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Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında nikotinik asetilkolin reseptör genlerinin karşılaştırılması

Year 2020, Volume: 60 Issue: 3, 73 - 80, 30.09.2020
https://doi.org/10.16955/bitkorb.704856

Abstract

Nikotinik asetilkolin reseptörleri (nAChRs) böcek sinir sisteminde hızlı kolinerjik sinaptik taşınmada görevlidirler. Neonikotinoid grubu insektisitler de bu reseptörleri hedef alarak böceklerin ölmesine neden olurlar. Bu çalışmada, Doğu Akdeniz Bölgesi’nden toplanan bazı Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) popülasyonlarında nAChR α1, α3 ve α4 genleri karşılaştırılarak filogenetik ilişkiler ortaya konulmuştur. Denemede Karataş-Gossypium hirsutum (Adana), Aydıncık-Solanum lycopersicum, Erdemli-S. lycopersicum, Samandağ-Cucumis sativus (Hatay) ve Kumluca-Capsicum annum (Antalya)’dan toplanan beş örnekle çalışmalar yürütülmüştür. nAChR α1, 3 ve 4 genleri tüm popülasyonlar için karşılaştırıldığında α1 genleri arasında bir farklılık belirlenmezken; α3 geninde referans gene (full α3) göre tüm popülasyonlarda V147I, A227T ve T534I aminoasitlerinde ve α4 geninde Aydıncık’ta S401G ve referans gene (full α4) göre tüm popülasyonlarda G198E spesifik aminoasit değişimleri belirlenmiştir. NCBI’dan seçilen aynı gen bölgeleriyle yapılan filogenetik analizlerde bu çalışmada çalışılan her gen kendi gen ailesi içerisinde yer almıştır. Elde edilen bu verilerin neonikotinoid grubu insektisitler nokta mutasyona dayalı dirençle ilgili ileride yürütülebilecek çalışmalara ışık tutması amaçlanmıştır.

Supporting Institution

Çukurova Üniversitesi BAP

Project Number

D3BAP2012

Thanks

Bu çalışma doktora tez çalışmasının sonuçlarını içermekte olup, desteklerinden dolayı Çukurova Üniversitesi BAP birimine (D3BAP2012) teşekkür ederiz. Ayrıca Bemisa tabaci nAChR α1, α3 ve α4 genlerine ait gen ve primer bilgisini bizimle paylaşan Dr. Martin Wlliamson (Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, United Kingdom)’a sonsuz şükranlarımızı sunarız.

References

  • Abbick J., 1991. The biochemistry of imidacloprid. Pflanzenschutz-NACh. Richten Bayer, 44: 198-195.
  • Bass C., Lansdell S. J., Millar N. S., Schroeder I., Turbergc A., Fielda L. M., Williamsona M. S., 2006. Molecular characterisation of nicotinic acetylcholine receptor subunits from the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). Insect Biochem Mol Biol 36:86–96.
  • Bass C., Puinean A. M., Andrews M., Cutler P., Daniels M., Elias J., Paul V. L., Crosswaite A. J., Denholm I., Field L. M., Foster S. P., Lind R., Williamson M. S., Slater R., 2011. Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC neuroscience, 12:51.
  • Bayhan E , Ulusoy M .R., Brown J. K., 2006. Host range, distribution, and natural enemies of Bemisia tabaci ‘B biotype’(Hemiptera: Aleyrodidae) in Turkey. Journal of Pest Science, 79(4), 233-240.
  • Brown J. K., Frohlich D. E., Rosell R. C., 1995. The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex?. Annual review of entomology, 40(1), 511-534.
  • Byrne D. N., Bellows Jr T. S., 1991. Whitefly biology. Annual review of entomology, 36(1), 431-457.
  • Felsenstein J., 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783-791.
  • Gao J. R., Deacutis J. M., Scott J. G., 2007. The nicotinic acetylcholine receptor subunits Mda5 and Mdb3 on autosome 1 of Musca domestica are not involved in spinosad resistance. Insect Mol Biol 16:691–701.
  • Guo J-M., Luo J., Feng L., Li F., Lin K., Wang G., 2018. Cloning and bioinformatics analysis of eight nicotinic acetylcholine receptor genes in Cydia pomonella. Journal of Environmental Entomology, 40(3), 624-632.
  • Ilias A., Lagnel J., Kapantaidaki D., Roditakis E., Tsigenopoulos C. S., Vontas J., Tsagkarakou A., 2015. Transcription analysis of neonicotinoid resistance in Mediterranean (MED) populations of B. tabaci reveal novel cytochrome. BMC Genomics, 16:.
  • Jones A. K., Satelle D. B., 2011. Diversity of insect nicotinic Acetylcholine reseptör subunits. Insect Nicotinic Acetylcholine Receptors, 683. cilt/Advances in Experimental Medicine and Biology, Edt.: Steeve Hervé Thany), Springer Science & Business Media, France, 118 pp.
  • Jones D. T., Taylor W. R., Thornton J. M., 1992. The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences 8: 275-282.
  • Karunker I., Juergen B., Bettina L., Tanja P., Nauen R., Emmanouil R., John V., Kevin G., Ian D., Shai M., 2008. Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochemistry And Molecular Biology, 38(6):634-44.
  • Karut K., 2007. Host instar suitability of Bemisia tabaci (Genn.)(Hom.: Aleyrodidae) for the parasitoid Eretmocerus mundus (Hym.: Aphelinidae). Journal of Pest Science, 80(2), 93-97.
  • Kimura M., 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16:111-120.
  • Liu Z., Williamson M. S., Lansdell S. J., Denholm I., Han Z., Millar N. S., 2005. A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (Brown planthopper). Proceedings of the National Academy of Sciences of the United States of America, 102(24): 8420–5.
  • Meng X., Zhang Y., Guo B., Sun H., Liu C., Liu Z., 2015. Identification of key amino acid differences contributing to neonicotinoid sensitivity between two nAChR α subunits from Pardosa pseudoannulata. Neuroscience Letters, 584, 123-128.
  • Nauen R., Denholm I., 2005. Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Archives of Insect Biochemistry and Physiology: Published in Collaboration with the Entomological Society of America, 58(4), 200-215.
  • Nauen R., Vontas J., Kaussmann M., Wolfel K., 2013. Pymetrozine is hydroxylated by CYP6CM1, a cytochrome P450 conferring neonicotinoid resistance in Bemisia tabaci. Pest management science, 69(4):457–61.
  • NCBI, 2020. https://www.ncbi.nlm.nih.gov/nuccore/?term=Bemisia+tabaci+Nicotinic+ acetylcholine (12.02.2019)
  • Nicholas K. B., Nicholas H. B. J., Deerfıeld D. W., 1997. GeneDoc: Analysis and Visualization of Genetic Variation. http://www.psc.edu/biomed/genedoc, EMBNEW.NEWS, 4:14.
  • Roditakis E., Morou E., Tsagkarakou A., Riga M., Nauen R., Paine M., Vontas J., 2011. Assessment of the Bemisia tabaci CYP6CM1vQ transcript and protein levels in laboratory and field-derived imidacloprid-resistant insects and cross-metabolism potential of the recombinant enzyme. Insect Science, 18 (1):23–29.
  • Saitou N., Nei M., 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4:406-425.
  • Satar G., ULUSOY M. R., Dong K., 2014. Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae)’de İki Yeni Nikotinik Asetil Kolin Reseptör Geninin (nAChR) Moleküler Karakterizasyonu. Türkiye V. Bitki Koruma Kongresi, 3-5 Şubat 2014, Antalya P:35
  • Satar G., Ulusoy M. R., Nauen R., Dong K., 2018. Neonicotinoid insecticide resistance among populations of Bemisia tabaci in the Mediterranean region of Turkey. Bulletin of Insectology, 71(2), 171-177.
  • Stenersen J., 2004. Nicotinoids and Neonicotinoids Chemical pesticides. Mode of Action and Toxicology, 135-136.
  • Tamura K., Stecher G., Peterson D., Filipski A., Kumar S., 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution30: 2725-2729.
  • Tan J., Salgado V. L., Hollingworth R. W., 2008. Neural actions of imidacloprid and their involvement in resistance in the Colorado potato beetle, Leptinotarsa decemlineata (Say). Pest Manag Sci, 64: 37–47.
  • Tang P. A., Jiang H. B., Xu Y-Q., An F-M., Wang J-J., 2009. Molecular characterization of two nicotinic acetylcholine receptor subunits from Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae). Arch. Insect Biochemical Physiology 72: 34–47.
  • Tomizawa M., Casida J. E., 2001. Structure and diversity of insect nicotinic acetylcholine receptors. Pest Manage Sci 57:914–922.
  • Tomizawa M., Casida J. E., 2003. Selective Toxicity of Neonicotinoids attributable to Specifıcity of Insect and Mammalian Nicotinik Receptors. Annu. Rev. Entomol., 48:339–64.
  • Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G., 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25:4876-4882.
  • Van Lenteren J. C. V., Noldus L. P. J. J., 1990. Whitefly-plant relationships: behavioural and ecological aspects. Whiteflies: their bionomics, pest status and management, 47, 49.
  • Wang R., Fang Y., Mu C., Qu C., Li F., Wang Z., Luo C., 2018. Baseline susceptibility and cross-resistance of cycloxaprid, a novel cis-nitromethylene neonicotinoid insecticide, in Bemisia tabaci MED from China. Crop Protection, 110, 283-287.
  • Yao M. D., Yang Y. H., Wu S. W., Wu Y. D. 2008*. Cloning and sequence analysis of a α-subunit gene of nicotinic acetylcholine receptor from Bemisia tabaci (Gennadius). Journal of Nanjing Agricultural University, 2. 41 (2):293-301
  • Yao X., Song F., Chen F., Zhang Y., Gu J., ,Liu S., Liu Z., 2008. Aminoacids within loops D, E and F of insect nicotinic acetylcholine receptor b subunits influence neonicotinoid selectivity. Insect Biochem. Mol. Biol. 38, 834–840.
  • Zhao Y., Yang Y. H., Wu S. W., Wu Y. D., 2009. Cloning, sequence analysis and developmental expression of a cDNA encoding nicotinic acetylcholine receptor a subunit from Plutella xylostella (L.) (Lepidoptera: Plutellidae). Acta Entomol Sinica 52:17–26.
  • Zewen L., Zhaojun H., Yinchang W., Lingchun Z., Hongwei Z., Chengjun L., 2003. Selection for imidacloprid resistance in Nilaparvata lugens: cross-resistance patterns and possible mechanisms. Pest Manag Science, 59:1355–1359

Comparison of nicotinic acetylcholine receptor genes in Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) populations

Year 2020, Volume: 60 Issue: 3, 73 - 80, 30.09.2020
https://doi.org/10.16955/bitkorb.704856

Abstract

Nicotinic acetylcholine receptors (nAChRs) mediate fast cholinergic synaptic transmission in the insect nervous system. Neonicotinoid group insecticides target these receptors, causing mortality at the insects. Phylogenetic relationship was revealed comparing nAChR α1, α3, and α4 genes for the some Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) populations belonging to East Mediterranean Region. Five B. tabaci populations collected from Karataş-Gossypium hirsutum (Adana), Aydıncık-Solanum lycopersicum, Erdemli-S. lycopersicum, (Mersin), Samandag-Cucumis sativus (Hatay), and Kumluca-Capsicum annum (Antalya) were used for the experiment. When nAChR α1, 3, and 4 genes were compared for all populations, no differences were determined for the α1 gene. However, V147I, A227T, and T534I unique amino acid changes in all populations according to the reference gene (full α3) in the α3 gene, S401G in Aydıncık, and G198E in all populations according to a reference gene (full α4) were determined. Phylogenetic tree results indicate that each novel isolates were clustered its own gene group of represensative isolates deposited from NCBI. The obtained results could shed light on the projects that can be carried out in the future regarding the point mutation-based resistance to the neonicotinoid group insecticides.

Project Number

D3BAP2012

References

  • Abbick J., 1991. The biochemistry of imidacloprid. Pflanzenschutz-NACh. Richten Bayer, 44: 198-195.
  • Bass C., Lansdell S. J., Millar N. S., Schroeder I., Turbergc A., Fielda L. M., Williamsona M. S., 2006. Molecular characterisation of nicotinic acetylcholine receptor subunits from the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). Insect Biochem Mol Biol 36:86–96.
  • Bass C., Puinean A. M., Andrews M., Cutler P., Daniels M., Elias J., Paul V. L., Crosswaite A. J., Denholm I., Field L. M., Foster S. P., Lind R., Williamson M. S., Slater R., 2011. Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC neuroscience, 12:51.
  • Bayhan E , Ulusoy M .R., Brown J. K., 2006. Host range, distribution, and natural enemies of Bemisia tabaci ‘B biotype’(Hemiptera: Aleyrodidae) in Turkey. Journal of Pest Science, 79(4), 233-240.
  • Brown J. K., Frohlich D. E., Rosell R. C., 1995. The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex?. Annual review of entomology, 40(1), 511-534.
  • Byrne D. N., Bellows Jr T. S., 1991. Whitefly biology. Annual review of entomology, 36(1), 431-457.
  • Felsenstein J., 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783-791.
  • Gao J. R., Deacutis J. M., Scott J. G., 2007. The nicotinic acetylcholine receptor subunits Mda5 and Mdb3 on autosome 1 of Musca domestica are not involved in spinosad resistance. Insect Mol Biol 16:691–701.
  • Guo J-M., Luo J., Feng L., Li F., Lin K., Wang G., 2018. Cloning and bioinformatics analysis of eight nicotinic acetylcholine receptor genes in Cydia pomonella. Journal of Environmental Entomology, 40(3), 624-632.
  • Ilias A., Lagnel J., Kapantaidaki D., Roditakis E., Tsigenopoulos C. S., Vontas J., Tsagkarakou A., 2015. Transcription analysis of neonicotinoid resistance in Mediterranean (MED) populations of B. tabaci reveal novel cytochrome. BMC Genomics, 16:.
  • Jones A. K., Satelle D. B., 2011. Diversity of insect nicotinic Acetylcholine reseptör subunits. Insect Nicotinic Acetylcholine Receptors, 683. cilt/Advances in Experimental Medicine and Biology, Edt.: Steeve Hervé Thany), Springer Science & Business Media, France, 118 pp.
  • Jones D. T., Taylor W. R., Thornton J. M., 1992. The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences 8: 275-282.
  • Karunker I., Juergen B., Bettina L., Tanja P., Nauen R., Emmanouil R., John V., Kevin G., Ian D., Shai M., 2008. Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochemistry And Molecular Biology, 38(6):634-44.
  • Karut K., 2007. Host instar suitability of Bemisia tabaci (Genn.)(Hom.: Aleyrodidae) for the parasitoid Eretmocerus mundus (Hym.: Aphelinidae). Journal of Pest Science, 80(2), 93-97.
  • Kimura M., 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16:111-120.
  • Liu Z., Williamson M. S., Lansdell S. J., Denholm I., Han Z., Millar N. S., 2005. A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (Brown planthopper). Proceedings of the National Academy of Sciences of the United States of America, 102(24): 8420–5.
  • Meng X., Zhang Y., Guo B., Sun H., Liu C., Liu Z., 2015. Identification of key amino acid differences contributing to neonicotinoid sensitivity between two nAChR α subunits from Pardosa pseudoannulata. Neuroscience Letters, 584, 123-128.
  • Nauen R., Denholm I., 2005. Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Archives of Insect Biochemistry and Physiology: Published in Collaboration with the Entomological Society of America, 58(4), 200-215.
  • Nauen R., Vontas J., Kaussmann M., Wolfel K., 2013. Pymetrozine is hydroxylated by CYP6CM1, a cytochrome P450 conferring neonicotinoid resistance in Bemisia tabaci. Pest management science, 69(4):457–61.
  • NCBI, 2020. https://www.ncbi.nlm.nih.gov/nuccore/?term=Bemisia+tabaci+Nicotinic+ acetylcholine (12.02.2019)
  • Nicholas K. B., Nicholas H. B. J., Deerfıeld D. W., 1997. GeneDoc: Analysis and Visualization of Genetic Variation. http://www.psc.edu/biomed/genedoc, EMBNEW.NEWS, 4:14.
  • Roditakis E., Morou E., Tsagkarakou A., Riga M., Nauen R., Paine M., Vontas J., 2011. Assessment of the Bemisia tabaci CYP6CM1vQ transcript and protein levels in laboratory and field-derived imidacloprid-resistant insects and cross-metabolism potential of the recombinant enzyme. Insect Science, 18 (1):23–29.
  • Saitou N., Nei M., 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4:406-425.
  • Satar G., ULUSOY M. R., Dong K., 2014. Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae)’de İki Yeni Nikotinik Asetil Kolin Reseptör Geninin (nAChR) Moleküler Karakterizasyonu. Türkiye V. Bitki Koruma Kongresi, 3-5 Şubat 2014, Antalya P:35
  • Satar G., Ulusoy M. R., Nauen R., Dong K., 2018. Neonicotinoid insecticide resistance among populations of Bemisia tabaci in the Mediterranean region of Turkey. Bulletin of Insectology, 71(2), 171-177.
  • Stenersen J., 2004. Nicotinoids and Neonicotinoids Chemical pesticides. Mode of Action and Toxicology, 135-136.
  • Tamura K., Stecher G., Peterson D., Filipski A., Kumar S., 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution30: 2725-2729.
  • Tan J., Salgado V. L., Hollingworth R. W., 2008. Neural actions of imidacloprid and their involvement in resistance in the Colorado potato beetle, Leptinotarsa decemlineata (Say). Pest Manag Sci, 64: 37–47.
  • Tang P. A., Jiang H. B., Xu Y-Q., An F-M., Wang J-J., 2009. Molecular characterization of two nicotinic acetylcholine receptor subunits from Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae). Arch. Insect Biochemical Physiology 72: 34–47.
  • Tomizawa M., Casida J. E., 2001. Structure and diversity of insect nicotinic acetylcholine receptors. Pest Manage Sci 57:914–922.
  • Tomizawa M., Casida J. E., 2003. Selective Toxicity of Neonicotinoids attributable to Specifıcity of Insect and Mammalian Nicotinik Receptors. Annu. Rev. Entomol., 48:339–64.
  • Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G., 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25:4876-4882.
  • Van Lenteren J. C. V., Noldus L. P. J. J., 1990. Whitefly-plant relationships: behavioural and ecological aspects. Whiteflies: their bionomics, pest status and management, 47, 49.
  • Wang R., Fang Y., Mu C., Qu C., Li F., Wang Z., Luo C., 2018. Baseline susceptibility and cross-resistance of cycloxaprid, a novel cis-nitromethylene neonicotinoid insecticide, in Bemisia tabaci MED from China. Crop Protection, 110, 283-287.
  • Yao M. D., Yang Y. H., Wu S. W., Wu Y. D. 2008*. Cloning and sequence analysis of a α-subunit gene of nicotinic acetylcholine receptor from Bemisia tabaci (Gennadius). Journal of Nanjing Agricultural University, 2. 41 (2):293-301
  • Yao X., Song F., Chen F., Zhang Y., Gu J., ,Liu S., Liu Z., 2008. Aminoacids within loops D, E and F of insect nicotinic acetylcholine receptor b subunits influence neonicotinoid selectivity. Insect Biochem. Mol. Biol. 38, 834–840.
  • Zhao Y., Yang Y. H., Wu S. W., Wu Y. D., 2009. Cloning, sequence analysis and developmental expression of a cDNA encoding nicotinic acetylcholine receptor a subunit from Plutella xylostella (L.) (Lepidoptera: Plutellidae). Acta Entomol Sinica 52:17–26.
  • Zewen L., Zhaojun H., Yinchang W., Lingchun Z., Hongwei Z., Chengjun L., 2003. Selection for imidacloprid resistance in Nilaparvata lugens: cross-resistance patterns and possible mechanisms. Pest Manag Science, 59:1355–1359
There are 38 citations in total.

Details

Primary Language Turkish
Journal Section Makaleler
Authors

Gül Satar 0000-0002-5120-3313

Mehmet Rifat Ulusoy

Project Number D3BAP2012
Publication Date September 30, 2020
Submission Date March 16, 2020
Acceptance Date May 14, 2020
Published in Issue Year 2020 Volume: 60 Issue: 3

Cite

APA Satar, G., & Ulusoy, M. R. (2020). Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında nikotinik asetilkolin reseptör genlerinin karşılaştırılması. Plant Protection Bulletin, 60(3), 73-80. https://doi.org/10.16955/bitkorb.704856
AMA Satar G, Ulusoy MR. Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında nikotinik asetilkolin reseptör genlerinin karşılaştırılması. Plant Protection Bulletin. September 2020;60(3):73-80. doi:10.16955/bitkorb.704856
Chicago Satar, Gül, and Mehmet Rifat Ulusoy. “Bemisia Tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında Nikotinik Asetilkolin reseptör Genlerinin karşılaştırılması”. Plant Protection Bulletin 60, no. 3 (September 2020): 73-80. https://doi.org/10.16955/bitkorb.704856.
EndNote Satar G, Ulusoy MR (September 1, 2020) Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında nikotinik asetilkolin reseptör genlerinin karşılaştırılması. Plant Protection Bulletin 60 3 73–80.
IEEE G. Satar and M. R. Ulusoy, “Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında nikotinik asetilkolin reseptör genlerinin karşılaştırılması”, Plant Protection Bulletin, vol. 60, no. 3, pp. 73–80, 2020, doi: 10.16955/bitkorb.704856.
ISNAD Satar, Gül - Ulusoy, Mehmet Rifat. “Bemisia Tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında Nikotinik Asetilkolin reseptör Genlerinin karşılaştırılması”. Plant Protection Bulletin 60/3 (September 2020), 73-80. https://doi.org/10.16955/bitkorb.704856.
JAMA Satar G, Ulusoy MR. Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında nikotinik asetilkolin reseptör genlerinin karşılaştırılması. Plant Protection Bulletin. 2020;60:73–80.
MLA Satar, Gül and Mehmet Rifat Ulusoy. “Bemisia Tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında Nikotinik Asetilkolin reseptör Genlerinin karşılaştırılması”. Plant Protection Bulletin, vol. 60, no. 3, 2020, pp. 73-80, doi:10.16955/bitkorb.704856.
Vancouver Satar G, Ulusoy MR. Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) popülasyonlarında nikotinik asetilkolin reseptör genlerinin karşılaştırılması. Plant Protection Bulletin. 2020;60(3):73-80.

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