Functional genomics of Apis mellifera: search for new genes and functional networks in the context of development, different castes and reproduction

• Grant number: 05/03926-5
• Support Opportunities: Research Projects - Thematic Grants
• Duration: May 01, 2006 - June 30, 2010
• Field of knowledge: Biological Sciences - Genetics - Animal Genetics
• Principal Investigator: Zilá Luz Paulino Simões
• Grantee: Zilá Luz Paulino Simões
• Host Institution: Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto (FFCLRP). Universidade de São Paulo (USP). Ribeirão Preto , SP, Brazil
• Pesquisadores principais: Klaus Hartmann Hartfelder ; Marcia Maria Gentile Bitondi
• Associated scholarship(s): 09/15635-6 - Characterization of genes encoding bursicona and research function of the product as possible heterodimeric regulator of differentiation of the exoskeleton of adult Apis mellifera, BP.IC; 09/05675-0 - Differential gene expression and induction of morphological characters in Apis mellifera, BP.DR; 09/00810-7 - Differential brain development and transcription profile of genes related to neurogenesis in castes of Apis mellifera, BP.PD; + associated scholarships 08/09505-0 - Differentially expressed genes in the development of the hindlegs of queens and workers of the honey bee, Apis mellifera, BP.DR; 08/05246-0 - Regulation of genes related with juvenile hormone metabolism in Apis mellifera, relationship with insulin-TOR pathway and dietary status, BP.PD; 08/00541-3 - Hexamerin genes in Apis mellifera: searching for alternative roles during development, BP.DR; 08/01446-4 - Molecular determinants of workers development in Apis mellifera, BP.DR; 07/08300-2 - Differentiation of adult in corbiculate bees: heterochrony of cuticular morphogenesis and secondary sources of ecdisteroids, BP.DR; 07/07594-2 - Regulatory and functional networks associated to vitellogenin gene expression in Apis mellifera castes, BP.PD; 07/05416-0 - FUNCTIONAL ANALYSIS OF CADHERINS IN Apis mellifera: PRODUCTION OF SPECIFIC ANTIBODIES AND RNAi MEDIATED SILENCING OF GENE FUNCTION, BP.DR; 07/05324-8 - Quantification of methil farnesoate epoxidase gene in Apis mellifera corpora allata and its regulation by JH and dietary in adult workers, BP.IC - associated scholarships

Abstract

With an active contribution (5021 ORESTES, deposited in the GenBank) and participation in the annotation of the recently sequenced genome of the honey bee our group now has consolidated knowledge and expertise in all aspects required for large-scale analyses of gene expression in honey bees. Following our long term questions of interest on mechanisms underlying caste and sex determination and those involved in reproduction and division of labor, already formulated in the pré-genomic era of honey bee research, we are now proposing a large-scale analysis of gene expression in different phases of the honey bee life cycle. We will focus on the following questions: the identification of genes involved in caste development, in programmed cell death of the larval ovary, in integument differentiation, in the activation of the adult ovary of queens and workers, in the functional cycle of the hypopharyngeal glands, and in early embryonic sex determination. In addition, we will screen our libraries for putative micro-RNAs to unveil the participation of this novel group of post-transcriptional regulators in the above contexts. The project adopts a dual strategy, a) the identification of candidate genes in the honey bee genome based on prior knowledge of gene function in other organisms, especially Gene Ontology attributes registered in flybase, and b) the search for novel genes by microarrays, subtractive hybridization strategies, and the generation of an embryonic cDNA library. The differential expression of all these genes will be tested and candidates of specific interest will be investigated by quantitative RT-PCR and silencing by RNAi. The joint information on gene expression in these contexts will be subjected to network analysis in order to detect functional linkage and organization in gene expression networks. (AU)

Scientific publications

(30)

(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)

DE PAULA JUNIOR, D. E.; DE OLIVEIRA, M. T.; BRUSCADIN, J. J.; PINHEIRO, D. G.; BOMTORIN, A. D.; COELHO JUNIOR, V. G.; MODA, L. M. R.; SIMOES, Z. L. P.; BARCHUK, A. R.. Caste-specific gene expression underlying the differential adult brain development in the honeybee Apis mellifera. Insect Molecular Biology, v. 30, n. 1, p. 42-56, FEB 2021. (11/03171-5, 05/03926-5)

VIEIRA, J.; FREITAS, F. C. P.; CRISTINO, A. S.; MODA, L. M. R.; MARTINS, J. R.; BITONDI, M. M. G.; SIMOES, Z. L. P.; BARCHUK, A. R.. miRNA-34 and miRNA-210 target hexamerin genes enhancing their differential expression during early brain development of honeybee (Apis mellifera) castes. Insect Molecular Biology, v. 30, n. 6, AUG 2021. (11/03171-5, 05/03926-5)

VIEIRA, JOSEANA; DE PAULA FREITAS, FLAVIA CRISTINA; CRISTINO, ALEXANDRE SANTOS; PINHEIRO, DANIEL GUARIZ; AGUIAR, LUIZ ROBERTO; FRAMARTINO BEZERRA LAURE, MARCELA APARECIDA; ROSATTO MODA, LIVIA MARIA; PAULINO SIMOES, ZILA LUZ; BARCHUK, ANGEL ROBERTO. olecular underpinnings of the early brain developmental response to differential feeding in the honey bee Apis mellifer. BIOCHIMICA ET BIOPHYSICA ACTA-GENE REGULATORY MECHANISMS, v. 1864, n. 9, SEP 2021. (11/03171-5, 05/03926-5)

LOURENCO, ANETE PEDRO; MARTINS, JULIANA RAMOS; SILVA TORRES, FERNANDA ANDRADE; MACKERT, ALINE; AGUIAR, LUIZ ROBERTO; HARTFELDER, KLAUS; GENTILE BITONDI, MARCIA MARIA; PAULINO SIMOES, ZILA LUZ. Immunosenescence in honey bees (Apis mellifera L.) is caused by intrinsic senescence and behavioral physiology. Experimental Gerontology, v. 119, p. 174-183, MAY 2019. (05/03302-1, 05/03926-5, 11/03171-5)

MELLO, T. R. P.; ALEIXO, A. C.; PINHEIRO, D. G.; NUNES, F. M. F.; CRISTINO, A. S.; BITONDI, M. M. G.; BARCHUK, A. R.; SIMOES, Z. L. P.. Hormonal control and target genes of ftz-f1 expression in the honeybee Apis mellifera: a positive loop linking juvenile hormone, ftz-f1, and vitellogenin. Insect Molecular Biology, v. 28, n. 1, p. 145-159, FEB 2019. (05/03926-5, 08/10757-3, 11/03171-5)

CRISTINO, A. S.; NUNES, F. M. F.; BARCHUK, A. R.; AGUIAR-COELHO, V. M.; SIMOES, Z. L. P.; BITONDI, M. M. G.. Organization, evolution and transcriptional profile of hexamerin genes of the parasitic wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). Insect Molecular Biology, v. 19, p. 10-pg., 2010-02-01. (05/03926-5, 07/07594-2)

LOURENCO, ANETE PEDRO; MARTINS, JULIANA RAMOS; GUIDUGLI-LAZZARINI, KARINA ROSA; FROES MACEDO, LILIANE MARIA; GENTILE BITONDI, MARCIA MARIA; PAULINO SIMOES, ZILA LUZ. Potential costs of bacterial infection on storage protein gene expression and reproduction in queenless Apis mellifera worker bees on distinct dietary regimes. JOURNAL OF INSECT PHYSIOLOGY, v. 58, n. 9, p. 1217-1225, SEP 2012. (05/03926-5)

BOMTORIN, ANA DURVALINA; BARCHUK, ANGEL ROBERTO; MODA, LIVIA MARIA; PAULINO SIMOES, ZILA LUZ. Hox Gene Expression Leads to Differential Hind Leg Development between Honeybee Castes. PLoS One, v. 7, n. 7, JUL 25 2012. (11/03171-5, 05/03926-5, 09/05675-0)

MODA, LIVIA MARIA; VIEIRA, JOSEANA; GUIMARAES FREIRE, ANNA CLAUDIA; BONATTI, VANESSA; BOMTORIN, ANA DURVALINA; BARCHUK, ANGEL ROBERTO; PAULINO SIMOES, ZILA LUZ. Nutritionally Driven Differential Gene Expression Leads to Heterochronic Brain Development in Honeybee Castes. PLoS One, v. 8, n. 5, MAY 30 2013. (09/00810-7, 05/03926-5, 09/05675-0)

MARTINS, JULIANA R.; ANHEZINI, LUCAS; DALLACQUA, RODRIGO P.; SIMOES, ZILA L. P.; BITONDI, MARCIA M. G.. A Honey Bee Hexamerin, HEX 70a, Is Likely to Play an Intranuclear Role in Developing and Mature Ovarioles and Testioles. PLoS One, v. 6, n. 12, DEC 9 2011. (10/16380-9, 08/00541-3, 05/03926-5)

AMDAM, GRO V.; NILSEN, KARI-ANNE; NORBERG, KARI; FONDRK, M. KIM; HARTFELDER, KLAUS. Variation in endocrine signaling underlies variation in social life history. American Naturalist, v. 170, n. 1, p. 37-46, July 2007. (05/03926-5)

BARCHUK, ANGEL R.; CRISTINO, ALEXANDRE S.; KUCHARSKI, ROBERT; COSTA, LUCIANO F.; SIMÕES, ZILÁ L. P.; MALESZKA, RYSZARD. Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Developmental Biology, v. 7, n. 70, 2007. (05/03926-5, 99/00719-6, 05/00587-5)

GUIDUGLI-LAZZARINI, KARINA ROSA; DO NASCIMENTO, ADRIANA MENDES; TANAKA, ERICA DONATO; DOLORS PIULACHS, MARIA; HARTFELDER, KLAUS; BITONDI, MARCIA GENTILE; SIMOES, ZILA LUZ PAULINO. Expression analysis of putative vitellogenin and lipophorin receptors in honey bee (Apis mellifera L.) queens and workers. JOURNAL OF INSECT PHYSIOLOGY, v. 54, n. 7, p. 1138-1147, JUL 2008. (05/03926-5)

ELIAS-NETO, MOYSES; NASCIMENTO, ANA L. O.; BONETTI, ANA M.; NASCIMENTO, FABIO S.; MATEUS, SIDNEI; GAROFALO, CARLOS A.; BITONDI, MARCIA M. G.. Heterochrony of cuticular differentiation in eusocial corbiculate bees. Apidologie, v. 45, n. 4, p. 397-408, JUL 2014. (12/09108-6, 07/08300-2, 10/16380-9, 05/03926-5)

COLONELLO-FRATTINI, NINIVE AGUIAR; GUIDUGLI-LAZZARINI, KARINA ROSA; PAULINO SIMOES, ZILA LUZ; HARTFELDER, KLAUS. Mars is close to venus - Female reproductive proteins are expressed in the fat body and reproductive tract of honey bee (Apis mellifera L.) drones. JOURNAL OF INSECT PHYSIOLOGY, v. 56, n. 11, p. 1638-1644, NOV 2010. (05/03926-5)

FRANCO NUNES, FRANCIS MORAIS; PAULINO SIMOES, ZILA LUZ. A non-invasive method for silencing gene transcription in honeybees maintained under natural conditions. Insect Biochemistry and Molecular Biology, v. 39, n. 2, p. 157-160, FEB 2009. (05/03926-5)

BARCHUK‚ A.R.; CRISTINO‚ A.S.; KUCHARSKI‚ R.; COSTA‚ L.F.; SIMÕES‚ Z.L.P.; MALESZKA‚ R.. Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Developmental Biology, v. 7, n. 1, p. 70, 2007. (05/00587-5, 05/03926-5, 99/00719-6)

LOURENÇO‚ A.P.; MACKERT‚ A.; CRISTINO‚ A.S.; SIMÕES‚ Z.L.P.. Validation of reference genes for gene expression studies in the honey bee‚ Apis mellifera‚ by quantitative real-time RT-PCR. Apidologie, v. 39, n. 3, p. 372-385, 2008. (05/03926-5)

COLONELLO-FRATTINI‚ N.A.; HARTFELDER‚ K.. Differential gene expression profiling in mucus glands of honey bee (Apis mellifera) drones during sexual maturation. Apidologie, v. 40, n. 4, p. 481-495, 2009. (99/00719-6, 05/03926-5)

TELES‚ A.C.A.S.; MELLO‚ T.R.P.; BARCHUK‚ A.R.; SIMÕES‚ Z.L.P.. Ultraspiracle of the stingless bees Melipona scutellaris and Scaptotrigona depilis: cDNA sequence and expression profiles during pupal development. Apidologie, v. 38, n. 5, p. 462-471, 2007. (05/03926-5)

ELIAS-NETO, MOYSES; SOARES, MICHELLE P. M.; SIMOES, ZILA L. P.; HARTFELDER, KLAUS; BITONDI, MARCIA M. G.. Developmental characterization, function and regulation of a Laccase2 encoding gene in the honey bee, Apis mellifera (Hymenoptera, Apinae). Insect Biochemistry and Molecular Biology, v. 40, n. 3, p. 11-pg., 2010-03-01. (07/08300-2, 05/03926-5, 05/03301-5)

BOMTORIN, ANA DURVALINA; MACKERT, ALINE; COUTO ROSA, GUSTAVO CONRADO; MODA, LIVIA MARIA; MARTINS, JULIANA RAMOS; GENTILE BITONDI, MARCIA MARIA; HARTFELDER, KLAUS; PAULINO SIMOES, ZILA LUZ. Juvenile Hormone Biosynthesis Gene Expression in the corpora allata of Honey Bee (Apis mellifera L.) Female Castes. PLoS One, v. 9, n. 1, JAN 29 2014. (11/03171-5, 05/03926-5, 09/05675-0)

CRISTINO, A. S.; NUNES, F. M. F.; BARCHUK, A. R.; AGUIAR-COELHO, V. M.; SIMOES, Z. L. P.; BITONDI, M. M. G.. Organization, evolution and transcriptional profile of hexamerin genes of the parasitic wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). Insect Molecular Biology, v. 19, n. 1, SI, p. 137-146, FEB 2010. (05/03926-5, 07/07594-2)

SOARES, MICHELLE P. M.; SILVA-TORRES, FERNANDA A.; ELIAS-NETO, MOYSES; NUNES, FRANCIS M. F.; SIMOES, ZILA L. P.; BITONDI, MARCIA M. G.. Ecdysteroid-Dependent Expression of the Tweedle and Peroxidase Genes during Adult Cuticle Formation in the Honey Bee, Apis mellifera. PLoS One, v. 6, n. 5, MAY 31 2011. (07/04314-9, 07/07594-2, 07/08300-2, 05/03926-5)

MACKERT, ALINE; HARTFELDER, KLAUS; GENTILE BITONDI, MARCIA MARIA; PAULINO SIMOES, ZILA LUZ. The juvenile hormone (JH) epoxide hydrolase gene in the honey bee (Apis mellifera) genome encodes a protein which has negligible participation in JH degradation. JOURNAL OF INSECT PHYSIOLOGY, v. 56, n. 9, p. 1139-1146, SEP 2010. (05/03926-5)

MARTINS, JULIANA R.; NUNES, FRANCIS M. F.; CRISTINO, ALEXANDRE S.; SIMOES, ZILAL P.; BITONDI, MARCIA M. G.. The four hexamerin genes in the honey bee: structure, molecular evolution and function deduced from expression patterns in queens, workers and drones. BMC MOLECULAR BIOLOGY, v. 11, MAR 26 2010. (08/00541-3, 05/03926-5)

ELIAS-NETO‚ M.; SOARES‚ M.P.M.; BITONDI‚ M.M.G.. Changes in integument structure during the imaginal molt of the honey bee. Apidologie, v. 40, n. 1, p. 29-39, 2009. (05/03926-5, 05/03301-5)

MARCO ANTONIO, DAVID SANTOS; GUIDUGLI-LAZZARINI, KARINA ROSA; DO NASCIMENTO, ADRIANA MENDES; PAULINO SIMOES, ZILA LUZ; HARTFELDER, KLAUS. RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers. NATURWISSENSCHAFTEN, v. 95, n. 10, p. 953-961, OCT 2008. (05/03926-5)

ELIAS-NETO, MOYSES; SOARES, MICHELLE P. M.; SIMOES, ZILA L. P.; HARTFELDER, KLAUS; BITONDI, MARCIA M. G.. Developmental characterization, function and regulation of a Laccase2 encoding gene in the honey bee, Apis mellifera (Hymenoptera, Apinae). Insect Biochemistry and Molecular Biology, v. 40, n. 3, SI, p. 241-251, MAR 2010. (07/08300-2, 05/03926-5, 05/03301-5)

MACKERT, ALINE; NASCIMENTO, ADRIANA MENDES DO; BITONDI, MÁRCIA MARIA GENTILE; HARTFELDER, KLAUS; SIMÕES, ZILÁ LUZ PAULINO. Identification of a juvenile hormone esterase-like gene in the honey bee, Apis mellifera L. - Expression analysis and functional assays. COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY B-BIOCHEMISTRY & MOLECULAR BIOLOGY, v. 150, n. 1, p. 33-44, May 2008. (05/03926-5)