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Meriç Delta Balıklarında Çevre Kirliliğinin Genotoksik Etkileri: Antioksidan Savunma, Isı Şok Protein Sinyali ve DNA Hasar-Onarım Mekanizmaları

Year 2020, Volume: 6 Issue: 1, 14 - 24, 25.04.2020
https://doi.org/10.17216/limnofish.516094

Abstract

Çalışmamızda, Gala ve Sığırcı Gölleri için ekonomik açıdan önemli olan balık türleri (Carassius gibelio (Bloch, 1782), Carassius carassius (Linnaeus, 1758), Scardinius erythrophthalmus (Linnaeus, 1758), Cyprinus carpio Linnaeus, 1758, Sander lucioperca (Linnaeus, 1758), Perca fluviatilis Linnaeus, 1758) üzerinde kirliliğin etkileri araştırılmıştır. Kirliliğin genotoksik etkileri, kas, solungaç ve karaciğer dokularında antioksidan savunma sinyali (GS, Cu-Zn SOD, CAT), ısı şok proteinleri (HSP26, HSP60, HSP70 ve HSP83) ve QRT-PCR testi ile DNA onarımı (SMUG1) metotları kullanılarak incelenmiştir. Ayrıca, RAPD analizi kullanılarak balık dokularındaki DNA hasarları belirlenmiştir. Bant değişimleri, özellikle tüm balıkların solungaç dokularında açıkça tespit edilmiştir. Ayrıca, C. gibellio, S. erythrophthalmus ve S. lucioperca'nın kas dokusunda CuZn-SOD'un nispi ekspresyonunda önemli bir artış gösterdiği tespit edilmiştir. CAT ekspresyonu tüm balık dokularında önemli ölçüde değişiklik sergilemiştir. Bununla birlikte, CAT 128,9, 102,1 ve 138,4 fg/ug total RNA'nın ekspresyon seviyesindeki en yüksek artış, S. lucioperca'nın kas, karaciğer ve solungaç dokularında belirlenmiştir. HSP60 ve HSP70 çevre kirliliğinden en az etkilenirken, S. lucioperca'nın karaciğer dokusunda en büyük DNA onarım aktivitesi açık şekilde gözlenmiştir. Çalışmamızın sonucunda, Gala ve Sığırcı Göllerindeki çevre kirliliğinin DNA stabilitesi ve savunma sinyallerinin gen ifadeleri üzerinde genotoksik etkileri olduğu ortaya konulmuştur. Ayrıca, S. lucioperca türünün, su kirliliğinin biyolojik olarak izlenmesinde biyoindikatör bir tür olarak kullanılabileceği sonucuna varılmıştır.

Thanks

Bu araştırma, Trakya Üniversitesi Bilimsel Araştırma Projeleri Birimi (TÜBAP 2016/86) tarafından finansal olarak desteklenmiştir.

References

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  • Atienzar FA, Conradi M, Evenden AJ, Jha AN, Depledge MH. 1999. Qualitative assessment of genotoxicity using random amplified polymorphic DNA, comparison of genomic template stability with key fitness parameters in Daphnia magna exposed to benzo[a]pyrene. Society Environmental Toxicology and Chemistry. 18(10):2275–2282. doi: 10.1002/etc.5620181023
  • Ayas Z. 2007. Review on DDT and its residues in Turkey’s wetlands. J Environ Biol. 28(4):707-715.
  • Batki H, Kucuksezgin F, Uslu O. 1999. Trace metal distribution in different chemical fractions of marine sediments along the eastern Aegean shelf. Toxıcol Envıron Chem. 70(1-2):243-258. doi: 10.1080/02772249909358752
  • Bourg EL. 2001. Oxidative stress, aging and longevity in Drosophila melanogaster. FEBS Letters 498(2-3):183-186. doi: 10.1016/S0014-5793(01)02457-7
  • Cenkci S, Yildiz M, Cigerci IH, Bozdag A, Terzi ESA. 2010. Evaluation of 2,4-D and Dicamba genotoxicity in bean seedlings using comet and RAPD assays. Ecotox Environ Safe. 73(7):1558-1564. doi: 10.1016/j.ecoenv.2010.07.033
  • Chang HC, Tang YC, Hayer-Hartl M, Hartl UC. 2007. SnapShot: molecular chaperones, Part I. Cell 128(1):-212.el-212.e2. doi: 10.1016/j.cell.2007.01.001
  • Conte C, Mutti I, Puglisi P, Ferrarini A, Regina G, Maestri E. 1998. DNA fingerprinting analysis by a PCR based method for monitoring the genotoxic effects of heavy metals pollution. Chemosphere. 37(14-15):2739-2749. doi: 10.1016/S0045-6535(98)00317-8
  • Doğanlar ZB. 2012. Physiological and genetic responses to pesticide mixture treatment of Veronica beccabunga. Water Air Soil Poll . 223(9):6201-6212. doi: 10.1007/s11270-012-1350-y
  • Doğanlar ZB, Doğanlar O, Tabakçıoğlu K. 2014. Genotoxic effects of heavy metal mixture in Drosophila melanogaster: expressions of heat shock proteins, RAPD profiles and mitochondrial DNA sequence. Water Air Soil Poll. 225:2104. doi: 10.1007/s11270-014-2104-9
  • Doğanlar O, Doğanlar ZB. 2015. Effects of a mixture of volatile organic compounds on total DNA and gene expression of heat shock proteins in Drosophila melanogaster. Arch Environ Con Tox. 68(2):395-404. doi: 10.1007/s00244-014-0089-4
  • Doğanlar ZB, Doğanlar O, Tozkir H, Gökalp FD, Doğan A, Yamaç F. Aktaş ÜE. 2018. Nonoccupational exposure of agricultural area residents to Pesticides: Pesticide accumulation and evaluation of genotoxicity. Arch Environ Con Tox. 75(4):530-544. doi: 10.1007/s00244-018-0545-7
  • Dökmeci AH. 2005. Gala Gölü ve gölü besleyen su kaynaklarında ağır metal kirliliğinin araştırılması. [Yüksek lisans tezi]. Trakya Üniversitesi. 112 s.
  • Duthie GG, Wahle KWJ, James WPT. 1989. Oxidants, antioxidants and cardiovascular disease. Nutr Res Rev. 2(1):51-62. doi: 10.1079/NRR19890007
  • Economos AC, Ballard RC, Miquel J, Binnard R, Philpott DE. 1982. Accelerated aging of fasted Drosophila. Preservation of physiological function and cellular fine structure by thiazolidine carboxylic acid (TCA). Exp Gerontol. 17(2):105-114. doi: 10.1016/0531-5565(82)90043-2
  • Elipek BÇ, Arslan N, Kirgiz T, Öterler B, Güher H, Özkan N. 2010. Analysis of Benthic Macroinvertebrates in Relation to Environmental Variables of Lake Gala, a National Park of Turkey. Turk J Fish Aquat Sc. 10:235-243. doi: 10.4194/trjfas.2010.0212
  • Ergin M, Yemenicioglu S. 1997. Geologic assessment of environmental impact in bottom sediments of the eastern Aegean sea. Int J Environ Stud. 51(4):323-334. doi: 10.1080/00207239708711090
  • Erkmen B, Kolankaya D. 2006. Determination of organochlorine pesticide residues in water, sediment, and fish samples from the Meriç Delta, Turkey. Int J Environ An Ch. 86(1-2):161-169. doi: 10.1080/03067310500247926
  • Güçlü H, Doganlar ZB, Gürlü VP, Özal A, Dogan A, Turhan MA, Doganlar O. 2018. Effects of cisplatin-5-fluorouracil combination therapy on oxidative stress, DNA damage, mitochondrial apoptosis, and death receptor signalling in retinal pigment epithelium cells. Cutan Ocul Toxicol. 37(3):291-304. doi: 10.1080/15569527.2018.1456548
  • Güher H, Erdoğan S, Kırgız T, Elipek BÇ. 2011. The Dynamics of Zooplankton in National Park of Lake Gala (Edirne-Turkey). Acta Zool Bulgar. 63(2):157-168.
  • Haap T, Triebskorn R, Kohler HR. 2008. Acute effects of diclofenac and DMSO to Daphnia magna: immobilization and Hsp70 induction. Chemosphere. 73(3):353-359. doi: 10.1016/j.chemosphere.2008.05.062
  • Kohler HR, Alberti G, Seniezak A. 2005. Lead induced hsp70 and hsp60 pattern transformation and leg malformation during postembryonic development in orbadit mite Archegozetes longisetosus Aoki. Comp Biochem Phys C. 141(4):398-405. doi: 10.1016/j.cbpc.2005.09.003
  • Liu W, Li PJ, Qi XM, Zhou QX, Zheng L, Sun TH, Yang YS. 2005. DNA changes in barley (Hordeum vulgare) seedlings induced by cadmium pollution using RAPD analysis. Chemosphere. 61(2):158-167. doi: 10.1016/j.chemosphere.2005.02.078
  • Macario AJL, Macario CE. 2005. Sick chaperones, cellular stress, and disease. New Engl J Med. 353:1489-1501. doi: 10.1056/NEJMra050111
  • Massie HR. 1988. Chemicals. In: Lints FA, Soliman MH, editors. Drosophila as a Model Organism for Ageing Studies. Glasgow: Blackie. p. 59-70.
  • Park WJ, Kriechbaumer V, Müller A, Piotrowski M, Meeley RB, Gierl A, Glawischnig E. 2003. The nitrilase ZmNIT2 converts indole-3-acetonitrile to indole-3-acetic acid. Plant Physiol, 133(2):794-802. doi: 10.1104/pp.103.026609
  • Posgai R, Caitlin B, McCulloch C, Murphy KR, Hussain SM, Rowe JJ, Nielsen MG. 2011. Differential toxicity of silver and titanium dioxide nanoparticles on Drosophila melanogaster development, reproductive effort, and viability: Size, coatings and antioxidants matter. Chemosphere. 85(1):34-42. doi: 10.1016/j.chemosphere.2011.06.040
  • Reveillaud I, Niedzwiecki A, Bensch KG, Fleming JE. 1991. Expression of bovine superoxide dismutase in Drosophila melanogaster augments resistance to oxidative stress. Mol Cell Biol. 11(2):632-640. doi: 10.1128/MCB.11.2.632
  • Ruddle DL, Yengoyan LS, Miquel J, Marcuson R, Fleing JE. 1988. Propyl gallate delays senecence in Drosophila melanogaster. Age; 11(2):54-58. doi: 10.1007/BF02431773
  • Singh MP, Ravi R, Mishraa M, Shrivastavac M, Saxenaa DK. 2010. Kar Chowdhuri D. Effects of co-exposure of benzene, toluene and xylene to Drosophila melanogaster: Alteration in hsp70, hsp60, hsp83, hsp26, ROS generation and oxidative stress markers. Chemosphere. 79(5):577-587. doi: 10.1016/j.chemosphere.2010.01.054
  • Staveley BE, Phillips JP, Hilliker AJ. 1990. Phenotipic consequences of copper-zinc superoxide dismutase overexpression in Drosophila melanogaster. Genome. 33(6):867-872. doi: 10.1139/g90-130
  • Sun J, Tower J. 1999. Flp recombinase-mediated induction of Cu/Zn-superoxide dismutase transgene expression can extend the life span of adult Drosophila melanogaster flies. Mol Cell Biol. 19(1):216-228. doi: 10.1128/MCB.19.1.216
  • Tang YC, Chang HC, Hayer-Hartl M, Hartl FU. 2007 SnapShot: molecular chaperones, part II. Cell. 128(2):412. doi: 10.1016/j.cell.2007.01.013
  • Tokatlı C. 2017. Bioecological and statistical risk assessment of toxic metals in sediments of a worldwide important wetland: Gala Lake National Park (Turkey). Arch Environ Prot. 43(1): 34-47. doi: 10.1515/aep-2017-0007
  • Tokatlı C. 2018. Essential and toxic element bioaccumulations in fishes of Gala and Siğirci Lakes (Meriç River Delta, Turkey). Acta Alimentaria. 47(4):470-478. doi: 10.1556/066.2018.47.4.10
  • Tokatlı C, Baştatlı Y. 2016. Trace and Toxic Element Levels in River Sediments. Pol J Environ Stud. 25(4):1715-1720. doi: 10.15244/pjoes/62678
  • Tokatlı C, Köse E, Uğurluoğlu A, Çiçek A, Emiroğlu Ö. 2014. Gala Gölü (Edirne) Su Kalitesinin Coğrafi Bilgi Sistemi (CBS) Kullanılarak Değerlendirilmesi. Sigma Journal of Engineering and Natural Sciences. 32(4):490-501.
  • Tokatlı C, Emiroğlu Ö, Çiçek A, Köse E, Başkurt S, Aksu S, Uğurluoğlu A, Şahin M, Baştatlı Y. 2016. Investigation of Toxic Metal Bioaccumulations in Fishes of Meriç River Delta (Edirne). Anadolu University Journal of Science and Technology C - Life Sciences and Biotechnology. 5(1):1-11. doi: 10.18036/btdc.32213
  • Yarar M, Magnin G. 1997. Türkiye’nin önemli kuş alanları. İstanbul: Doğal Hayatı Koruma Derneği 313 s.
  • Yılmaz GB. 2004. Gala gölü ve çevresinde ağır metal derişiminin dinamiği. [Yüksek lisans tezi], Trakya Üniversitesi. 59 s.

Genotoxic Effects of Environmental Pollution in Meriç Delta Fish: Expressions of Antioxidant Defence Signals, Heat Shock Proteins and DNA Damage-Repair Mechanisms

Year 2020, Volume: 6 Issue: 1, 14 - 24, 25.04.2020
https://doi.org/10.17216/limnofish.516094

Abstract

In this study, the effects of pollution on economically important fish species for Gala and Sığırcı Lakes [Carassius gibelio (Bloch, 1782), Carassius carassius (Linnaeus, 1758), Scardinius erythrophthalmus (Linnaeus, 1758), Cyprinus carpio Linnaeus, 1758, Sander lucioperca (Linnaeus, 1758), Perca fluviatilis Linnaeus, 1758)] were investigated. The genotoxic effects of environmental pollution were investigated with reference to gene expressions of antioxidant defense signal (GS, Cu-Zn SOD, CAT), heat shock proteins (HSP26, HSP60, HSP70 and HSP83) and DNA repair (SMUG1) by qRT-PCR assay in muscle, liver and gill tissue of fish species. Additionally, DNA damage determined using RAPD assay. Band changes were clearly detected, especially in the gill tissues of all fishes. In addition, a significant increase in the relative expression of CuZn-SOD in muscle tissue of C. gibellio, S. erythrophthalmus and S. lucioperca. The expression of CAT changed significantly at all tissue of fishes. However, the highest increase in expression level of CAT 128.9, 102.1 and 138.4 fg/µg total RNA was determined in muscle, liver and gill tissues of S. lucioperca. While the HSP60 and HSP70 was the least affected by environmental pollutions, greatest DNA repair activity was clearly observed in liver tissue of S. lucioperca. We conclude that environmental pollution in Gala and Sığırcı Lake exert genotoxic effects on DNA stability, and gen expressions of defense signaling. Additionally, S. lucioperca may be a bio-indicator species for biomonitoring to water pollution.

References

  • Anonim 2005. Edirne İl Çevre Durum Raporu. Edirne Valiliği İl Çevre Ve Orman Müdürlüğü.
  • Atienzar FA, Conradi M, Evenden AJ, Jha AN, Depledge MH. 1999. Qualitative assessment of genotoxicity using random amplified polymorphic DNA, comparison of genomic template stability with key fitness parameters in Daphnia magna exposed to benzo[a]pyrene. Society Environmental Toxicology and Chemistry. 18(10):2275–2282. doi: 10.1002/etc.5620181023
  • Ayas Z. 2007. Review on DDT and its residues in Turkey’s wetlands. J Environ Biol. 28(4):707-715.
  • Batki H, Kucuksezgin F, Uslu O. 1999. Trace metal distribution in different chemical fractions of marine sediments along the eastern Aegean shelf. Toxıcol Envıron Chem. 70(1-2):243-258. doi: 10.1080/02772249909358752
  • Bourg EL. 2001. Oxidative stress, aging and longevity in Drosophila melanogaster. FEBS Letters 498(2-3):183-186. doi: 10.1016/S0014-5793(01)02457-7
  • Cenkci S, Yildiz M, Cigerci IH, Bozdag A, Terzi ESA. 2010. Evaluation of 2,4-D and Dicamba genotoxicity in bean seedlings using comet and RAPD assays. Ecotox Environ Safe. 73(7):1558-1564. doi: 10.1016/j.ecoenv.2010.07.033
  • Chang HC, Tang YC, Hayer-Hartl M, Hartl UC. 2007. SnapShot: molecular chaperones, Part I. Cell 128(1):-212.el-212.e2. doi: 10.1016/j.cell.2007.01.001
  • Conte C, Mutti I, Puglisi P, Ferrarini A, Regina G, Maestri E. 1998. DNA fingerprinting analysis by a PCR based method for monitoring the genotoxic effects of heavy metals pollution. Chemosphere. 37(14-15):2739-2749. doi: 10.1016/S0045-6535(98)00317-8
  • Doğanlar ZB. 2012. Physiological and genetic responses to pesticide mixture treatment of Veronica beccabunga. Water Air Soil Poll . 223(9):6201-6212. doi: 10.1007/s11270-012-1350-y
  • Doğanlar ZB, Doğanlar O, Tabakçıoğlu K. 2014. Genotoxic effects of heavy metal mixture in Drosophila melanogaster: expressions of heat shock proteins, RAPD profiles and mitochondrial DNA sequence. Water Air Soil Poll. 225:2104. doi: 10.1007/s11270-014-2104-9
  • Doğanlar O, Doğanlar ZB. 2015. Effects of a mixture of volatile organic compounds on total DNA and gene expression of heat shock proteins in Drosophila melanogaster. Arch Environ Con Tox. 68(2):395-404. doi: 10.1007/s00244-014-0089-4
  • Doğanlar ZB, Doğanlar O, Tozkir H, Gökalp FD, Doğan A, Yamaç F. Aktaş ÜE. 2018. Nonoccupational exposure of agricultural area residents to Pesticides: Pesticide accumulation and evaluation of genotoxicity. Arch Environ Con Tox. 75(4):530-544. doi: 10.1007/s00244-018-0545-7
  • Dökmeci AH. 2005. Gala Gölü ve gölü besleyen su kaynaklarında ağır metal kirliliğinin araştırılması. [Yüksek lisans tezi]. Trakya Üniversitesi. 112 s.
  • Duthie GG, Wahle KWJ, James WPT. 1989. Oxidants, antioxidants and cardiovascular disease. Nutr Res Rev. 2(1):51-62. doi: 10.1079/NRR19890007
  • Economos AC, Ballard RC, Miquel J, Binnard R, Philpott DE. 1982. Accelerated aging of fasted Drosophila. Preservation of physiological function and cellular fine structure by thiazolidine carboxylic acid (TCA). Exp Gerontol. 17(2):105-114. doi: 10.1016/0531-5565(82)90043-2
  • Elipek BÇ, Arslan N, Kirgiz T, Öterler B, Güher H, Özkan N. 2010. Analysis of Benthic Macroinvertebrates in Relation to Environmental Variables of Lake Gala, a National Park of Turkey. Turk J Fish Aquat Sc. 10:235-243. doi: 10.4194/trjfas.2010.0212
  • Ergin M, Yemenicioglu S. 1997. Geologic assessment of environmental impact in bottom sediments of the eastern Aegean sea. Int J Environ Stud. 51(4):323-334. doi: 10.1080/00207239708711090
  • Erkmen B, Kolankaya D. 2006. Determination of organochlorine pesticide residues in water, sediment, and fish samples from the Meriç Delta, Turkey. Int J Environ An Ch. 86(1-2):161-169. doi: 10.1080/03067310500247926
  • Güçlü H, Doganlar ZB, Gürlü VP, Özal A, Dogan A, Turhan MA, Doganlar O. 2018. Effects of cisplatin-5-fluorouracil combination therapy on oxidative stress, DNA damage, mitochondrial apoptosis, and death receptor signalling in retinal pigment epithelium cells. Cutan Ocul Toxicol. 37(3):291-304. doi: 10.1080/15569527.2018.1456548
  • Güher H, Erdoğan S, Kırgız T, Elipek BÇ. 2011. The Dynamics of Zooplankton in National Park of Lake Gala (Edirne-Turkey). Acta Zool Bulgar. 63(2):157-168.
  • Haap T, Triebskorn R, Kohler HR. 2008. Acute effects of diclofenac and DMSO to Daphnia magna: immobilization and Hsp70 induction. Chemosphere. 73(3):353-359. doi: 10.1016/j.chemosphere.2008.05.062
  • Kohler HR, Alberti G, Seniezak A. 2005. Lead induced hsp70 and hsp60 pattern transformation and leg malformation during postembryonic development in orbadit mite Archegozetes longisetosus Aoki. Comp Biochem Phys C. 141(4):398-405. doi: 10.1016/j.cbpc.2005.09.003
  • Liu W, Li PJ, Qi XM, Zhou QX, Zheng L, Sun TH, Yang YS. 2005. DNA changes in barley (Hordeum vulgare) seedlings induced by cadmium pollution using RAPD analysis. Chemosphere. 61(2):158-167. doi: 10.1016/j.chemosphere.2005.02.078
  • Macario AJL, Macario CE. 2005. Sick chaperones, cellular stress, and disease. New Engl J Med. 353:1489-1501. doi: 10.1056/NEJMra050111
  • Massie HR. 1988. Chemicals. In: Lints FA, Soliman MH, editors. Drosophila as a Model Organism for Ageing Studies. Glasgow: Blackie. p. 59-70.
  • Park WJ, Kriechbaumer V, Müller A, Piotrowski M, Meeley RB, Gierl A, Glawischnig E. 2003. The nitrilase ZmNIT2 converts indole-3-acetonitrile to indole-3-acetic acid. Plant Physiol, 133(2):794-802. doi: 10.1104/pp.103.026609
  • Posgai R, Caitlin B, McCulloch C, Murphy KR, Hussain SM, Rowe JJ, Nielsen MG. 2011. Differential toxicity of silver and titanium dioxide nanoparticles on Drosophila melanogaster development, reproductive effort, and viability: Size, coatings and antioxidants matter. Chemosphere. 85(1):34-42. doi: 10.1016/j.chemosphere.2011.06.040
  • Reveillaud I, Niedzwiecki A, Bensch KG, Fleming JE. 1991. Expression of bovine superoxide dismutase in Drosophila melanogaster augments resistance to oxidative stress. Mol Cell Biol. 11(2):632-640. doi: 10.1128/MCB.11.2.632
  • Ruddle DL, Yengoyan LS, Miquel J, Marcuson R, Fleing JE. 1988. Propyl gallate delays senecence in Drosophila melanogaster. Age; 11(2):54-58. doi: 10.1007/BF02431773
  • Singh MP, Ravi R, Mishraa M, Shrivastavac M, Saxenaa DK. 2010. Kar Chowdhuri D. Effects of co-exposure of benzene, toluene and xylene to Drosophila melanogaster: Alteration in hsp70, hsp60, hsp83, hsp26, ROS generation and oxidative stress markers. Chemosphere. 79(5):577-587. doi: 10.1016/j.chemosphere.2010.01.054
  • Staveley BE, Phillips JP, Hilliker AJ. 1990. Phenotipic consequences of copper-zinc superoxide dismutase overexpression in Drosophila melanogaster. Genome. 33(6):867-872. doi: 10.1139/g90-130
  • Sun J, Tower J. 1999. Flp recombinase-mediated induction of Cu/Zn-superoxide dismutase transgene expression can extend the life span of adult Drosophila melanogaster flies. Mol Cell Biol. 19(1):216-228. doi: 10.1128/MCB.19.1.216
  • Tang YC, Chang HC, Hayer-Hartl M, Hartl FU. 2007 SnapShot: molecular chaperones, part II. Cell. 128(2):412. doi: 10.1016/j.cell.2007.01.013
  • Tokatlı C. 2017. Bioecological and statistical risk assessment of toxic metals in sediments of a worldwide important wetland: Gala Lake National Park (Turkey). Arch Environ Prot. 43(1): 34-47. doi: 10.1515/aep-2017-0007
  • Tokatlı C. 2018. Essential and toxic element bioaccumulations in fishes of Gala and Siğirci Lakes (Meriç River Delta, Turkey). Acta Alimentaria. 47(4):470-478. doi: 10.1556/066.2018.47.4.10
  • Tokatlı C, Baştatlı Y. 2016. Trace and Toxic Element Levels in River Sediments. Pol J Environ Stud. 25(4):1715-1720. doi: 10.15244/pjoes/62678
  • Tokatlı C, Köse E, Uğurluoğlu A, Çiçek A, Emiroğlu Ö. 2014. Gala Gölü (Edirne) Su Kalitesinin Coğrafi Bilgi Sistemi (CBS) Kullanılarak Değerlendirilmesi. Sigma Journal of Engineering and Natural Sciences. 32(4):490-501.
  • Tokatlı C, Emiroğlu Ö, Çiçek A, Köse E, Başkurt S, Aksu S, Uğurluoğlu A, Şahin M, Baştatlı Y. 2016. Investigation of Toxic Metal Bioaccumulations in Fishes of Meriç River Delta (Edirne). Anadolu University Journal of Science and Technology C - Life Sciences and Biotechnology. 5(1):1-11. doi: 10.18036/btdc.32213
  • Yarar M, Magnin G. 1997. Türkiye’nin önemli kuş alanları. İstanbul: Doğal Hayatı Koruma Derneği 313 s.
  • Yılmaz GB. 2004. Gala gölü ve çevresinde ağır metal derişiminin dinamiği. [Yüksek lisans tezi], Trakya Üniversitesi. 59 s.
There are 40 citations in total.

Details

Primary Language Turkish
Subjects Limnology, Fisheries Management
Journal Section Research Article
Authors

Cem Tokatlı 0000-0003-2080-7920

Oğuzhan Doğanlar 0000-0003-2654-7269

Zeynep Banu Doğanlar 0000-0002-1365-9897

Publication Date April 25, 2020
Published in Issue Year 2020Volume: 6 Issue: 1

Cite

APA Tokatlı, C., Doğanlar, O., & Doğanlar, Z. B. (2020). Meriç Delta Balıklarında Çevre Kirliliğinin Genotoksik Etkileri: Antioksidan Savunma, Isı Şok Protein Sinyali ve DNA Hasar-Onarım Mekanizmaları. Journal of Limnology and Freshwater Fisheries Research, 6(1), 14-24. https://doi.org/10.17216/limnofish.516094