Effects of diazinon on olfactory epithelium and genes related to olfactory signal transduction in Caspian roach, Rutilus caspicus

Document Type : Research Paper


1 Department of Fisheries, Faculty of Natural Resources, University of Tehran, Karaj, Iran

2 Aquatic inland waters Research Center, Gorgan, Iran


Olfaction in fishes is biologically-essential chemoreceptors. It provokes important behaviors for the survival of fish such as feeding, reproduction, avoiding predator and intraspecific communication. Pesticides can affect the olfactory epithelium and genes related to olfactory transduction and impair olfactory function.  The present study aims to determine how toxicity of diazinon impacts olfaction of Caspian roach, Rutilus caspicus in histological and gene levels. We exposed fish (0.7 ± 0.05 g in weight) to 0, 1, 2 and 3 mg L-1 diazinon (60 fish in each 3- replicate 60-L glass tank) for 7 days in freshwater. Diazinon concentrations were chosen based on reports on its concentration in surface waters. Mortality rate, histological events of olfactory epithelium, and genes expression at the 7th day after diazinon exposure included a significant decrease in the number of olfactory receptor cells (ORCs), while increased goblet cells (GCs). In addition, G­protein αi (Gpαi) was significantly upregulated, whereas calmodulin-dependent kinase II α (CaMKIIα) was significantly downregulated after 7 days as compared to the control group. These results indicate that diazinon can impair olfactory function through effect on the olfactory epithelium and olfactory signal transduction pathways in the Caspian roach fingerlings.


Bettini, S, Ciani, F & Franceschini, V 2006, Recovery of the olfactory receptor neurons in the African Tilapia mariae following exposure to low copper level. Aquatic Toxicology, 76: 321-328.
Cali, JJ, Zwaagstra, JC, Mons, N, Cooper, DM & Krupinski, J 1994, Type VIII adenylyl cyclase. A Ca2+/calmodulin-stimulated enzyme expressed in discrete regions of rat brain. Journal of Biological Chemistry, 269: 12190-12195.
Choi, EJ, Xia, Z & Storm, DR 1992, Stimulation of the type III olfactory adenylyl cyclase by calcium and calmodulin. Biochemistry, 31: 6492-6498.
Coad, B.W 1980. Environmental change and its impact on the freshwater fishes of Iran. Biological Conservation, 19: 51-80.
DeMaria, S & Ngai, J 2010, The cell biology of smell. Journal of Cell Biology, 19: 443-452.
Elinder, F & ArhemMetal, P 2003. Metal ion effects on ion channel gating. Quarterly Reviews of Biophysics, 36: 373-427.
Hajirezaee, S, Mirvaghe, AR, Farahmand, H & Agh, N 2016, Effects of diazinon on adaptation to sea-water by the endangered Persian sturgeon (Acipenser persicus), fingerlings. Ecotoxicology and Environmental Safety, 133: 413-423.
Hara, TJ 1975, Olfaction in fish. In Progress in Neurobiology, 5: 271-335.
Hedayati, SAA, Jabale, AR & Jahanbakhshi, AR 2016, Determination of LC of Diazinon in silver carp (Hypophthalmicthys molitrix) and Caspian roach (Rutilus rutilus caspicus). Journal of Aquatic Ecology, 6: 138-143.
Holloway, A, Keene, J, Noakes, D & Moccia, R 2004, Effects of clove oil and MS-222 on blood hormone profiles in rainbow trout (Oncorhynchus mykiss) Walbaum. Aquaculture Research, 35: 1025-1030.
Imanpoor, MR & Roohi, Z 2015, Effects of Sangrovit-supplemented diet on growth performance, blood biochemical parameters, survival and stress resistance to salinity in the Caspian roach (Rutilus rutilus) fry. Aquaculture Research, 47: 2874-2880.
Kasumyan, AO 2004, The Olfactory system in fish: Structure, function, and role in behavior. Journal of Ichthyology, 44: 180-223.
Keyvanshokoh, S & Kalbasi, MR 2009, Genetic variation of Caspian Sea roach (Rutilus rutilus caspius) in Iran using RAPD markers. New Genetic, 1: 41-46.
KhosraviKatuli, Kh, MojaziAmiri, B, Massarsky, A & Yelghi, S 2013, Impact of a short-term diazinon exposure on the osmoregulation potentiality of Caspian roach (Rutilus rutilus) fingerlings. MSc. Dissertation at Tehran University, Iran. 140 p.
KhosraviKatuli, Kh, MojaziAmiri, B, Massarsky, A & Yelghi, S 2014, Impact of a short-term diazinon exposure on the osmoregulation potentiality of Caspian roach (Rutilus rutilus) fingerlings. Chemosphere, 108: 396-404.
Kiabi, BH, Abdoli, A & Naderi, M 1999, Status of the fish fauna in the South Caspian basin of Iran. Journal of Zoology in the Middle East, 18: 57-65.
Liu, Z, Tang, R, Li, D, Hu, Q & Wang, Y 2015, Subacute Microcystin-LR Exposure Alters the Metabolism of Thyroid Hormones in Juvenile Zebrafish (Danio Rerio). Toxins, 7: 337-352.
Maryoung, LA, Blunt, B, Tierney, KB & Schlenk, D 2015, Sublethal toxicity of chlorpyrifos to salmonid olfaction after hypersaline acclimation. Aquatic Toxicology, 161: 94-101.
Maryoung, LA, Lavado, R & Schlenk, D 2014, Impacts of hypersaline acclimation on the acute toxicity of the organophosphate chlorpyrifos to salmonids. Aquatic Toxicology, 152: 284-290.
Mojazi Amiri, B, Genbo Xu, E, Kupsco, A, Giroux, M, Hoseinzadeh, M & Schlenk, D 2017, The effect of chlorpyrifos on salinity acclimation of juvenile rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology, 195: 97-102.
Moore, A & Waring, CP 1996, Sublethal effects of the pesticide Diazinon on olfactory function in mature male Atlantic salmon (Salmo salar L.) parr. The Journal of Fish Biology, 48: 758-775.
Moore, A & Waring, CP 1998. Mechanistic effects of a triazine pesticide on reproductive endocrine function in mature male Atlantic salmon (Salmo salar L.) parr. Pesticide Biochemistry and Physiology, 62: 41-50.
Olsen, KH 2011, Effects of Pollutants on Olfactory Mediated Behaviors in Fish and Crustaceans.  In: T, Breithaupt, M, Thiel (Eds.), Chemical Communication in Crustaceans, New York: Springer, pp. 507-529.
Pesce, SF, Cazenave, J, Monferran, VM, Frede, S & Wunderlin, DA 2008, Integrated survey of lindane toxicity on neotropical fish, Corydoras paleatus and Jeninsia mutidentata. Environmental Pollution, 156: 775-783.
Pifferi, S, Menini, A & Kurahashi, T 2010, Signal Transduction in Vertebrate Olfactory Cilia. In: Menini, A., (Ed.), The Neurobiology of Olfaction (Chapter 8). Boca Raton (FL): CRC Press/ Taylor & Francis.
Pourgholam, R, Ghiyasi, M, Rezai, M, Nasrollahzadeh, H & Saiedi, AA Safari, R. et al. 2013, Histopathological studies of some organs of grass carp (Ctenopharyngodon idella) exposed to sublethal concentrations of diazinon. Journal of Mazandaran University of Medical Science, 23: 282-287.
Roberts, R 1989. Fish Pathology. Second ed. Bailliere Tindall, WB Saunders, London, 467 p.
Rospars, JP, Gu, Y, Grémiaux, A & Lucas, Ph 2010, Odor Transduction in Olfactory Receptor Neurons. Chinese Journal of Physiology, 53: 364-372.
Sandahl, JFBaldwin, DHJenkins, JJ & Scholz, NL 2005, Comparative thresholds for acetylcholinesterase inhibition and behavioral impairment in coho salmon exposed to chlorpyrifos. Environmental Toxicology and Chemistry, 24: 136-45.
Saravanan, M, Kumar, PK & Ramesh, M 2011, Haematological and biochemical responses of freshwater teleost, Cyprinus carpio (Actinopterygii: Cypriniformes) during acute and sublethal exposure to lindane. Pesticide Biochemistry and Physiology, 100: 206 – 211.
Schulz, A & Schoneberg, T 2003, The Structural Evolution of a P2Y-like G-protein-coupled Receptor. Journal of Biological Chemistry, 37: 35531–35541.
Shayeghi, M, Shahtaheri, SJ & Selsele, M 2001, Phosphorous insecticides residues in Mazandaran river waters, Iran (2000). Iranian Journal of Public Health, 3: 115-118.
Soleimani, N, Hoseinifar, SH, Merrifield, DL, Barati, M & Abadi, ZH 2012, Dietary supplementation of fructooligosaccharide (FOS) improves the innate immune response, stress resistance, digestive enzyme activities and growth performance of Caspian roach (Rutilus rutilus) fry. Fish and Shellfish Immunology, 32: 316-321.
Taussig, R, Tang, WJ, Hepler, JR & Gilman, AG 1994, Distinct patterns of bidirectional regulation of mammalian adenylyl cyclase. Journal of Biological Chemistry, 269: 6093–6100. 
Tierney, KB, Baldwin, DH, Hara, TJ, Ross, PS, Scholz, NL & Kennedy, CJ 2010, Olfactory toxicity in fishes. Aquatic toxicology, 96: 2-26.
Tilton, FA, Tilton, SC, Bammler, TK, Beyer, RP, Stapleton, PL, Scholz, NL & Gallagher, EP 2011, Transcriptional impact of organophosphate and metal mixtures on olfaction: Copper dominates the chlorpyrifos-induced response in adult zebrafish. Aquatic Toxicology, 102: 205-215.
Ueda, H, Nakamura, Sh, Nakamura, T, Inada, K, Okubo, T, Furukawa, N, Murakami, R, et al. 2016, Involvement of hormones in olfactory imprinting and homing in chum salmon. Scientific reports, 6: 1-11.
Waring, CP &Moore, A 1997, Sublethal effects of a carbomate pesticide on pheromonal mediated endocrine function in mature Atlantic salmon (Salmo salar) parr. Fish Physiology and Biochemistry, 17: 203-211.
William, ChR & Gallagher, EP 2013, Effects of cadmium on olfactory mediated behaviors and molecular biomarkers in coho salmon (Oncorhynchus kisutch). Aquatic Toxicology, 15: 295-302.
Wolf, MC & Moore, PA 2002, The effects of the herbicide metolachlor on the perception of chemical stimuli by Orconectes rusticus. Journal of the North American Benthological Society, 21: 457–467.