. The QTL is above the 99% genome-wide threshold, with a 95% confidence interval covering the map interval between positions 8.9 and 12.2 Mb on chromosome 11. Strikingly, a genome browser analysis in BeeBase revealed that lncov1 maps right in the center of this interval, while lncov2 is located close to the 12.2 Mb border of the QTL (Figure 3).

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