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Causal analysis of Apis mellifera development - regulatory genes and hierachical networks of gene expression in the specification of tissue and organs

Grant number: 11/03171-5
Support type:Research Projects - Thematic Grants
Duration: August 01, 2011 - January 31, 2016
Field of knowledge:Biological Sciences - Genetics - Molecular Genetics and Genetics of Microorganisms
Principal researcher:Zilá Luz Paulino Simões
Grantee:Zilá Luz Paulino Simões
Home Institution: Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto (FFCLRP). Universidade de São Paulo (USP). Ribeirão Preto , SP, Brazil
Principal researchers:Klaus Hartmann Hartfelder
Assoc. researchers:Marcia Maria Gentile Bitondi
Associated grant(s):13/16208-0 - EMBO | EMBL Symposium: The Non-Coding Genome, AR.EXT
Associated scholarship(s):15/04823-7 - Detection of transcripts zelda during oogenesis of Apis mellifera, BP.IC
14/26659-1 - Function of DNA methyltransferases and caracterization of the DNA methylation profile in the aging process of honey bees (Apis mellifera, Apidae, Hymenoptera), BP.MS
14/18091-5 - Identification and characterization of miRNA-target interactions in the metamorphosis of Apis mellifera, BP.MS
+ associated scholarships 14/14194-4 - Molecular characterization of circadian cycle elements in the development and senescence of Apis mellifera, BP.DR
14/08147-3 - Genes differently expressed during ovary development in the bee, Apis mellifera., BP.MS
14/05757-5 - Functional analysis of the long noncoding ovary-1 (lncov1) gene and the transcriptome of worker ovaries of the honey bee, Apis mellifera L., BP.DR
13/24733-7 - Oxidative metabolism in caste differentiation in honeybees: number and structure of gene expression and mitochondrial functional indicators, BP.DR
12/24284-5 - Comparative approach of cuticular maturation heterochrony in social and solitary bees using RNA-Seq, hydrocarbons quantification and electron microscopy, BP.DR
12/12941-1 - Next-generation mRNA sequencing for high-throughput analysis of the metamorphosis in Apis mellifera castes, BP.PD
12/15096-0 - Expression of a nitric oxide synthase and nitric oxide levels in the development of queens and workers of Apis mellifera, BP.MS
12/07641-9 - Egfr and Hypoxia pathways in Apis mellifera queens and workers development - a sistemic approach of their interaction with Juvenile Hormone and Nitric acid, BP.PD
11/15810-2 - Functional analysis of lnc-ovary-1 (Group11.31), the first long non-coding RNA in Apis mellifera, caste-specific development in the ovary, BP.MS
11/21731-8 - Regulatory molecules of larval growth and metamorphosis in honeybee workers Apis mellifera, BP.IC
09/15772-3 - Caste-specific molecular determinants of ovary development in the honey bee, Apis mellifera., BP.PD - associated scholarships

Abstract

Bees are by far the most important pollinators in both natural and agricultural ecosystems, and the recent decline of their populations poses a major threat to this equilibrium. A promising strategy to overcome or at least diminish this risk is the mass rearing of these pollinators by means of rational management techniques. These, however, require profound knowledge on these organisms in terms of systems biology. Although since decades honey bees are well studied and figure as a model organism for behavioral plasticity, communication, learning and memory, important aspects of their biology are still little understood. The thousands of individuals that compose a colony show coordinated behavior and a highly sophisticated organization, wherein a single queen, a female tuned to high reproductive output, produces some eggs that give rise to males, an even a lesser number of eggs that will develop into female reproductives, whilst the overwhelming majority of the her eggs will give rise to workers. These workers are facultatively sterile females which have a well developed nervous system essential facing complex cognitive challenges to which queens are not exposed. The aims of this project are to provide insights into the developmental biology of bees by means of state-of-the-art protocols of Genetics and Molecular Biology, as well as to understand the flux of this information through hierarchical regulatory networks of gene expression. Such state-of-the-art tools are: Next Generation Sequencing, ab initio analysis of the A. mellifera genome, especially of regulatory RNAs, analyses of gene expression through microarrays, as well as functional approaches, such as RNA interference, in situ hybridization and immunohistochemistry. All results should finally serve to construct gene regulatory networks. (AU)

Articles published in Agência FAPESP Newsletter about the research grant:
MicroRNAs agem como moduladores do comportamento das abelhas 
MicroRNAs act as modulators of bee behavior  
Revista <i>Nature Genetics</i> destaca pesquisa brasileira 
Articles published in Pesquisa FAPESP Magazine about the research grant:
A theory in motion 
Un enjambre ordenado 
An orderly swarm 

Scientific publications (24)
(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. Web of Science Citations: 0.
SANTOS, DOUGLAS ELIAS; SOUZA, ANDERSON DE OLIVEIRA; TIBERIO, GUSTAVO JACOMINI; ALBERICI, LUCIANE CARLA; HARTFELDER, KLAUS. Differential expression of antioxidant system genes in honey bee (Apis mellifera L.) caste development mitigates ROS-mediated oxidative damage in queen larvae. GENETICS AND MOLECULAR BIOLOGY, v. 43, n. 4 2020. Web of Science Citations: 0.
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. Web of Science Citations: 1.
FALCON, TIAGO; PINHEIRO, DANIEL G.; FERREIRA-CALIMAN, MARIA JULIANA; TURATTI, IZABEL C. C.; PINTO DE ABREU, FABIANO C.; GALASCHI-TEIXEIRA, JULIANA S.; MARTINS, JULIANA R.; ELIAS-NETO, MOYSES; SOARES, MICHELLE P. M.; LAURE, MARCELA B.; FIGUEIREDO, VERA L. C.; LOPES, NORBERTO PEPORINE; SIMOES, ZILA L. P.; GAROFALO, CARLOS A.; BITONDI, MARCIA M. G. Exploring integument transcriptomes, cuticle ultrastructure, and cuticular hydrocarbons profiles in eusocial and solitary bee species displaying heterochronic adult cuticle maturation. PLoS One, v. 14, n. 3 MAR 14 2019. Web of Science Citations: 2.
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. Web of Science Citations: 0.
CARDOSO-JUNIOR, CARLOS A. M.; GUIDUGLI-LAZZARINI, KARINA R.; HARTFELDER, KLAUS. DNA methylation affects the lifespan of honey bee (Apis mellifera L.) workers - Evidence for a regulatory module that involves vitellogenin expression but is independent of juvenile hormone function. Insect Biochemistry and Molecular Biology, v. 92, p. 21-29, JAN 2018. Web of Science Citations: 7.
CERVONI, MARIO S.; CARDOSO-JUNIOR, CARLOS A. M.; CRAVEIRO, GIOVANA; SOUZA, ANDERSON DE O.; ALBERICI, LUCIANE C.; HARTFELDER, KLAUS. Mitochondrial capacity, oxidative damage and hypoxia gene expression are associated with age-related division of labor in honey bee (Apis mellifera L.) workers. Journal of Experimental Biology, v. 220, n. 21, p. 4035-4046, NOV 1 2017. Web of Science Citations: 6.
NELSON, RONALD M.; WALLBERG, ANDREAS; PAULINO SIMOES, ZILA LUZ; LAWSON, DANIEL J.; WEBSTER, MATTHEW T. Genomewide analysis of admixture and adaptation in the Africanized honeybee. Molecular Ecology, v. 26, n. 14, p. 3603-3617, JUL 2017. Web of Science Citations: 15.
FREITAS, FLAVIA C. P.; PIRES, CAMILLA V.; CLAUDIANOS, CHARLES; CRISTINO, ALEXANDRE S.; SIMOES, ZILA L. P. MicroRNA-34 directly targets pair-rule genes and cytoskeleton component in the honey bee. SCIENTIFIC REPORTS, v. 7, JAN 18 2017. Web of Science Citations: 5.
MARCO ANTONIO, DAVID S.; HARTFELDER, KLAUS. Toward an Understanding of Divergent Compound Eye Development in Drones and Workers of the Honeybee (Apis mellifera L.): A Correlative Analysis of Morphology and Gene Expression. JOURNAL OF EXPERIMENTAL ZOOLOGY PART B-MOLECULAR AND DEVELOPMENTAL EVOLUTION, v. 328, n. 1-2, p. 139-156, JAN-FEB 2017. Web of Science Citations: 3.
LAGO, DENYSE CAVALCANTE; HUMANN, FERNANDA CARVALHO; BARCHUK, ANGEL ROBERTO; ABRAHAM, KURUVILLA JOSEPH; HARTFELDER, KLAUS. Differential gene expression underlying ovarian phenotype determination in honey bee, Apis mellifera L., caste development. Insect Biochemistry and Molecular Biology, v. 79, p. 1-12, DEC 2016. Web of Science Citations: 8.
MACEDO, L. M. F.; NUNES, F. M. F.; FREITAS, F. C. P.; PIRES, C. V.; TANAKA, E. D.; MARTINS, J. R.; PIULACHS, M. -D.; CRISTINO, A. S.; PINHEIRO, D. G.; SIMOES, Z. L. P. MicroRNA signatures characterizing caste-independent ovarian activity in queen and worker honeybees (Apis mellifera L.). Insect Molecular Biology, v. 25, n. 3, p. 216-226, JUN 2016. Web of Science Citations: 10.
MARTINS, JULIANA RAMOS; GENTILE BITONDI, MARCIA MARIA. The HEX 110 Hexamerin Is a Cytoplasmic and Nucleolar Protein in the Ovaries of Apis mellifera. PLoS One, v. 11, n. 3 MAR 8 2016. Web of Science Citations: 4.
PIRES, CAMILLA VALENTE; DE PAULA FREITAS, FLAVIA CRISTINA; CRISTINO, ALEXANDRE S.; DEARDEN, PETER K.; PAULINO SIMOES, ZILA LUZ. Transcriptome Analysis of Honeybee (Apis Mellifera) Haploid and Diploid Embryos Reveals Early Zygotic Transcription during Cleavage. PLoS One, v. 11, n. 1 JAN 11 2016. Web of Science Citations: 9.
SADD, BEN M.; BARRIBEAU, SETH M.; BLOCH, GUY; DE GRAAF, DIRK C.; DEARDEN, PETER; ELSIK, CHRISTINE G.; GADAU, JUERGEN; GRIMMELIKHUIJZEN, CORNELIS J. P.; HASSELMANN, MARTIN; LOZIER, JEFFREY D.; ROBERTSON, HUGH M.; SMAGGHE, GUY; STOLLE, ECKART; VAN VAERENBERGH, MATTHIAS; WATERHOUSE, ROBERT M.; BORNBERG-BAUER, ERICH; KLASBERG, STEFFEN; BENNETT, ANNA K.; CAMARA, FRANCISCO; GUIGO, RODERIC; HOFF, KATHARINA; MARIOTTI, MARCO; MUNOZ-TORRES, MONICA; MURPHY, TERENCE; SANTESMASSES, DIDAC; AMDAM, GRO V.; BECKERS, MATTHEW; BEYE, MARTIN; BIEWER, MATTHIAS; BITONDI, MARCIA M. G.; BLAXTER, MARK L.; BOURKE, ANDREW F. G.; BROWN, MARK J. F.; BUECHEL, SEVERINE D.; CAMERON, ROSSANAH; CAPPELLE, KAAT; CAROLAN, JAMES C.; CHRISTIAENS, OLIVIER; CIBOROWSKI, KATE L.; CLARKE, DAVID F.; COLGAN, THOMAS J.; COLLINS, DAVID H.; CRIDGE, ANDREW G.; DALMAY, TAMAS; DREIER, STEPHANIE; DU PLESSIS, LOUIS; DUNCAN, ELIZABETH; ERLER, SILVIO; EVANS, JAY; FALCON, TIAGO; FLORES, KEVIN; FREITAS, FLAVIA C. P.; FUCHIKAWA, TARO; GEMPE, TANJA; HARTFELDER, KLAUS; HAUSER, FRANK; HELBING, SOPHIE; HUMANN, FERNANDA C.; IRVINE, FRANO; JERMIIN, LARS S.; JOHNSON, CLAIRE E.; JOHNSON, REED M.; JONES, ANDREW K.; KADOWAKI, TATSUHIKO; KIDNER, JONATHAN H.; KOCH, VASCO; KOEHLER, ARIAN; KRAUS, F. BERNHARD; LATTORFF, H. MICHAEL G.; LEASK, MEGAN; LOCKETT, GABRIELLE A.; MALLON, EAMONN B.; ANTONIO, DAVID S. MARCO; MARXER, MONIKA; MEEUS, IVAN; MORITZ, ROBIN F. A.; NAIR, AJAY; NAPFLIN, KATHRIN; NISSEN, INGA; NIU, JINZHI; NUNES, FRANCIS M. F.; OAKESHOTT, JOHN G.; OSBORNE, AMY; OTTE, MARIANNE; PINHEIRO, DANIEL G.; ROSSIE, NINA; RUEPPELL, OLAV; SANTOS, CAROLINA G.; SCHMID-HEMPEL, REGULA; SCHMITT, BJOERN D.; SCHULTE, CHRISTINA; SIMOES, ZILA L. P.; SOARES, MICHELLE P. M.; SWEVERS, LUC; WINNEBECK, EVA C.; WOLSCHIN, FLORIAN; YU, NA; ZDOBNOV, EVGENY M.; AQRAWI, PESHTEWANI K.; BLANKENBURG, KERSTIN P.; COYLE, MARCUS; FRANCISCO, LIEZL; HERNANDEZ, ALVARO G.; HOLDER, MICHAEL; HUDSON, MATTHEW E.; JACKSON, LARONDA; JAYASEELAN, JOY; JOSHI, VANDITA; KOVAR, CHRISTIE; LEE, SANDRA L.; MATA, ROBERT; MATHEW, TITTU; NEWSHAM, IRENE F.; NGO, ROBIN; OKWUONU, GEOFFREY; PHAM, CHRISTOPHER; PU, LING-LING; SAADA, NEHAD; SANTIBANEZ, JIREH; SIMMONS, DENARD; THORNTON, REBECCA; VENKAT, AARTI; WALDEN, KIMBERLY K. O.; WU, YUAN-QING; DEBYSER, GRIET; DEVREESE, BART; ASHER, CLAIRE; BLOMMAERT, JULIE; CHIPMAN, ARIEL D.; CHITTKA, LARS; FOUKS, BERTRAND; LIU, JISHENG; O'NEILL, MEAGHAN P.; SUMNER, SEIRIAN; PUIU, DANIELA; QU, JIAXIN; SALZBERG, STEVEN L.; SCHERER, STEVEN E.; MUZNY, DONNA M.; RICHARDS, STEPHEN; ROBINSON, GENE E.; GIBBS, RICHARD A.; SCHMID-HEMPEL, PAUL; WORLEY, KIM C. The genomes of two key bumblebee species with primitive eusocial organization. Genome Biology, v. 16, APR 24 2015. Web of Science Citations: 131.
CRISTINO, ALEXANDRE S.; BARCHUK, ANGEL R.; FREITAS, FLAVIA C. P.; NARAYANAN, RAMESH K.; BIERGANS, STEPHANIE D.; ZHAO, ZHENGYANG; SIMOES, ZILA L. P.; REINHARD, JUDITH; CLAUDIANOS, CHARLES. Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee. NATURE COMMUNICATIONS, v. 5, NOV 2014. Web of Science Citations: 31.
FALCON, TIAGO; FERREIRA-CALIMAN, MARIA JULIANA; FRANCO NUNES, FRANCIS MORAIS; TANAKA, ERICA DONATO; DO NASCIMENTO, FABIO SANTOS; GENTILE BITONDI, MARCIA MARIA. Exoskeleton formation in Apis mellifera: Cuticular hydrocarbons profiles and expression of desaturase and elongase genes during pupal and adult development. Insect Biochemistry and Molecular Biology, v. 50, p. 68-81, JUL 2014. Web of Science Citations: 21.
DALLACQUA, RODRIGO PIRES; GENTILE BITONDI, MARCIA MARIA. Dimorphic Ovary Differentiation in Honeybee (Apis mellifera) Larvae Involves Caste-Specific Expression of Homologs of Ark and Buffy Cell Death Genes. PLoS One, v. 9, n. 5 MAY 20 2014. Web of Science Citations: 11.
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. Web of Science Citations: 25.
HUMANN, FERNANDA C.; TIBERIO, GUSTAVO J.; HARTFELDER, KLAUS. Sequence and Expression Characteristics of Long Noncoding RNAs in Honey Bee Caste Development - Potential Novel Regulators for Transgressive Ovary Size. PLoS One, v. 8, n. 10 OCT 31 2013. Web of Science Citations: 26.
NUNES, FRANCIS M. F.; IHLE, KATE E.; MUTTI, NAVDEEP S.; SIMOES, ZILA L. P.; AMDAM, GRO V. The gene vitellogenin affects microRNA regulation in honey bee (Apis mellifera) fat body and brain. Journal of Experimental Biology, v. 216, n. 19, p. 3724-3732, OCT 2013. Web of Science Citations: 28.
MIRANDA SOARES, MICHELLE PRIOLI; BARCHUK, ANGEL ROBERTO; QUIRINO SIMOES, ANA CAROLINA; CRISTINO, ALEXANDRE DOS SANTOS; DE PAULA FREITAS, FLAVIA CRISTINA; CANHOS, LUISA LANGE; GENTILE BITONDI, MARCIA MARIA. Genes involved in thoracic exoskeleton formation during the pupal-to-adult molt in a social insect model, Apis mellifera. BMC Genomics, v. 14, AUG 28 2013. Web of Science Citations: 16.
LOURENCO, ANETE P.; GUIDUGLI-LAZZARINI, KARINA R.; FREITAS, FLAVIA C. P.; BITONDI, MARCIA M. G.; SIMOES, ZILA L. P. Bacterial infection activates the immune system response and dysregulates microRNA expression in honey bees. Insect Biochemistry and Molecular Biology, v. 43, n. 5, p. 474-482, MAY 2013. Web of Science Citations: 23.
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. Web of Science Citations: 9.

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