Sex- and caste-specific transcriptomes of larval honey bee (Apis mellifera L.) gonads: DMRT A2 and Hsp83 are differentially expressed and regulated by juvenile hormone.
RNA-seq
differential gene expression
ovary
social insect
testis
Journal
Insect molecular biology
ISSN: 1365-2583
Titre abrégé: Insect Mol Biol
Pays: England
ID NLM: 9303579
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
received:
06
09
2021
accepted:
21
04
2022
pubmed:
8
5
2022
medline:
9
9
2022
entrez:
7
5
2022
Statut:
ppublish
Résumé
The gonads of honey bee, Apis mellifera, queens and drones are each composed of hundreds of serial units, the ovarioles and testioles, while the ovaries of the adult subfertile workers consist of only few ovarioles. We performed a comparative RNA-seq analysis on early fifth-instar (L5F1) larval gonads, which is a critical stage in gonad development of honey bee larvae. A total of 1834 genes were identified as differentially expressed (Padj < 0.01) among the three sex and caste phenotypes. The Gene Ontology analysis showed significant enrichment for metabolism, protein or ion binding, and oxidoreductase activity, and a KEGG analysis revealed metabolic pathways as enriched. In a principal component analysis for the total transcriptomes and hierarchical clustering of the DEGs, we found higher similarity between the queen and worker ovary transcriptomes compared to the drone testis, despite the onset of programmed cell death in the worker ovaries. Four DEGs were selected for RT-qPCR analyses, including their response to juvenile hormone (JH), which is a critical factor in the caste-specific development of the ovaries. Among these, DMRT A2 and Hsp83 were found upregulated by JH and, thus, emerged as potential molecular markers for sex- and caste-specific gonad development in honey bees.
Substances chimiques
Juvenile Hormones
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
593-608Informations de copyright
© 2022 Royal Entomological Society.
Références
Aufauvre, J., Misme-Aucouturier, B., Viguès, B., Texier, C., Delbac, F. & Blot, N. (2014) Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLoS One, 9, e91686. https://doi.org/10.1371/journal.pone.0091686
Barton, L.J., LeBlanc, M.G. & Lehmann, R. (2016) Finding their way: themes in germ cell migration. Current Opinion in Cell Biology, 42, 128-137. https://doi.org/10.1016/j.ceb.2016.07.007
Belles, X. (2020) Insect metamorphosis - from natural history to regulation of development and evolution. Cambridge, MA: Academic Press.
Belles, X. & Santos, C.G. (2014) The MEKRE93 (Methoprene tolerant-Krüppel homolog 1-E93) pathway in the regulation of insect metamorphosis, and the homology of the pupal stage. Insect Biochemistry and Molecular Biology, 52, 60-68. https://doi.org/10.1016/j.ibmb.2014.06.009
Beye, M., Hasselmann, M., Fondrk, M.K., Page, R.E. & Omholt, S.W. (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell, 114, 419-429. https://doi.org/10.1016/S0092-8674(03)00606-8
Beye, M., Seelmann, C., Gempe, T., Hasselmann, M., Vekemans, X., Fondrk, M.K. et al. (2013) Gradual molecular evolution of a sex determination switch through incomplete penetrance of femaleness. Current Biology, 23, 2559-2564. https://doi.org/10.1016/j.cub.2013.10.070
Bomtorin, A.D., Mackert, A., Rosa, G.C.C., Moda, L.M., Martins, J.R., Bitondi, M.M.G. et al. (2014) Juvenile hormone biosynthesis gene expression in the corpora allata of honey bee (Apis mellifera L.) female castes. PLoS One, 9, e86923. https://doi.org/10.1371/journal.pone.0086923
Brito, D.V., Silva, C.G.N., Hasselmann, M., Viana, L.S., Astolfi-Filho, S. & Carvalho-Zilse, G.A. (2015) Molecular characterization of the gene feminizer in the stingless bee Melipona interrupta (Hymenoptera: Apidae) reveals association to sex and caste development. Insect Biochemistry and Molecular Biology, 66, 24-30. https://doi.org/10.1016/j.ibmb.2015.09.008
Büchler, R., Andonov, S., Bienefeld, K., Costa, C., Hatjina, F., Kezic, N. et al. (2013) Standard methods for rearing and selection of Apis mellifera queens. Journal of Apicultural Research, 52(1), 1-30. https://doi.org/10.3896/IBRA.1.52.1.07
Cameron, R.C., Duncan, E.J. & Dearden, P.K. (2013) Biased gene expression in early honeybee larval development. BMC Genomics, 14, 913. https://doi.org/10.1186/1471-2164-14-903
Cardoso-Júnior, C.A.M., Oldroyd, B.P. & Ronai, I. (2021) Vitellogenin expression in the ovaries of adult honeybee workers provides insights into the evolution of reproductive and social traits. Insect Molecular Biology, 30, 277-286. https://doi.org/10.1111/imb.12694
Church, S.H., de Medeiros, B.A.S., Donoughe, S., Reyes, N.L.M. & Extavour, C.G. (2021) Repeated loss of variation in insect ovary morphology hughlights the role of development in evolution. Proceedings of the Royal Society B. Biologial Sciences, 288, 20210150. https://doi.org/10.1098/rspb.2021.0150
Cruz-Landim, C. (2009) Abelhas: morfologia e função de sistemas. São Paulo: Editora UNESP.
Ding, D., Parkhurst, S.M., Halsell, S.R. & Lipshitz, H.D. (1993) Dynamic Hsp83 RNA localization during Drosophila oogenesis and embryogenesis. Molecular and Cellular Biology, 13, 3773-3781. https://doi.org/10.1128/mcb.13.6.3773-3781.1993
Evans, J.D. & Wheeler, D.E. (1999) Differential gene expression between developing queens and workers in the honey bee, Apis mellifera. Proceedings of the National Academy of Science of the United States of America, 96, 5575-5580. https://doi.org/10.1073/pnas.96.10.5575
Ewels, P., Magnusson, M., Lundin, S. & Käller, M. (2016) MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics, 32, 3047-3048. https://doi.org/10.1093/bioinformatics/btw354
Ferreira, A., Abdalla, F.C., Kerr, W.E. & Cruz-Landim, C. (2004) Comparative anatomy of the male reproductive internal organs of 51 species of bees. Neotropical Entomology, 33, 569-576. https://doi.org/10.1590/1519-566X2004000500005
Flatt, T., Amdam, G.V., Kirkwood, T.B.L. & Omholt, S.W. (2013) Life-history evolution and the polyphenic regulation of somatic maintenance and survival. The Quarterly Review of Biology, 88, 185-218. https://doi.org/10.1086/671484
Gempe, T. & Beye, M. (2010) Function and evolution of sex determination mechanisms, genes and pathways in insects. BioEssays, 33, 52-60. https://doi.org/10.1002/bies.201000043
Gilboa, L. & Lehmann, R. (2006) Soma-germline interactions coordinate homeostasis and growth in the Drosophila gonad. Nature, 443, 97-100. https://doi.org/10.1038/nature05068
Godt, D. & Laski, F.A. (1995) Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the recruitment of bric-a-brac. Development, 121, 173-187. https://doi.org/10.1242/dev.12.1.1.173
Green, D.A. & Extavour, C.G. (2012) Convergent evolution of a reproductive trait through distinct developmental mechanisms in Drosophila. Developmental Biology, 372, 120-130. https://doi.org/10.1016/j.dbio.2012.09.014
Hartfelder, K. & Steinbrück, G. (1997) Germ cell cluster formation and cell death are alternatives in caste-specific differentiation of the larval honey bee ovary. Invertebrate Reproduction and Development, 31, 237-250. https://doi.org/10.1080/0724259.1997.9672582
Hartfelder, K., Tiberio, G.J., Lago, D.C., Dallacqua, R.P. & Bitondi, M.M.G. (2018) The ovary and its genes-developmental processes underlying the establishment and function of a highly divergent reproductive system in the female castes of the honey bee, Apis mellifera. Apidologie, 49, 49-70. https://doi.org/10.1007/s13592-017-0548-9
Hasselmann, M., Gempe, T., Schiøtt, M., Nunes-Silva, C.G., Otte, M. & Beye, M. (2008) Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature, 454, 519-522. https://doi.org/10.1038/nature07052
Hazelrigg, T., Watkins, W.S., Macey, D., Tu, C., Karow, M. & Lin, X. (1990) The exuperantia gene is required for Drosophila spermatogenesis as well as anteroposterior polarity of the developing oocyte, and encodes overlapping sex-specific transcripts. Genetics, 126, 607-617. https://doi.org/10.1093/genetics/126.3.607
He, Q., Wen, D., Jia, Q., Cui, C., Wang, J., Palli, S.R. et al. (2014) Heat shock protein 83 (hsp83) facilitates methoprene tolerant (met) nuclear import to modulate juvenile hormone signaling. Journal of Biological Chemistry, 289, 27874-27885. https://doi.org/10.1074/jbc.M114.582825
He, X.J., Jiang, W.J., Zhou, M., Barron, A.B. & Zeng, Z.J. (2017) A comparison of honeybee (Apis mellifera) queen, worker and drone larvae by RNA-Seq. Insect Science, 26, 499-509. https://doi.org/10.1111/1744-7917.12557
Hrassnigg, N. & Crailsheim, K. (2005) Differences in drone and worker physiology in honeybees (Apis mellifera). Apidologie, 36, 255-277. https://doi.org/10.1051/apido
Huang, D.W., Sherman, B.T. & Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4, 44-57. https://doi.org/10.1038/nprot.2008.211
Humann, F.C. & Hartfelder, K. (2011) Representational difference analysis (RDA) reveals differential expression of conserved as well as novel genes during caste-specific development of the honey bee (Apis mellifera L.) ovary. Insect Biochemistry and Molecular Biology, 41, 602-612. https://doi.org/10.1016/j.ibmb.2011.03.013
Jia, L.Y., Chen, L., Keller, L., Wang, J., Xiao, J.H. & Huang, D.W. (2019) Doublesex evolution is correlated with social complexity in ants. Genome Biology and Evolution, 10, 3230-3242. https://doi.org/10.1093/gbe/evy250
Jindra, M., Palli, S.R. & Riddiford, L.M. (2013) The juvenile hormone signaling pathway in insect development. Annual Review of Entomology, 58, 181-204. https://doi.org/10.1146/annurev-ento-120811-153700
Johnson, B.R. & Jasper, W.C. (2016) Complex patterns of differential expression in candidate master regulatory genes for social behavior in honey bees. Behavioral Ecology and Sociobiology, 70, 1033-1043. https://doi.org/10.1007/s00265-016-2071-9
Kang, I., Kim, W., Lim, J.Y., Lee, Y. & Shin, C. (2021) Organ-specific transcriptome analysis reveals differential gene expression in different castes under natural conditions in Apis cerana. Scientific Reports, 11, 11267. https://doi.org/10.1038/s41598-021-90635-3
Kerr, W.E. (1974) Sex determination in bees III. Caste determination and genetic control in Melipona. Insectes Sociaux, 21, 357-368.
Kerr, W.E. (1990) Why are workers in social Hymenoptera not males? Brazilian Journal of Genetics, 13, 133-136.
Kim, D., Langmead, B. & Salzberg, S.L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods, 4, 357-360. https://doi.org/10.1038/nmeth.3317
Kim, H.-Y. (2017) Statistical notes for clinical researchers: Chi-squared test and Fisher's exact test. Restorative Dentistry & Endodontics, 42, 152-155. https://doi.org/10.5395/rde.2017.42.2.152
Koeniger, G., Koeniger, N., Ellis, J. & Connor, L. (2014) Mating biology of honey bees (Apis mellifera). Kalamazoo, MI: Wicwas Press.
Kopp, A. (2012) Dmrt genes in the development and evolution of sexual dimorphism. Trends in Genetics, 28, 175-184. https://doi.org/10.1038/jid.2014.371
Korb, J. & Heinze, J. (2021) Ageing and sociality: why, when and how does sociality change ageing patterns? Philosophical Transactions of the Royal Society B Biological Sciences, 376, 2019072720190727. https://doi.org/10.1098/rstb.2019.0727
Lago, D.C., Humann, F.C., Barchuk, A.R., Abraham, K.J. & Hartfelder, K. (2016) Differential gene expression underlying ovarian phenotype determination in honey bee, Apis mellifera L., caste development. Insect Biochemistry and Molecular Biology, 79, 1-12. https://doi.org/10.1016/j.ibmb.2016.10.001
Lago, D.C., Martins, J.R., Dallacqua, R.P., Santos, D.E., Bitondi, M.M.G. & Hartfelder, K. (2020) Testis development and spermatogenesis in drones of the honey bee, Apis mellifera L. Apidologie, 51, 935-955. https://doi.org/10.1007/s13592-020-00773-2
Liao, Y., Smyth, G.K. & Shi, W. (2014) Feature counts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30, 923-930. https://doi.org/10.1093/bioinformatics/btt656
Linksvayer, T.A., Kaftanoglu, O., Akyol, E., Blatch, S., Amdam, G.V. & Page, R.E. (2011) Larval and nurse worker control of developmental plasticity and the evolution of honey bee queen-worker dimorphism. Journal of Evolutionary Biology, 24, 1939-1948. https://doi.org/10.1111/j.1420-9101.2011.02331.x
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
Lourenço, A.P., Mackert, A., Cristino, A.D.S. & Simões, Z.L.P. (2008) Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie, 39, 372-385. https://doi.org/10.1051/apido:2008015
Love, A.M., Anders, S., Huber, W. & Love, M.M. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550. https://doi.org/10.1186/s13059-014-0550-8
Mackert, A., Nascimento, D.A.M., Bitondi, M.M.G., Hartfelder, K. & Simões, Z.L.P. (2008) 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 and Molecular Biology, 150, 33-44. https://doi.org/10.1016/j.cbpb.2008.01.004
Martins, G.F. & Serrão, J.E. (2004) A comparative study of the ovaries in some Brazilian bees (Hymenoptera; Apoidea). Papeis Avulsos de Zoologia, 44, 45-53. https://doi.org/10.1590/S0031-10492003000600001
Méndez-Lucas, A., Hyroššová, P., Novellasdemunt, L., Viñals, F. & Perales, J.C. (2014) Mitochondrial phosphoenolpyruvate carboxykinase (PEPCK-M) is a pro-survival, endoplasmic reticulum (ER) stress response gene involved in tumor cell adaptation to nutrient availability. Journal of Biological Chemistry, 289, 22090-22102.
Michelette, E.R.F. & Soares, A.E.E. (1993) Characterization of preimaginal developmental stages in Africanized honey bee workers (Apis mellifera L.). Apidologie, 24, 431-440. https://doi.org/10.1051/apido:19930410
Page, R.J. & Peng, C. (2001) Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Experimental Gerontology, 36, 695-711.
Rachinsky, A. & Hartfelder, K. (1990) Corpora allata activity, a prime regulating element for caste-specific juvenile hormone titre in honey bee larvae (Apis mellifera carnica). Journal of Insect Physiology, 36, 189-194. https://doi.org/10.1016/0022-1910(90)90121-U
Rachinsky, A., Strambi, C., Strambi, A. & Hartfelder, K. (1990) Caste and metamorphosis - hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae. General and Comparative Endocrinology, 79, 31-38. https://doi.org/10.1016/0016-6480(90)90085-Z
Rangel, J., Böröczky, K., Schal, C. & Tarpy, D.R. (2016) Honey bee (Apis mellifera) queen reproductive potential affects queen mandibular gland pheromone composition and worker retinue response. PLoS One, 11, e0156027. https://doi.org/10.1371/journal.pone.0156027
Rembold, H. (1987) Caste specific modulation of juvenile hormone titers in Apis mellifera. Insect Biochemistry, 17, 1003-1006. https://doi.org/10.1016/0020-1790(87)90110-7
Rembold, H., Kremer, J.-P. & Ulrich, G.M. (1980) Characterization of postembryonic developmental stages of the female castes of the honey bee, Apis mellifera L. Apidologie, 11, 29-38. https://doi.org/10.1051/apido:19800104
Ronai, I., Vergoz, V. & Oldroyd, B.P. (2016) The mechanistic, genetic, and evolutionary basis of worker sterility in the social Hymenoptera. Advances in the Study of Behavior, 48, 251-317. https://doi.org/10.1016/bs.asb.2016.03.002
Roth, A., Vleurinck, C., Netschitailo, O., Bauer, V., Otte, M., Kaftanoglu, O. et al. (2019) A genetic switch for worker nutrition mediated traits in honeybees. PLoS Biology, 17, e3000171. https://doi.org/10.1371/journal.pbio.3000171
Santos, C.G., Humann, F.C. & Hartfelder, K. (2019) Juvenile hormone signaling in insect oogenesis. Current Opinion in Insect Science, 31, 43-48. https://doi.org/10.1016/j.cois.2018.07.010
Sarikaya, D.P. & Extavour, C.G. (2015) The Hippo pathway regulates homeostatic growth of stem cell niche precursosr in the Drosophila ovary. PLoS Genetics, 11, e1004962. https://doi.org/10.1371/louenal.pgen.1004962
Schmidt Capella, I.C. & Hartfelder, K. (1998) Juvenile hormone effect on DNA synthesis and apoptosis in caste-specific differentiation of the larval honey bee (Apis mellifera L.) ovary. Journal of Insect Physiology, 44, 385-391. https://doi.org/10.1016/S0022-1910(98)00027-4
Slessor, K.N., Kaminski, L.-A., King, G.G.S. & Winston, M.L. (1990) Semiochemicals of the honeybee queen mandibular glands. Journal of Chemical Ecology, 16, 851-860. https://doi.org/10.1007/BF01016495
Snodgrass, R.E. (1956) Anatomy of the honey bee. Ithaca, NY: Cornell University Press.
Stearns, S.C. (1992) The evolution of life histories. Oxford: Oxford University Press.
Verhulst, E.C., van de Zande, L. & Beukeboom, L.W. (2010) Insect sex determination: it all evolves around transformer. Current Opinion in Genetics and Devevelopment, 20, 376-383. https://doi.org/10.1016/j.gde.2010.05.001
Vleurinck, C., Raub, S., Sturgill, D., Oliver, B. & Beye, M. (2016) Linking genes and brain development of honeybee workers: A whole-transcriptome approach. PLoS One, 11, e157980. https://doi.org/10.1371/journal.pone.0157980
Volff, J.-N., Zarkower, D., Bardwell, V.J. & Schartl, M. (2003) Evolutionary dynamics of the DM domain gene family in metazoans. Journal of Molecular Biology, 57, S241-S249. https://doi.org/10.1007/s00239-003-0033-0
Wallberg, A., Bunikis, I., Vinnere-Petterson, O., Mosbech, M.-B., Childers, A.K., Evans, J.D. et al. (2019) A hybrid de novo genome assembly of the honeybee, Apis mellifera, with chromosome-length scaffolds. BMC Genomics, 20, 275. https://doi.org/10.1186/s12864-019-5642-0
Wang, L., Wang, S. & Li, W. (2012) RSeQC: quality control of RNA-seq experiments. Bioinformatics, 28, 2184-2185. https://doi.org/10.1093/bioinformatics/bts356
Wexler, J.R., Plachetzki, D.C. & Kopp, A. (2014) Pan-metazoan phylogeny of the DMRT gene family: A framework for functional studies. Development, Genes and Evolution, 224, 175-181. https://doi.org/10.1007/s00427-014-0473-0
Whittle, C.A. & Extavour, C.G. (2019) Selection shapes turnover and magnitude of sex-biased expression in drosophila gonads. Evolutionary Biology, 19, 60. https://doi.org/10.1186/s12862-019-1377-4
Winston, M. (1987) The biology of the honey bee. Cambridge, MA: Harvard University Press.
Wu, X.B., Wang, Z.L., Gan, H.Y., Li, S.Y. & Zeng, Z.J. (2016) Transcriptome comparison between newly emerged and sexually matured bees of Apis mellifera. Journal of Asia-Pacific Entomology, 19, 893-897. https://doi.org/10.1016/j.aspen.2016.08.002
Xu, P.J., Xiao, J.H., Xia, Q.Y., Murphy, B. & Huang, D.W. (2010) Apis mellifera has two isoforms of cytoplasmic HSP90. Insect Molecular Biology, 19, 593-597. https://doi.org/10.1111/j.1365-2583.2010.01015.x
Zander, E. (1916) Die Ausbildung des Geschlechts bei der Honigbiene (Apis mellifica L.). Zeitschrift für Angewandte Entomologie, 3, 1-74.