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Changes in the Gene Expression Profiles of the Hypopharyngeal Gland of Worker Honeybees in Association with Worker Behavior and Hormonal Factors.

Ueno T, Takeuchi H, Kawasaki K, Kubo T - PLoS ONE (2015)

Bottom Line: In the present study, to clarify the molecular mechanisms that coordinate HPG physiology with worker behavior, we first analyzed whether Ambuffy, AmMMP1, mrjp2 (a gene encoding one of major royal jelly protein isoforms), and Hbg3 (a gene encoding α-glucosidase III) expression, is associated with worker behavior in 'single-cohort colonies' where workers of almost the same age perform different tasks.Expression of these genes correlated with the worker's role, while controlling for age, indicating their regulation associated with the worker's behavior.Our findings suggest that both ecdysone- and JH-signaling cooperatively regulate the physiological state of the HPGs in association with the worker's behavior.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Graduate School of Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, 113-0033, Japan; Faculty of Pharmaceutical Sciences, Doshisha Women's College, Kyotanabe, Kyoto, 610-0395, Japan.

ABSTRACT
The hypopharyngeal glands (HPGs) of worker honeybees undergo physiological changes along with the age-dependent role change from nursing to foraging: nurse bee HPGs secrete mainly major royal jelly proteins, whereas forager HPGs secrete mainly α-glucosidase III, which converts the sucrose in the nectar into glucose and fructose. We previously identified two other genes, Apis mellifera buffy (Ambuffy) and Apis mellifera matrix metalloproteinase 1 (AmMMP1), with enriched expression in nurse bee and forager HPGs, respectively. In the present study, to clarify the molecular mechanisms that coordinate HPG physiology with worker behavior, we first analyzed whether Ambuffy, AmMMP1, mrjp2 (a gene encoding one of major royal jelly protein isoforms), and Hbg3 (a gene encoding α-glucosidase III) expression, is associated with worker behavior in 'single-cohort colonies' where workers of almost the same age perform different tasks. Expression of these genes correlated with the worker's role, while controlling for age, indicating their regulation associated with the worker's behavior. Associated gene expression suggested the possible involvement of some hormonal factors in its regulation. We therefore examined the relationship between ecdysone- and juvenile hormone (JH)-signaling, and the expression profiles of these 'indicator' genes (nurse bee HPG-selective genes: mrjp2 and Ambuffy, and forager HPG-selective genes: Hbg3 and AmMMP1). Expression of both ecdysone-regulated genes (ecdysone receptor, mushroom body large type Kenyon cell specific protein-1, and E74) and JH-regulated genes (Methoprene tolerant and Krüppel homolog 1) was higher in the forager HPGs than in the nurse bee HPGs, suggesting the possible roles of ecdysone- and JH-regulated genes in worker HPGs. Furthermore, 20-hydroxyecdysone-treatment repressed both nurse bee- and forager-selective gene expression, whereas methoprene-treatment enhanced the expression of forager-selective genes and repressed nurse bee-selective genes in the HPGs. Our findings suggest that both ecdysone- and JH-signaling cooperatively regulate the physiological state of the HPGs in association with the worker's behavior.

No MeSH data available.


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Quantification of gene transcripts in the HPGs of workers derived from ‘single-cohort colonies’.Nurse bees (N) and precocious foragers (P) were collected from two single-cohort colonies. Relative mRNA levels of mrjp2 (A), Hbg3 (B), Ambuffy (C), and AmMMP1 (D) in the HPGs of workers derived from two single-cohort colonies are indicated with standard error. The amount of mRNA in the HPG of nurse bees is defined as 1. Transcript amounts were normalized with that of ribosomal protein 49 (rp49). Asterisks indicate significant differences between nurse bees and precocious foragers (*, p < 0.05; t-test). The expressions of mrjp2 and Ambuffy in some workers could not be quantified because signal intensities of these samples were lower than the detection threshold. Thus, number of samples are different from each gene.
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pone.0130206.g002: Quantification of gene transcripts in the HPGs of workers derived from ‘single-cohort colonies’.Nurse bees (N) and precocious foragers (P) were collected from two single-cohort colonies. Relative mRNA levels of mrjp2 (A), Hbg3 (B), Ambuffy (C), and AmMMP1 (D) in the HPGs of workers derived from two single-cohort colonies are indicated with standard error. The amount of mRNA in the HPG of nurse bees is defined as 1. Transcript amounts were normalized with that of ribosomal protein 49 (rp49). Asterisks indicate significant differences between nurse bees and precocious foragers (*, p < 0.05; t-test). The expressions of mrjp2 and Ambuffy in some workers could not be quantified because signal intensities of these samples were lower than the detection threshold. Thus, number of samples are different from each gene.

Mentions: First, we examined whether expression of mrjp2 and Hbg3 correlates with the worker’s role or age using a single-cohort colony. Comparison of the mean expression levels in pooled samples from two colonies revealed that mrjp2 expression was approximately 40-fold higher in nurse bees than in precocious foragers (Welch’s t-test, p<0.01), whereas Hbg3 expression was approximately 130-fold higher in precocious foragers than in nurse bees (Welch’s t-test, p<0.05) (Fig 2). These expression patterns of mrjp2 and Hbg3 were similar to those of nurse bees and foragers derived from normal colonies (Fig 2) [19].


Changes in the Gene Expression Profiles of the Hypopharyngeal Gland of Worker Honeybees in Association with Worker Behavior and Hormonal Factors.

Ueno T, Takeuchi H, Kawasaki K, Kubo T - PLoS ONE (2015)

Quantification of gene transcripts in the HPGs of workers derived from ‘single-cohort colonies’.Nurse bees (N) and precocious foragers (P) were collected from two single-cohort colonies. Relative mRNA levels of mrjp2 (A), Hbg3 (B), Ambuffy (C), and AmMMP1 (D) in the HPGs of workers derived from two single-cohort colonies are indicated with standard error. The amount of mRNA in the HPG of nurse bees is defined as 1. Transcript amounts were normalized with that of ribosomal protein 49 (rp49). Asterisks indicate significant differences between nurse bees and precocious foragers (*, p < 0.05; t-test). The expressions of mrjp2 and Ambuffy in some workers could not be quantified because signal intensities of these samples were lower than the detection threshold. Thus, number of samples are different from each gene.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4470657&req=5

pone.0130206.g002: Quantification of gene transcripts in the HPGs of workers derived from ‘single-cohort colonies’.Nurse bees (N) and precocious foragers (P) were collected from two single-cohort colonies. Relative mRNA levels of mrjp2 (A), Hbg3 (B), Ambuffy (C), and AmMMP1 (D) in the HPGs of workers derived from two single-cohort colonies are indicated with standard error. The amount of mRNA in the HPG of nurse bees is defined as 1. Transcript amounts were normalized with that of ribosomal protein 49 (rp49). Asterisks indicate significant differences between nurse bees and precocious foragers (*, p < 0.05; t-test). The expressions of mrjp2 and Ambuffy in some workers could not be quantified because signal intensities of these samples were lower than the detection threshold. Thus, number of samples are different from each gene.
Mentions: First, we examined whether expression of mrjp2 and Hbg3 correlates with the worker’s role or age using a single-cohort colony. Comparison of the mean expression levels in pooled samples from two colonies revealed that mrjp2 expression was approximately 40-fold higher in nurse bees than in precocious foragers (Welch’s t-test, p<0.01), whereas Hbg3 expression was approximately 130-fold higher in precocious foragers than in nurse bees (Welch’s t-test, p<0.05) (Fig 2). These expression patterns of mrjp2 and Hbg3 were similar to those of nurse bees and foragers derived from normal colonies (Fig 2) [19].

Bottom Line: In the present study, to clarify the molecular mechanisms that coordinate HPG physiology with worker behavior, we first analyzed whether Ambuffy, AmMMP1, mrjp2 (a gene encoding one of major royal jelly protein isoforms), and Hbg3 (a gene encoding α-glucosidase III) expression, is associated with worker behavior in 'single-cohort colonies' where workers of almost the same age perform different tasks.Expression of these genes correlated with the worker's role, while controlling for age, indicating their regulation associated with the worker's behavior.Our findings suggest that both ecdysone- and JH-signaling cooperatively regulate the physiological state of the HPGs in association with the worker's behavior.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Graduate School of Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, 113-0033, Japan; Faculty of Pharmaceutical Sciences, Doshisha Women's College, Kyotanabe, Kyoto, 610-0395, Japan.

ABSTRACT
The hypopharyngeal glands (HPGs) of worker honeybees undergo physiological changes along with the age-dependent role change from nursing to foraging: nurse bee HPGs secrete mainly major royal jelly proteins, whereas forager HPGs secrete mainly α-glucosidase III, which converts the sucrose in the nectar into glucose and fructose. We previously identified two other genes, Apis mellifera buffy (Ambuffy) and Apis mellifera matrix metalloproteinase 1 (AmMMP1), with enriched expression in nurse bee and forager HPGs, respectively. In the present study, to clarify the molecular mechanisms that coordinate HPG physiology with worker behavior, we first analyzed whether Ambuffy, AmMMP1, mrjp2 (a gene encoding one of major royal jelly protein isoforms), and Hbg3 (a gene encoding α-glucosidase III) expression, is associated with worker behavior in 'single-cohort colonies' where workers of almost the same age perform different tasks. Expression of these genes correlated with the worker's role, while controlling for age, indicating their regulation associated with the worker's behavior. Associated gene expression suggested the possible involvement of some hormonal factors in its regulation. We therefore examined the relationship between ecdysone- and juvenile hormone (JH)-signaling, and the expression profiles of these 'indicator' genes (nurse bee HPG-selective genes: mrjp2 and Ambuffy, and forager HPG-selective genes: Hbg3 and AmMMP1). Expression of both ecdysone-regulated genes (ecdysone receptor, mushroom body large type Kenyon cell specific protein-1, and E74) and JH-regulated genes (Methoprene tolerant and Krüppel homolog 1) was higher in the forager HPGs than in the nurse bee HPGs, suggesting the possible roles of ecdysone- and JH-regulated genes in worker HPGs. Furthermore, 20-hydroxyecdysone-treatment repressed both nurse bee- and forager-selective gene expression, whereas methoprene-treatment enhanced the expression of forager-selective genes and repressed nurse bee-selective genes in the HPGs. Our findings suggest that both ecdysone- and JH-signaling cooperatively regulate the physiological state of the HPGs in association with the worker's behavior.

No MeSH data available.


Related in: MedlinePlus