CASTE DEVELOPMENT IN HYMENOPTERA, A MOLECULAR VIEW FOR FARMING IMPROVEMENT OF STINGLESS BEES

D.M. Moreno-Cálix, F. Guillén-Chable, M.A. Gallardo Flores, K.J. Cantarero, L.C. Rodríguez-Zapata, Enrique Castano

Abstract


Background: The evolution and genetic elements for the development of the caste is an enigma in Hymenoptera, as well as the total impact that the genetic elements given in the food of the larvae have on the development of bees. During the last decades, micro RNAs (miRNAs) from nurse bee secretions in larval food have been found to constitute an additional element in the regulatory control of caste determination. Furthermore, social differentiation is a complex developmental process influenced by genetic, epigenetic, and environmental factors. Objective: To examine and summarize miRNAs as a regulatory component of larval food with an effect on caste development in eusocial hymenoptera. Methodology. The sequences of miRNAs expressed in eusocial bees were obtained from miRBase.org. MUSCLE V.3 enabled alignment and correction was carried out using Fast.Dist. The TreeDyn software was used to obtain the phylogenetic trees. Results: The role of diet and the relationship with microRNAs in caste differentiation and regulation may be part of a general mechanism that involves selective plant genetic information necessary for insect development. Implications: The in vitro cultivation of stingless bees is a practice that is already carried out in some species of commercial importance; However, studies that demonstrate how development, differentiation and regulation of gene expression would be shaping the differentiation of different castes are still gaps that must begin to be addressed. In vitro breeding would require the study of environmental and molecular variables that would modulate the expression of the castes. Conclusion: The biogenesis, regulation and functions of microRNA in Eukarya are still obscure, however, some light has been shed on the molecular basis of caste differentiation in eusocial bees modulated by 2 miRN transfer pathways; endogenous and exogenous.

Keywords


eusociality; caste determination; microRNA; epigenetic regulation.

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References


Ashby, R., Forêt, S., Searle, I. and Maleszka, R., 2016. MicroRNAs in Honey Bee Caste Determination. Scientific Reports, 6, p. 18794. https://doi.org/10.1038/srep18794

Barchuk, A.R., Cristino, A.S., Kucharski, R., Costa, L.F., Simões, Z.L.P. and Maleszka, R., 2007. Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Developmental Biology, 7, p. 70. https://doi.org/10.1186/1471-213X-7-70

Bonasio, R., Zhang, G., Ye, C., Mutti, N.S., Fang, X., Qin, N., Donahue, G., Yang, P., Li, Q., Li, C., Zhang, P., Huang, Z., Berger, S.L., Reinberg, D., Wang, J. and Liebig, J., 2010. Genomic Comparison of the Ants Camponotus floridanus and Harpegnathos saltator. Science, 329, pp. 1068–1071. https://doi.org/10.1126/science.1192428

Buttstedt, A., Ihling, C.H., Pietzsch, M. and Moritz, R.F.A., 2016. Royalactin is not a royal making of a queen. Nature, 537, p. E10–E12. https://doi.org/10.1038/nature19349

Collins, D.H., Mohorianu, I., Beckers, M., Moulton, V., Dalmay, T. and Bourke, A.F.G., 2017. MicroRNAs Associated with Caste Determination and Differentiation in a Primitively Eusocial Insect. Scientific Reports, 7, p 45674. https://doi.org/10.1038/srep45674

Cridge, A., Leask, M., Duncan, E. and Dearden, P., 2015. What do studies of insect polyphenisms tell Us about nutritionally-triggered epigenomic changes and their consequences? Nutrients, 7, pp. 1787–1797. https://doi.org/10.3390/nu7031787

Denli, A.M., Tops, B.B.J., Plasterk, R.H.A., Ketting, R.F. and Hannon, G.J., 2004. Processing of primary microRNAs by the Microprocessor complex. Nature, 432, pp. 231–235. https://doi.org/10.1038/nature03049

Djuranovic, S., Nahvi, A. and Green, R., 2011. A Parsimonious Model for Gene Regulation by miRNAs. Science, 331, pp. 550–553. https://doi.org/10.1126/science.1191138

Greenberg, J.K., Xia, J., Zhou, X., Thatcher, S.R., Gu, X., Ament, S.A., Newman, T.C., Green, P.J., Zhang, W., Robinson, G.E. and Ben-Shahar, Y., 2012. Behavioral plasticity in honey bees is associated with differences in brain microRNA transcriptome. Genes, Brain and Behavior, 11, pp. 660–670. https://doi.org/10.1111/j.1601-183X.2012.00782.x

Gregory, R.I., Yan, K., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N. and Shiekhattar, R., 2004. The Microprocessor complex mediates the genesis of microRNAs. Nature, 432, pp. 235–240. https://doi.org/10.1038/nature03120

Gu, L. and Knipple, D.C., 2013. Recent advances in RNA interference research in insects: Implications for future insect pest management strategies. Crop Protection, 45, pp. 36–40. https://doi.org/https://doi.org/10.1016/j.cropro.2012.10.004

György, H., Juanita, M., E, P.A., Éva, B. and Thomas, T., D, Z.P., 2001. A cellular function for the RNA-interference enzyme dicer in the maturation of the let-7 small temporal RNA. Science, 293, pp. 834–838. https://doi.org/10.1126/science.1062961

Hartfelder, K., Cnaani, J. and Hefetz, A., 2000. Caste-specific differences in ecdysteroid titers in early larval stages of the bumblebee Bombus terrestris. Journal of Insect Physiology, 46, pp. 1433–1439. https://doi.org/10.1016/S0022-1910(00)00067-6

Heimberg, A.M., Sempere, L.F., Moy, V.N., Donoghue, P.C.J. and Peterson, K.J., 2008. MicroRNAs and the advent of vertebrate morphological complexity. Proceedings of the National Academy of Sciences, 105, pp. 2946–2950. https://doi.org/10.1073/pnas.0712259105

Hughes, W.O.H., Sumner, S., van Borm, S. and Boomsma, J.J., 2003. Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proceedings of the National Academy of Sciences 100, pp. 9394–9397. https://doi.org/10.1073/pnas.1633701100

Huntzinger, E. and Izaurralde, E., 2011. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nature Reviews Genetics, 12, pp. 99–110. https://doi.org/10.1038/nrg2936

Hutvagner, G. and Simard, M.J., 2008. Argonaute proteins: Key players in RNA silencing. Nature Reviews Molecular Cell Biology, 9, pp. 22–32. https://doi.org/10.1038/nrm2321

Kerr, W.E., 1950. Genetic determination of castes in the genus melipona. Genetics, 35, pp. 143–152. https://doi.org/10.1093/genetics/35.2.143

Ketting, R.F., Fischer, S.E.J., Bernstein, E., Sijen, T., Hannon, G.J. and Plasterk, R.H.A., 2001. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes & Development, 15, pp. 2654–2659. https://doi.org/10.1101/gad.927801

Ledda, B., Ottaggio, L., Izzotti, A., Sukkar, S.G. and Miele, M., 2020. Small RNAs in eucaryotes: New clues for amplifying microRNA benefits. Cell & Bioscience, 10, p. 1. https://doi.org/10.1186/s13578-019-0370-3

Lee, Y., Jeon, K., Lee, J.-T., Kim, S. and Kim, V.N., 2002. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J, 21, pp. 4663–4670. https://doi.org/10.1093/emboj/cdf476

Lee, Y., Kim, M., Han, J., Yeom, K.-H., Lee, S., Baek, S.H. and Kim, V.N., 2004. MicroRNA genes are transcribed by RNA polymerase II. The EMBO Journal, 23, pp. 4051–4060. https://doi.org/https://doi.org/10.1038/sj.emboj.7600385

Lisboa, L.C.O., Serrão, J.E., Cruz-Landim, C. and Campos, L.A.O., 2005. Effect of larval food amount on ovariole development in queens of Trigona spinipes (Hymenoptera, Apinae). Anatomia, Histologia, Embryologia, 34, pp. 179–184. https://doi.org/https://doi.org/10.1111/j.1439-0264.2005.00591.x

Lu, C.-Y., Weng, Y.-T., Tan, B. and Hsu, C.-Y., 2021. The trophocytes and oenocytes of worker and queen honey bees (Apis mellifera) exhibit distinct age-associated transcriptome profiles. Geroscience, 43, pp. 1863–1875. https://doi.org/10.1007/s11357-021-00360-y

Lucas, K. and Raikhel, A.S., 2013a. Insect microRNAs: biogenesis, expression profiling and biological functions. Insect Biochem Mol Biol, 43, pp. 24–38. https://doi.org/10.1016/j.ibmb.2012.10.009

Lucas, K. and Raikhel, A.S., 2013b. Insect microRNAs: biogenesis, expression profiling and biological functions. Insect Biochem Mol Biol,43, pp.24–38. https://doi.org/10.1016/j.ibmb.2012.10.009

Mao, W., Schuler, M.A. and Berenbaum, M.R., 2015. A dietary phytochemical alters caste-associated gene expression in honey bees. Science Advances, 1, p. e1500795. https://doi.org/10.1126/sciadv.1500795

Madeira, F., Pearce, M., Tivey, A.R.N., Basutkar, P., Lee, J., Edbali, O., Madhusoodanan, N., Kolesnikov, A. and Lopez, R., 2022. Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Research, 50(W1), W276-W279. http://doi.org/10.1093/nar/gkac240

Michener, C.D., 2007. The bees of the world, 2nd ed. ed. Johns Hopkins University Press, Baltimore.

Michener, C.D., 1974. The social behavior of the bees: a comparative study. Belknap Press of Harvard University Press, Cambridge, Mass.

Mohr, A.M. and Mott, J.L., 2015. Overview of microRNA biology. Semin Liver Dis, 35, pp. 3–11. https://doi.org/10.1055/s-0034-1397344

O’Brien, J., Hayder, H., Zayed, Y. and Peng, C., 2018. Overview of microrna biogenesis, mechanisms of actions, and circulation. Frontiers in Endocrinology, 9, p. 402. https://doi.org/10.3389/fendo.2018.00402

Palandri, A., L’hôte, D., Cohen-Tannoudji, J., Tricoire, H. and Monnier, V., 2015. Frataxin inactivation leads to steroid deficiency in flies and human ovarian cells. Human Molecular Genetics, 24, pp. 2615–2626. https://doi.org/10.1093/hmg/ddv024

Perkins, D.O., Jeffries, C.D., Jarskog, L.F., Thomson, J.M., Woods, K., Newman, M.A., Parker, J.S., Jin, J. and Hammond, S.M., 2007. microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biology,8, p. R27. https://doi.org/10.1186/gb-2007-8-2-r27

Quezada-Euán, J.J.G., 2018. Stingless Bees of Mexico: The biology, management and conservation of an ancient heritage. Springer International Publishing, Cham.

Rachinsky, A., Strambi, C., Strambi, A. and Hartfelder, K., 1990. Caste and metamorphosis: Hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae. General and Comparative Endocrinology, 79, pp. 31–38. https://doi.org/10.1016/0016-6480(90)90085-Z

Rodriguez, A., Griffiths-Jones, S., Ashurst, J.L. and Bradley, A., 2004. Identification of mammalian microRNA host genes and transcription units. Genome Research, 14, pp. 1902–1910. https://doi.org/10.1101/gr.2722704

Santhekadur, P.K. and Kumar, D.P., 2019. RISC assembly and post-transcriptional gene regulation in Hepatocellular Carcinoma. Genes Dis, 7, pp. 199–204. https://doi.org/10.1016/j.gendis.2019.09.009

Schanen, B.C. and Li, X., 2011. Transcriptional regulation of mammalian miRNA genes. Genomics, 97, pp. 1–6. https://doi.org/https://doi.org/10.1016/j.ygeno.2010.10.005

Smith, C.R., Anderson, K.E., Tillberg, C.V., Gadau, J. and Suarez, A.V., 2008. Caste determination in a polymorphic social insect: Nutritional, social, and genetic factors. The American Naturalist, 172, pp. 497–507. https://doi.org/10.1086/590961

Smith, C.R. and Suarez, A.V, 2010. The trophic ecology of castes in harvester ant colonies. Functional Ecology, 24, pp. 122–130. https://www.jstor.org/stable/40407771

Solenn, P., Anna, V., Chris, W., Philip, E., Francisco, C., G, F.P., L, A.C., P, J.T., Anne, S.-P., Martin, B., Irene, G.-N., E, M.A., Felix, K., Ernesto, L., Marina, M.-H., Luis, R.-A.J., S, N.F., Shankar, B., Toni, G., E, T.J., Simon, A., Heinz, H., H, H.W.O., Roderic, G., Wolf, R. and Seirian, S., 2015. Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies. Proceedings of the National Academy of Sciences, 112, pp. 13970–13975. https://doi.org/10.1073/pnas.1515937112

Søvik, E., Bloch, G. and Ben-Shahar, Y., 2015. Function and evolution of microRNAs in eusocial Hymenoptera. Frontiers in Genetics, 6, p. 193. https://doi.org/10.3389/fgene.2015.00193

Sumner, S., Bell, E. and Taylor, D., 2018. A molecular concept of caste in insect societies. Current Opinion in Insect Science,25, pp. 42–50. https://doi.org/10.1016/j.cois.2017.11.010

Sumner, S., Pereboom, J.J.M. and Jordan, W.C., 2006. Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis. Proceedings of the Royal Society B: Biological Sciences, 273, pp. 19–26. https://doi.org/10.1098/rspb.2005.3291

Tomoyasu, Y., Miller, S.C., Tomita, S., Schoppmeier, M., Grossmann, D. and Bucher, G., 2008. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biology,9, p. R10. https://doi.org/10.1186/gb-2008-9-1-r10

Villagra, C. and Frías-Lasserre, D., 2020. Epigenetic molecular mechanisms in insects. Neotropical Entomology, 49, pp. 615–642. https://doi.org/10.1007/s13744-020-00777-8

W, K.S., L, B.B., 2001. A role for the RNase III Enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science, 293, pp. 2269–2271. https://doi.org/10.1126/science.1062039

Wei, H., He, X.J., Liao, C.H., Wu, X.B., Jiang, W.J., Zhang, B., Zhou, L. bin, Zhang, L.Z., Barron, A.B. and Zeng, Z.J., 2019. A Maternal Effect on Queen Production in Honeybees. Current Biology, 29, pp. 2208-2213.e3. https://doi.org/https://doi.org/10.1016/j.cub.2019.05.059

Yan, H., Simola, D.F., Bonasio, R., Liebig, J., Berger, S.L. and Reinberg, D., 2014. Eusocial insects as emerging models for behavioural epigenetics. Nature Reviews Genetics, 15, pp. 677–688. https://doi.org/10.1038/nrg3787

Ylla, G., Fromm, B., Piulachs, M.-D. and Belles, X., 2016. The microRNA toolkit of insects. Scientific Reports, 6, p. 37736. https://doi.org/10.1038/srep37736

Zhu, K., Liu, M., Fu, Z., Zhou, Z., Kong, Y., Liang, H., Lin, Z., Luo, J., Zheng, H., Wan, P., Zhang, J., Zen, K., Chen, J., Hu, F., Zhang, C.-Y., Ren, J. and Chen, X., 2017. Plant microRNAs in larval food regulate honeybee caste development. PLOS Genetics, 13, p. e1006946. https://doi.org/10.1371/journal.pgen.1006946




URN: http://www.revista.ccba.uady.mx/urn:ISSN:1870-0462-tsaes.v27i3.52143

DOI: http://dx.doi.org/10.56369/tsaes.5214

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