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Proteome of the Head and Thorax Salivary Glands in the Stingless Bee Proteome of the head and thorax salivary glands in the stingless bee Melipona quadrifasciata anthidioides Douglas Elias-Santos, Maria Fialho, Rui Vitorino, Leandro Oliveira, José Zanuncio, José Serrão To cite this version: Douglas Elias-Santos, Maria Fialho, Rui Vitorino, Leandro Oliveira, José Zanuncio, et al.. Proteome of the head and thorax salivary glands in the stingless bee Melipona quadrifasciata anthidioides . Apidologie, Springer Verlag, 2013, 44 (6), pp.684-698. 10.1007/s13592-013-0217-6. hal-01201338 HAL Id: hal-01201338 https://hal.archives-ouvertes.fr/hal-01201338 Submitted on 17 Sep 2015 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2013) 44:684–698 Original article * INRA, DIB and Springer-Verlag France, 2013 DOI: 10.1007/s13592-013-0217-6 Proteome of the head and thorax salivary glands in the stingless bee Melipona quadrifasciata anthidioides 1 1 2 Douglas ELIAS-SANTOS , Maria do Carmo Q. FIALHO , Rui VITORINO , 1 3 1 Leandro L. OLIVEIRA , José C. ZANUNCIO , José Eduardo SERRÃO 1Departamento de Biologia Geral, Universidade Federal de Viçosa, 36570-000 Viçosa, Minas Gerais, Brazil 2Department of Chemistry, University of Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal 3Departamento de Biologia Animal, Universidade Federal de Viçosa, 36570-000 Viçosa, Minas Gerais, Brazil Received 1 March 2013 – Revised 7 May 2013 – Accepted 23 May 2013 Abstract – The exocrine glands of social insects are related to the social communication, reproduction, and development of individuals. Eusocial bees have two types of salivary glands: the head salivary gland, which possibly functions in marking food sources, and the thorax salivary gland, which produces saliva. This study evaluated the major protein content of the head and thorax salivary glands of the stingless bee Melipona quadrifasciata anthidioides forager workers. The head salivary gland expresses 27 proteins in high quantity, including heat shock proteins, enzymes of the glycolysis pathway, gene regulation proteins, and an odorant- binding protein. The thorax salivary gland expresses 12 proteins, including heat shock proteins, cellular detoxification proteins, energy metabolism proteins, and proteins linked to environmental stress. The proteins identified in both the head and thorax salivary glands contribute to our understanding of their possible functions in stingless bees. behavior / odorant-binding protein / heat shock protein / Hymenoptera / stress 1. INTRODUCTION and diversity in the insect body. The best- known functions of the exocrine glands are Social Hymenoptera are intriguing insects related to the communication, reproduction, and because of the complexity and organization of development of individuals (Cruz-Landim and their social lives. In bees, queens and workers Abdalla 2002). For communication, exocrine form distinct castes, each playing important glands release chemicals termed pheromones, roles within the colony (Michener 1974). More- which are a mix of compounds causing physi- over, in highly eusocial bees, there is a division of ological and/or behavioral responses in other labor between workers, which favors protection individuals of the same species (Free 1987). against natural enemies, increases resistance to The salivary glands of eusocial bees are environmental stress, and in resource storage classified into two types: head salivary glands (Roubik 1989). (labial glands) and thorax salivary glands. Almost all aspects of the social lives of Thorax salivary glands have secretory units that insects are linked to chemical signals produced open into an excretory duct toward the head and by exocrine glands that occur in high numbers fuses with the ducts of the head salivary glands (Cruz-Landim 1967). The secretory cells of the Corresponding author: J.E. Serrão, [email protected] thorax salivary glands of Scapitotrigona postica Manuscript editor: James Nieh (Meliponini), Xylocopa suspecta (Xylocopini), Proteome of salivary glands in M. quadrifasciata anthidioides 685 and Centris fuscata (Centridini) bees are rich in identify the main protein constituents of both rough endoplasmic reticulum (Cruz-Landim the head and thorax salivary glands in the 2009) and may be involved in the production stingless bee Melipona quadrifasciata anthi- of enzymes, such as proteases, lipases, and dioides workers to enhance the understanding of lactases, as reported for Apotrigona nebulata, the functions of these glands in social bees. Melipona becheeii, and S. postica (Arnold and Delage-Darchen 1978; Delage-Darchen et al. 2. MATERIAL AND METHODS 1979; Delage-Darchen and Darchen 1982; Costa and Cruz-Landim 2001). Nine proteins 2.1. Bees and salivary glands occur in both thorax salivary gland of Apis melifera workers and in stored royal jelly Forager workers of M. quadrifasciata anthidioides (Fujita et al. 2012). were obtained from three colonies kept in the apiary The head salivary glands occur only in the of the Federal University of Viçosa (20°45′ N, 42°52′ stingless bees Euglossini, Bombini, Meliponini, W), Viçosa state of Minas Gerais, Brazil. and Apini (Cruz-Landim 2009). These glands For head and thorax salivary gland extraction, 51 are derived from a secondary growth of the forager workers were collected from each colony, thorax salivary glands and are formed by totaling 153 bees. The bees were collected from close multicellular alveoli with a thin cuticle lining to the colony entrance when returning with corbicu- the gland lumen (Cruz-Landim 1967). Secretory lae loaded with pollen grains. Bees were cryoanes- cells of the head salivary gland have features of thetized, dissected in phosphate-buffered saline, and cells that metabolize lipids in old bees, but in the head and thorax salivary glands were transferred young workers, the secretory cells have well- to 1 % protease inhibitor cocktail (Sigma, P27147), developed rough endoplasmic reticulum and homogenized in buffer [(7 M urea, 2 M thiourea, 4 % high concentrations of free ribosomes (Cruz- CHAPS, 2 % immobilized pH gradient (IPG) buffer, Landim 2009). A possible function of the head 40 mM dithiothreitol (DTT)], and centrifuged at salivary glands is to contribute to the worker’s 14,000×g for 30 min at 4 °C. To obtain soluble recruitment for foraging and trail marking proteins, only the supernatant was collected and (Jarau et al. 2004a). In the stingless bees stored at −80 °C until use. The amount of protein in Geotrigona subterrania and Geotrigona mom- the samples was determined according to the Brad- buca, head salivary glands and mandibular ford method using bovine serum albumin as a glands together play a role in marking food standard. sources and worker recruitment (Blum et al. 1970; Stangler et al. 2009). Moreover, in the 2.2. Two-dimensional gel electrophoresis orchid bee Euglossa viridissima, the head salivary glands play a role in the mechanism For isoelectric focusing of soluble proteins from of fragrance collection in plants (Eltz et al. the head and thorax salivary glands, immobiline 2007). The secretion of the head salivary glands DryStrip, pH 3–10 (7 cm, GE Healthcare), were is also related to wax manipulation for nest rehydrated in 150 μL of rehydration buffer (7 M urea, building (Heselhaus 1922), mandible lubrication 2 M thiourea, 4 % CHAPS, 2 % IPG buffer, 0.002 % (Simpson 1960), and resin manipulation (Santos Bromophenol blue) containing 100 μg of protein et al. 2009). In A. mellifera, head salivary from each sample for 24 h in five voltage steps (200- glands produce some proteins found in royal V step-n-hold for 1 h, 500-V step-n-hold for 1 h, jelly (Fujita et al. 2012). 1,000-V gradient for 1 h, 8,000-V gradient for 3 h, Considering that the head and thorax salivary and 8,000-V gradient for 4 h). The Ettan IPGphor glands of bees produce different substances that III® was used for focusing. The second dimension of have different functions as well as the ecolog- sodium dodecyl sulfate polyacrylamide gel electro- ical and economic importance and the risk of phoresis (SDS-PAGE) was performed using a Mini extinction of stingless bees, this study aimed to Protean IITM (Bio Rad) onto a 12 % polyacrylamide 686 D. Elias-Santos et al. gel. The focused strips were equilibrated in buffer the mass range of 800–4,500 Da with about 1,500 (6 M urea, 75 mM Tris–HCl, 29.3 % glycerol, 2 % laser shots. For each sample spot, a data-dependent SDS, 0.002 % Bromophenol blue) containing 1 % acquisition method was created to select the four most DTT for 20 min under stirring. Following this, the intense peaks, excluding those from the matrix, trypsin buffer was replaced by the same buffer containing autolysis, or acrylamide, for subsequent MS/MS data 2.5 % iodoacetamide for 20 min in the dark. The acquisition. Mass spectra were internally calibrated with strips were then washed for 5 s in running buffer (3 % autodigested peaks of trypsin (MH+ =842.5, Tris–HCl, 14.4 % glycine, 1 % SDS, pH 8.8) and run 2,211.42 Da) allowing a mass accuracy >25 ppm. on 12 % SDS-PAGE gels at 200 V for 50 min. The gel was stained for 16 h in Coomassie G-250 solution 2.5. Protein identification (0.002 % Coomassie blue G-250, 10 % acetic acid, 50 % ethanol). To validate the data, three gels were The spectra were processed and analyzed using made for each gland. Then, the gels were digitalized the Global Protein Server Workstation (Applied and analyzed using Image Master 2D Platinum 7.0 Biosystems), which uses internal MASCOT software for spot detection and analysis. Each spot was (v.2.1.0, Matrix Science, London, UK) to search the assigned a different symbol for identification and peptide mass fingerprints and MS/MS data.
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