Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera

Author(s)

Barchuk, Angel R. ; Cristino, Alexandre S. ; Kucharski, Robert ; Costa, Luciano F. ; Simões, Zilá L. P. ^[5] ; Maleszka, Ryszard

• Document type: Journal article
• Source: BMC Developmental Biology; v. 7, n. 70 2007.
• Field of knowledge: Biological Sciences - Genetics

Abstract

In 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. By 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. We 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. (AU)

• FAPESP's process: 05/03926-5 - Functional genomics of Apis mellifera: search for new genes and functional networks in the context of development, different castes and reproduction
• Grantee: Zilá Luz Paulino Simões
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 99/00719-6 - Africanized honeybees: an integrated analysis of the africanization process of Apis mellifera, focusing on determinants in fertility of drones, queens and workers
• Grantee: Zilá Luz Paulino Simões
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 05/00587-5 - Mesh (graph) modeling and techniques of pattern recognition: structure, dynamics and applications
• Grantee: Roberto Marcondes Cesar Junior
• Support Opportunities: Research Projects - Thematic Grants