Transcriptome analysis of Apis mellifera under benomyl stress to discriminate the gene expression in response to development and immune systems

References

• Rhoades, P. The Importance of Bees in Natural and Agricultural Ecosystems. In National Proceedings: Forest and Conservation Nursery Associations-2012. Proceedings RMRS-P-69; Haase, DL; Pinto, JR; Wilkinson, KM, technical coordinators; Fort Collins, CO: US Department of Agriculture, Forest Service, Rocky Mountain Research Station, 2013; Vol. 69, pp 77–79.
   Google Scholar
• van der Zee, R.; Pisa, L.; Andonov, S.; Brodschneider, R.; Charrière, J.-D.; Chlebo, R.; Coffey, M. F.; Crailsheim, K.; Dahle, B.; Gajda, A.; et al. Managed Honey Bee Colony Losses in Canada, China, Europe, Israel and Turkey, for the Winters of 2008–9 and 2009–10. J. Apic. Res. 2012, 51, 100–114. DOI: 10.3896/IBRA.1.51.1.12.
   Web of Science ®Google Scholar
• Peng, Y. C.; Yang, E. C. Sublethal Dosage of Imidacloprid Reduces the Microglomerular Density of Honey Bee Mushroom Bodies. Sci. Rep. 2016, 6, 19298. DOI: 10.1038/srep19298.
   PubMed Web of Science ®Google Scholar
• Raine, N. E. In the Impacts of Pesticides on Bumblebees: From Individual Behaviour to Colony Function. Presented at the Entomological Society of America Annual Meeting 2014, 2014.
   Google Scholar
• Brandt, A.; Gorenflo, A.; Siede, R.; Meixner, M.; Büchler, R. The Neonicotinoids Thiacloprid, Imidacloprid, and Clothianidin Affect the Immunocompetence of Honey Bees (Apis mellifera L.). J. Insect Physiol. 2016, 86, 40–47. DOI: 10.1016/j.jinsphys.2016.01.001.
   PubMed Web of Science ®Google Scholar
• Reeves, A. M. The Effects of Pesticide Exposures on the Nutritional and Immune Health of the Honey Bee, Apis mellifera L. Doctoral dissertation, Virginia Tech, 2014.
   Google Scholar
• Dai, P. L.; Wang, Q.; Sun, J. H.; Liu, F.; Wang, X.; Wu, Y. Y.; Zhou, T. Effects of Sublethal Concentrations of Bifenthrin and Deltamethrin on Fecundity, Growth, and Development of the Honeybee Apis mellifera Ligustica. Environ. Toxicol. Chem. 2010, 29, 644–649. DOI: 10.1002/etc.67.
   PubMed Web of Science ®Google Scholar
• Gaba, M.; Mohan, C. Development of Drugs Based on Imidazole and Benzimidazole Bioactive Heterocycles: Recent Advances and Future Directions. Med. Chem. Res. 2016, 25, 173–210. DOI: 10.1007/s00044-015-1495-5.
   Web of Science ®Google Scholar
• Guo, Y.; Jiang, Z.; Zhang, M.; Feng, L.; Zhao, J.; Li, J. Determination of Carbendazim and Thiabendazole in Environmental Water by Solid Phase Extraction and High Performance Liquid Chromatography. Chin. J. Anal. Chem. 2005, 33, 395–397.
   Google Scholar
• Goulson, D.; Nicholls, E.; Botías, C.; Rotheray, E. L. Bee Declines Driven by Combined Stress from Parasites, Pesticides, and Lack of Flowers. Science 2015, 347, 1435–1435. DOI: 10.1126/science.1255957.
   Web of Science ®Google Scholar
• Lim, J.; Miller, M. G. The Role of the Benomyl Metabolite Carbendazim in Benomyl-Induced Testicular Toxicity. Toxicol. Appl. Pharmacol. 1997, 142, 401–410. DOI: 10.1006/taap.1996.8042.
   PubMed Web of Science ®Google Scholar
• Kaur, T.; Toor, A. P.; Wanchoo, R. K. Parametric Study on Degradation of Fungicide Carbendazim in Dilute Aqueous Solutions Using Nano TiO2. Desalin. Water Treat. 2015, 54, 122–131. DOI: 10.1080/19443994.2013.879081.
   Web of Science ®Google Scholar
• Li, Y.; Zhou, B.; Qian, M.; Wang, Q.; Zhang, H. Transfer Assessment of Carbendazim Residues from Rape Flowers to Apicultural Products. J. Anal. Method Chem. 2017, 2017, 6075405. [ DOI: 10.1155/2017/6075405.
   Web of Science ®Google Scholar
• Dai, J.; Fan, T.; Shu, R.; Liu, J.; Zhang, Y.; Zhang, L.; Chen, M.; Wei, G. The Residues and Enrichment of the Bactericide Benomyl in Bees and Honey. J. Residuals Sci. Technol. 2017, 14, 27–33.
   Google Scholar
• Nirmala, R.; Nehra, K. Toxic Effect of Insecticides on Survival of Giant Honey Bee (Apis dorsata F.). Ann. Agri Bio Res. 2015, 20, 54–59.
   Google Scholar
• Cizelj, I.; Glavan, G.; Božič, J.; Oven, I.; Mrak, V.; Narat, M. Prochloraz and Coumaphos Induce Different Gene Expression Patterns in Three Developmental Stages of the Carniolan Honey Bee (Apis mellifera Carnica Pollmann). Pestic. Biochem. Physiol. 2016, 128, 68–75. DOI: 10.1016/j.pestbp.2015.09.015.
   PubMed Web of Science ®Google Scholar
• Patel, R. K.; Jain, M. NGS QC Toolkit: A Toolkit for Quality Control of Next Generation Sequencing Data. PLoS One 2012, 7, e30619. DOI: 10.1371/journal.pone.0030619.
   PubMed Web of Science ®Google Scholar
• Langmead, B. Aligning Short Sequencing Reads with Bowtie. Curr. Protoc. Bioinform. 2010, 32, 1–14. DOI: 10.1002/0471250953.bi1107s32.
   Google Scholar
• Mortazavi, A.; Williams, B. A.; McCue, K.; Schaeffer, L.; Wold, B. Mapping and Quantifying Mammalian Transcriptomes by RNA-Seq. Nat. Methods 2008, 5, 621–628. DOI: 10.1038/nmeth.1226.
   PubMed Web of Science ®Google Scholar
• Anders, S.; Huber, W. Differential Expression of RNA-Seq Data at the Gene Level—The DESeq Package. European Molecular Biology Laboratory (EMBL): Heidelberg, Germany, 2012; Vol. 10, p f1000research.
   Google Scholar
• Wirth, T.; Morelli, G.; Kusecek, B.; van Belkum, A.; van der Schee, C.; Meyer, A.; Achtman, M. The Rise and Spread of a New Pathogen: Seroresistant Moraxella catarrhalis. Genome Res. 2007, 17, 1647–1656. DOI: 10.1101/gr.6122607.
   PubMed Web of Science ®Google Scholar
• Carani, F. R.; Duran, B. O. d. S.; Piedade, W. P.; Costa, F. A. A. d.; Val, V. M. F. d. A.; Silva, M. D. P. Expression of Growth-Related Factors in Skeletal Muscle of Pirarucu (Arapaima gigas) during Growth. J. Aquac. Res. Dev. 2014, 5, 1–7.
   Google Scholar
• Li, Z.; Yu, T.; Chen, Y.; Heerman, M.; He, J.; Huang, J.; Nie, H.; Su, S. Brain Transcriptome of Honey Bees (Apis mellifera) Exhibiting Impaired Olfactory Learning Induced by a Sublethal Dose of Imidacloprid. Pestic. Biochem. Physiol. 2019, 156, 36–43. DOI: 10.1016/j.pestbp.2019.02.001.
   PubMed Web of Science ®Google Scholar
• Buttstedt, A.; Moritz, R. F. A.; Erler, S. Origin and Function of the Major Royal Jelly Proteins of the Honeybee (Apis mellifera) as Members of the Yellow Gene Family. Biol. Rev. 2014, 89, 255–269. DOI: 10.1111/brv.12052.
   PubMed Web of Science ®Google Scholar
• Feng, M.; Fang, Y.; Han, B.; Xu, X.; Fan, P.; Hao, Y.; Qi, Y.; Hu, H.; Huo, X.; Meng, L. In-Depth N-Glycosylation Reveals Species-Specific Modifications and Functions of the Royal Jelly Protein from Western (Apis mellifera) and Eastern Honeybees (Apis cerana). J. Proteome Res. 2015, 14, 5327–5340. DOI: 10.1021/acs.jproteome.5b00829.
   PubMed Web of Science ®Google Scholar
• Adamo, S. Why Should an Immune Response Activate the Stress Response? Insights from the Insects (the Cricket Gryllus Texensis). Brain, Behav. Immun. 2010, 24, 194–200. DOI: 10.1016/j.bbi.2009.08.003.
   PubMed Web of Science ®Google Scholar
• Lichtenstein, L.; Grübel, K.; Spaethe, J. Opsin Expression Patterns Coincide with Photoreceptor Development during Pupal Development in the Honey Bee, Apis mellifera. BMC Dev. Biol. 2018, 18, 1–11. DOI: 10.1186/s12861-018-0162-8.
   PubMed Web of Science ®Google Scholar
• Zou, P.; Sun, Y.; Sun, H. B.; Zhu, C. L. Prokaryotic Expression of the Major Antigenic Domain in Opsin from Culex pipiens Pallens and Preparation of Polyclonal Antibodies. J. Pathog. Biol. 2012, 7（05)，15–18.
   Google Scholar
• Wan, X. Research Progress in the Structure and Function of Insect Olfactory Systems. Acta Entomol. Sin. 2015, 58, 688–698.
   Google Scholar
• Twick, I.; Lee, J. A.; Ramaswami, M. Olfactory Habituation in Drosophila-Odor Encoding and Its Plasticity in the Antennal Lobe. Prog. Brain Res. 2014, 208, 3–38.
   PubMed Web of Science ®Google Scholar
• Gurkan, S. Insights into the Defence of Honey Bees, Apis mellifera L. against Insecticides. Doctoral dissertation, University of Liverpool, 2015.
   Google Scholar
• Mackert, A.; do Nascimento, A. M.; Bitondi, M. M. G.; Hartfelder, K.; Simões, Z. L. P. Identification of a Juvenile Hormone Esterase-like Gene in the Honey Bee, Apis mellifera L.—Expression Analysis and Functional Assays. Comp. Biochem. Phys. B 2008, 150, 33–44. DOI: 10.1016/j.cbpb.2008.01.004.
   PubMed Web of Science ®Google Scholar
• Evans, J. D.; Pettis, J. S. Colony-Level Impacts of Immune Responsiveness in Honey Bees, Apis mellifera. Evolution 2005, 59, 2270–2274. DOI: 10.1554/05-060.1.
   PubMed Web of Science ®Google Scholar
• Chan, Q. W.; Melathopoulos, A. P.; Pernal, S. F.; Foster, L. J. The Innate Immune and Systemic Response in Honey Bees to a Bacterial Pathogen, Paenibacillus larvae. BMC Genomics 2009, 10, 387–387. DOI: 10.1186/1471-2164-10-387.
   PubMed Web of Science ®Google Scholar
• Evans, J.; Aronstein, K.; Chen, Y. P.; Hetru, C.; Imler, J. L.; Jiang, H.; Kanost, M.; Thompson, G.; Zou, Z.; Hultmark, D. Immune Pathways and Defence Mechanisms in Honey Bees Apis mellifera. Insect Mol. Biol. 2006, 15, 645–656. DOI: 10.1111/j.1365-2583.2006.00682.x.
   PubMed Web of Science ®Google Scholar
• Patrycja, P.; Rajmund, S. Changes in the Expression of Antimicrobial Peptide Genes in Honey Bees (Apis mellifera) under the Influence of Various Pathogens. Ann. Parasitol. 2020, 66, 457–465.
   PubMedGoogle Scholar
• Wu, Y.; Zheng, Y.; Chen, Y.; Chen, G.; Zheng, H.; Hu, F. Apis cerana Gut Microbiota Contribute to Host Health Though Stimulating Host Immune System and Strengthening Host Resistance to Nosema ceranae. R. Soc. Open Sci. 2020, 7, 192100. DOI: 10.1098/rsos.192100.
   PubMed Web of Science ®Google Scholar
• Ezzati-Tabrizi, R.; Farrokhi, N.; Talaei-Hassanloui, R.; Mehdi Alavi, S.; Hosseininaveh, V. Insect Inducible Antimicrobial Peptides and Their Applications. Curr. Protein Pept. Sci. 2013, 14, 698–710.
   PubMed Web of Science ®Google Scholar
• Zhang, J.; Goyer, C.; Pelletier, Y. Environmental Stresses Induce the Expression of Putative Glycine‐Rich Insect Cuticular Protein Genes in Adult Leptinotarsa decemlineata (Say). Insect Mol. Biol. 2008, 17, 209–216. DOI: 10.1111/j.1365-2583.2008.00796.x.
   PubMed Web of Science ®Google Scholar