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Determination of potential insect vectors and subgroups of aster yellows phytoplasma in the carrot (Daucus carota L.) (Apiaceae) cultivation areas of Ankara and Konya Provinces, Türkiye

Year 2022, Volume: 46 Issue: 4, 385 - 398, 07.01.2023
https://doi.org/10.16970/entoted.1118787

Abstract

Aster yellows phytoplasma (16Sr-I, AYp) is a widespread plant pathogen affecting a wide range of economically important crops. AYp can be distributed widely via insect vectors and is associated with severe redness and yellowing in carrot leaves. The presence of potential insect vectors of aster yellows phytoplasma was investigated in the Ankara and Konya Provinces, the largest carrot production areas in Türkiye. Forty-five insect samples were collected during the field studies between March and September 2020. Morphological and molecular studies have shown that Neophilaenus campestris (Fallén, 1805) (Hemiptera: Aphrophoridae), Empoasca decipiens Paoli, 1930 (Hemiptera: Cicadellidae) and Psammotettix striatus (L., 1758) (Hemiptera: Cicadellidae) carried 16SrI-F phytoplasma. Psammotettix striatus collected from different locations contained subgroup 16SrI-R, as well. In addition, subgroup 16SrI-B was determined in Cicadula divaricata Ribaut, 1952 (Hemiptera: Cicadellidae) and in a psyllid (Psylloidea: Psyllidae) species. Empoasca sp., Anaceratagallia sp. (Hemiptera: Cicadellidae) and Psammotettix confinis (Dahlbom, 1850) (Hemiptera: Cicadellidae) were determined as potential phytoplasma vectors. Phytoplasma 16Sr rRNA and insect cytochrome oxidase gene nucleotide sequences were used for phylogenetic analysis. The results will contribute to vector-based control of aster yellows phytoplasmas in carrot cultivation areas.

Supporting Institution

Bilecik Şeyh Edebali University Scientific Research Projects

Project Number

2017-02.BŞEÜ.06-01

Thanks

This manuscript is a part of the PhD thesis of the first/corresponding author. The authors are grateful to Bilecik Şeyh Edebali University Scientific Research Projects for supporting this project (Code: 2017-02.BŞEÜ.06-01). We would like to thank Dr. Xaiver Foissac for providing a positive control in the molecular detection of phytoplasmas.

References

  • Alfaro-Fernández, A., I. Ibañez, E. Bertolini, D. Hernández-Llopis, M. Cambra & M. I. Font, 2017. Transmission of Spiroplasma citri in carrot seeds and development of a real-time PCR for its detection. Journal of Plant Pathology, 99 (2): 371-379.
  • Bertaccini, A., 2007. Phytoplasmas: diversity, taxonomy, and epidemiology. Frontiers in Bioscience, 12: 673-689.
  • Bertaccini, A. & I. M. Lee, 2018. “Phytoplasmas: An Update, 1-31”. In: Phytoplasmas: Plant Pathogenic Bacteria - I. Characterisation and Epidemiology of Phytoplasma-Associated Diseases (Eds. G. P. Rao, A., Bertaccini, N. Fiore & L. W. Liefting), Springer, Singapur, 345 pp.
  • Bertolini, E., G.R. Teresani, M. Loiseau, F. A. O. Tanaka, S. Barbé, C. Martínez, P. Gentit, M. Lopez & M. Cambra, 2015. Transmission of ‘Candidatus Liberibacter solanacearum’ in carrot seeds. Plant Pathology, 64 (2): 276-285.
  • Carminati, G., E. Satta, S. Paltrinieri & A. Bertaccini, 2019. Simultaneous evaluation of ‘Candidatus Phytoplasma’ and ‘Candidatus Liberibacter solanacearum’ seed transmission in carrot. Phytopathology Mollicutes, 9 (1): 141-142.
  • Cebrián, M. C., F. J. Villaescusa, A. Alfaro-Fernández, A. Hermoso de Mendoza, M. C. Córdoba-Sellés, C. Jordá, J. C. Ferrándiz, S. Sanjuán & M. I. Font, 2010. First report of Spiroplasma citri in carrot in Europe. Plant Disease, 94 (10): 1264.
  • Deng, S. & C. Hiruki, 1991. Amplification of 16S rRNA genes from culturable and non-culturable mollicutes. Journal of Microbiological Methods, 14 (1): 53-61.
  • Duduk, B., A. Bulajić, N. Duduk, A. Calari, S. Paltrinieri, B. Krstić & A. Bertaccini, 2007. Identification of phytoplasmas belonging to aster yellows ribosomal group (16SrI) in vegetables in Serbia. Bulletin of Insectology, 60 (2): 341-342.
  • Duduk, B., P. Peric, D. Marcic, T. Drobnjakovic, L. Picciau, A. Alma & A. Bertaccini, 2008. Phytoplasmas in carrots: disease and potential vectors in Serbia. Bulletin of Insectology, 61 (2): 327-331.
  • Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology & Biotechnology, 3 (5): 294-299.
  • Frost, K. E., D. K. Willis & R. L. Groves, 2011. Detection and variability of aster yellows phytoplasma titer in its insect vector, Macrosteles quadrilineatus (Hemiptera: Cicadellidae). Journal of Economic Entomology, 104 (6): 1800-1815.
  • Gera, A., L. Maslenin, P. G. Weintraub & M. Mawassi, 2011. Phytoplasma and spiroplasma diseases in open-field crops in Israel. Bulletin of Insectology, 64 (Supplement): 53-54.
  • Gundersen, D. E. & I. M. Lee, 1996. Ultrasensitive detection of phytoplasmas by nested-PCR assays using two universal primer pairs. Phytopathologia Mediterranea, 35 (3): 144-151.
  • Hall, T. A., 1999. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95-98.
  • Harrison, N. A., R. E. Davis, C. Oropeza, E. E. Helmick, M. Narvaez, S. Eden-Green, M. Dollet & M. Dickinson, 2014. ‘Candidatus Phytoplasma palmicola’, associated with a lethal yellowing-type disease of coconut (Cocos nucifera L.) in Mozambique. International Journal of Systematic & Evolutionary Microbiology, 64 (6):1890-1899.
  • Hebert, P. D., A. Cywinska, S. L. Ball & J. R. deWaard, 2003. Biological identifications through DNA barcodes. Proceedings Biological Sciences, 270 (1512): 313-321.
  • Hogenhout, S. A. & R. Loria, 2008. Virulence mechanisms of Gram-positive plant pathogenic bacteria. Plant Biology, 11 (4): 449-456.
  • Hogenhout, S. A., K. Oshima, E. Ammar, S. Kakizawa, H. N. Kingdom & S. Namba, 2008. Phytoplasmas: bacteria that manipulate plants and insects. Molecular Plant Pathology, 9 (4): 403-423.
  • Hoy, C. W., X. Zhou, L. R. Nault, S. A. Miller & J. Styer, 1999. Host plant, phytoplasma, and reproductive status effects on flight behavior of aster leafhopper (Homoptera: Cicadellidae). Annals of Entomological Society of America, 92 (4): 523-528.
  • İnak, E., E. Özdemir, A. E. Atış, F. Randa-Zelyüt, A. İnak, Ü. Demir, Ü. E. Roditakis & J. Vontas, 2021. Population structure and insecticide resistance status of Tuta absoluta populations from Turkey. Pest Management Science, 77 (10): 4741-4748.
  • Katoh, K., J. Rozewicki & K. D. Yamada, 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinformatics, 19 & 20 (4):1160-1166.
  • Kumar, S., G. Stecher, M. Li, C. Knyaz & K. Tamura, 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology Evolution, 35 (6): 1547-1549.
  • Kumari, S., K. Nagendran, A. B. Rai, B. Singh, G. P. Rao & A. Bertaccini, 2019. Global status of phytoplasma diseases in vegetable crops. Frontiers Microbiology, 10: 1349.doi: 10.3389/fmicb.2019.01349
  • Lee I. M., K. D. Bottner, J. E. Munyaneza, R.E. Davis, J. M. Crosslin & L. J. du Toit, 2006. Carrot purple leaf: a new spiroplasmal disease associated with carrots in Washington State. Plant Diseases, 90 (8): 989-993.
  • Lorenz, K., B. Schneider, U. Ahrens & E. Seemüller, 1995. Detection of the apple proliferation and pear decline phytoplasmas by PCR amplification of ribosomal and nonribosomal DNA. Phytopathology, 85: 771-776.
  • McCoy, R. E., A. Caudwell, C. J. Chang, T. A. Chen, L. N. Chiykowski, M. T. Cousin, J. L. Dale, G. T. N. de Leeuw, D. A. Golino, K. J. Hackett, B. C. Kirkpatrick, R. Marwitz, H. Petzold, R. H. Sinha, M. Sugiura, R. F. Whitcomb, I. L. Yang, B. M. Zhu & E. Seemüller, 1989. “Plant Diseases Associated with Mycoplasmalike Organisms, 545-560”. In: The Mycoplasmas, Vol. 5 (Eds. R. F. Whitcomb & J. G. Tully). Academic Press, New York, 679 pp.
  • Pastore, M., E. Raffone, M. Santonastaso, R. Priore, S. Paltrinieri, A. Bertaccini & A. M. Simeone, 2004. Phytoplasma detection in Empoasca decedens and Empoasca spp. and their possible role as vectors of European stone fruit yellows (16SrXB) phytoplasma. Acta Horticulturae, 657: 507-511.
  • Randa-Zelyüt, F., F. Ertunç & D. Şenal, 2022. The association of 16SrVI and 16SrI phytoplasma groups with carrot seeds and weeds in Ankara and Konya provinces in Turkey. Plant Protection Bulletin, 62 (1): 24-33.
  • Satta, E., A. S. Ramírez, S. Paltrinieri, N. Contaldo, P. Benito, J. B. Poveda & A. Bertaccini, 2017. Simultaneous detection of mixed ‘Candidatus Phytoplasma asteris’ and ‘Ca. Liberibacter solanacearum’ infection in carrot. Phytopathologia Mediterranea, 55 (3): 401-409.
  • Stillson, P. T. & Z. Szendrei, 2020. Identifying leafhopper targets for controlling Aster Yellows in carrots and celery. Insects, 11 (7): 411.
  • Stolarczyk, J. & J. Janick, 2011. Carrot: history and iconography. Chronica, 51 (2): 13-18.
  • Tamer, A., M. Aydemir & A. Has, 1997. Ankara ve Konya illerinde korunga ve yoncada görülen zararlı ve faydalı böcekler üzerinde faunistik çalışmalar. Bitki Koruma Bülteni, 37 (3): 125-161 (in Turkish with abstract in English).
  • Tamura, K., 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular Biology & Evolution, 9 (4): 678-687.
  • TUIK, 2021. Turkish Statistical Institute. (Web page: https://data.tuik.gov.tr/Kategori/GetKategori?p=tarim-111&dil=1) (Date accessed: 16.12.2021).
  • Weintraub, P. G. & L. A. Beanland, 2006. Insect vectors of phytoplasmas. Annual Review of Entomology, 51: 91-111.
  • Zhao, Y., W. Wei, I. M. Lee, J. Shao, X. Suo & R. E. Davis, 2013. “The iPhyClassifier, an Interactive Online Tool for Phytoplasma Classification and Taxonomic Assignment, 329-338”. In: Phytoplasma. Methods in Molecular Biology (Eds. M. Dickinson & J. Hodgetts), Vol: 938. Humana Press, Totowa, 421 pp.

Ankara ve Konya (Türkiye) illeri havuç (Daucus carota L.) (Apiaceae) ekim alanlarında aster yellows fitoplazmasının altgruplarının ve potansiyel böcek vektörlerinin belirlenmesi

Year 2022, Volume: 46 Issue: 4, 385 - 398, 07.01.2023
https://doi.org/10.16970/entoted.1118787

Abstract

Aster yellows fitoplazma (AYp), ekonomik açıdan önemli farklı tarım ürünlerini etkileyen yaygın bir bitki patojenidir. AYp, böcek vektörleri aracılığıyla geniş alanlara yayılabilir ve havuç yapraklarında şiddetli kızarıklık ve sararma ile ilişkilendirilir. Türkiye'nin en büyük havuç üretim alanları olan Ankara ve Konya illerinde aster yellows fitoplazmasının potansiyel böcek vektörlerinin varlığı araştırılmıştır. Mart-Eylül 2020 tarihleri arasında arazi çalışmalarında 45 böcek örneği toplanmıştır. Morfolojik ve moleküler çalışmalar Neophilaenus campestris (Fallén, 1805) (Hemiptera: Aphrophoridae), Empoasca decipiens Paoli, 1930 (Hemiptera: Cicadellidae) ve Psammotettix striatus (L., 1758) (Hemiptera: Cicadellidae) türlerinin 16SrI-F altgrubu ile bulaşık olduğunu göstermiştir. Bununla birlikte, farklı lokasyonlardan toplanan P. striatus türü ise 16SrI-R altgrubu ile bulaşıktı. Cicadula divaricata Ribaut, 1952 (Hemiptera: Cicadellidae) ve bir psyllid (Psylloidea: Psyllidae) türünde 16SrI-B altgrubu saptanmıştır. Empoasca sp., Anaceratagallia sp. (Hemiptera: Cicadellidae) ve Psammotettix confinis (Dahlbom, 1850) (Hemiptera: Cicadellidae) ise potansiyel fitoplazma vektörleri olarak belirlenmiştir. Elde edilen fitoplazma 16S rRNA ve böcek sitokrom oksidaz genlerinin nükleotit dizileri filogenetik çalışmalarda kullanılmıştır. Bu sonuçlar, havuç ekim alanlarında aster yellows fitoplazmalarının vektör kontrolüne katkıda bulunacaktır.

Project Number

2017-02.BŞEÜ.06-01

References

  • Alfaro-Fernández, A., I. Ibañez, E. Bertolini, D. Hernández-Llopis, M. Cambra & M. I. Font, 2017. Transmission of Spiroplasma citri in carrot seeds and development of a real-time PCR for its detection. Journal of Plant Pathology, 99 (2): 371-379.
  • Bertaccini, A., 2007. Phytoplasmas: diversity, taxonomy, and epidemiology. Frontiers in Bioscience, 12: 673-689.
  • Bertaccini, A. & I. M. Lee, 2018. “Phytoplasmas: An Update, 1-31”. In: Phytoplasmas: Plant Pathogenic Bacteria - I. Characterisation and Epidemiology of Phytoplasma-Associated Diseases (Eds. G. P. Rao, A., Bertaccini, N. Fiore & L. W. Liefting), Springer, Singapur, 345 pp.
  • Bertolini, E., G.R. Teresani, M. Loiseau, F. A. O. Tanaka, S. Barbé, C. Martínez, P. Gentit, M. Lopez & M. Cambra, 2015. Transmission of ‘Candidatus Liberibacter solanacearum’ in carrot seeds. Plant Pathology, 64 (2): 276-285.
  • Carminati, G., E. Satta, S. Paltrinieri & A. Bertaccini, 2019. Simultaneous evaluation of ‘Candidatus Phytoplasma’ and ‘Candidatus Liberibacter solanacearum’ seed transmission in carrot. Phytopathology Mollicutes, 9 (1): 141-142.
  • Cebrián, M. C., F. J. Villaescusa, A. Alfaro-Fernández, A. Hermoso de Mendoza, M. C. Córdoba-Sellés, C. Jordá, J. C. Ferrándiz, S. Sanjuán & M. I. Font, 2010. First report of Spiroplasma citri in carrot in Europe. Plant Disease, 94 (10): 1264.
  • Deng, S. & C. Hiruki, 1991. Amplification of 16S rRNA genes from culturable and non-culturable mollicutes. Journal of Microbiological Methods, 14 (1): 53-61.
  • Duduk, B., A. Bulajić, N. Duduk, A. Calari, S. Paltrinieri, B. Krstić & A. Bertaccini, 2007. Identification of phytoplasmas belonging to aster yellows ribosomal group (16SrI) in vegetables in Serbia. Bulletin of Insectology, 60 (2): 341-342.
  • Duduk, B., P. Peric, D. Marcic, T. Drobnjakovic, L. Picciau, A. Alma & A. Bertaccini, 2008. Phytoplasmas in carrots: disease and potential vectors in Serbia. Bulletin of Insectology, 61 (2): 327-331.
  • Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology & Biotechnology, 3 (5): 294-299.
  • Frost, K. E., D. K. Willis & R. L. Groves, 2011. Detection and variability of aster yellows phytoplasma titer in its insect vector, Macrosteles quadrilineatus (Hemiptera: Cicadellidae). Journal of Economic Entomology, 104 (6): 1800-1815.
  • Gera, A., L. Maslenin, P. G. Weintraub & M. Mawassi, 2011. Phytoplasma and spiroplasma diseases in open-field crops in Israel. Bulletin of Insectology, 64 (Supplement): 53-54.
  • Gundersen, D. E. & I. M. Lee, 1996. Ultrasensitive detection of phytoplasmas by nested-PCR assays using two universal primer pairs. Phytopathologia Mediterranea, 35 (3): 144-151.
  • Hall, T. A., 1999. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95-98.
  • Harrison, N. A., R. E. Davis, C. Oropeza, E. E. Helmick, M. Narvaez, S. Eden-Green, M. Dollet & M. Dickinson, 2014. ‘Candidatus Phytoplasma palmicola’, associated with a lethal yellowing-type disease of coconut (Cocos nucifera L.) in Mozambique. International Journal of Systematic & Evolutionary Microbiology, 64 (6):1890-1899.
  • Hebert, P. D., A. Cywinska, S. L. Ball & J. R. deWaard, 2003. Biological identifications through DNA barcodes. Proceedings Biological Sciences, 270 (1512): 313-321.
  • Hogenhout, S. A. & R. Loria, 2008. Virulence mechanisms of Gram-positive plant pathogenic bacteria. Plant Biology, 11 (4): 449-456.
  • Hogenhout, S. A., K. Oshima, E. Ammar, S. Kakizawa, H. N. Kingdom & S. Namba, 2008. Phytoplasmas: bacteria that manipulate plants and insects. Molecular Plant Pathology, 9 (4): 403-423.
  • Hoy, C. W., X. Zhou, L. R. Nault, S. A. Miller & J. Styer, 1999. Host plant, phytoplasma, and reproductive status effects on flight behavior of aster leafhopper (Homoptera: Cicadellidae). Annals of Entomological Society of America, 92 (4): 523-528.
  • İnak, E., E. Özdemir, A. E. Atış, F. Randa-Zelyüt, A. İnak, Ü. Demir, Ü. E. Roditakis & J. Vontas, 2021. Population structure and insecticide resistance status of Tuta absoluta populations from Turkey. Pest Management Science, 77 (10): 4741-4748.
  • Katoh, K., J. Rozewicki & K. D. Yamada, 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinformatics, 19 & 20 (4):1160-1166.
  • Kumar, S., G. Stecher, M. Li, C. Knyaz & K. Tamura, 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology Evolution, 35 (6): 1547-1549.
  • Kumari, S., K. Nagendran, A. B. Rai, B. Singh, G. P. Rao & A. Bertaccini, 2019. Global status of phytoplasma diseases in vegetable crops. Frontiers Microbiology, 10: 1349.doi: 10.3389/fmicb.2019.01349
  • Lee I. M., K. D. Bottner, J. E. Munyaneza, R.E. Davis, J. M. Crosslin & L. J. du Toit, 2006. Carrot purple leaf: a new spiroplasmal disease associated with carrots in Washington State. Plant Diseases, 90 (8): 989-993.
  • Lorenz, K., B. Schneider, U. Ahrens & E. Seemüller, 1995. Detection of the apple proliferation and pear decline phytoplasmas by PCR amplification of ribosomal and nonribosomal DNA. Phytopathology, 85: 771-776.
  • McCoy, R. E., A. Caudwell, C. J. Chang, T. A. Chen, L. N. Chiykowski, M. T. Cousin, J. L. Dale, G. T. N. de Leeuw, D. A. Golino, K. J. Hackett, B. C. Kirkpatrick, R. Marwitz, H. Petzold, R. H. Sinha, M. Sugiura, R. F. Whitcomb, I. L. Yang, B. M. Zhu & E. Seemüller, 1989. “Plant Diseases Associated with Mycoplasmalike Organisms, 545-560”. In: The Mycoplasmas, Vol. 5 (Eds. R. F. Whitcomb & J. G. Tully). Academic Press, New York, 679 pp.
  • Pastore, M., E. Raffone, M. Santonastaso, R. Priore, S. Paltrinieri, A. Bertaccini & A. M. Simeone, 2004. Phytoplasma detection in Empoasca decedens and Empoasca spp. and their possible role as vectors of European stone fruit yellows (16SrXB) phytoplasma. Acta Horticulturae, 657: 507-511.
  • Randa-Zelyüt, F., F. Ertunç & D. Şenal, 2022. The association of 16SrVI and 16SrI phytoplasma groups with carrot seeds and weeds in Ankara and Konya provinces in Turkey. Plant Protection Bulletin, 62 (1): 24-33.
  • Satta, E., A. S. Ramírez, S. Paltrinieri, N. Contaldo, P. Benito, J. B. Poveda & A. Bertaccini, 2017. Simultaneous detection of mixed ‘Candidatus Phytoplasma asteris’ and ‘Ca. Liberibacter solanacearum’ infection in carrot. Phytopathologia Mediterranea, 55 (3): 401-409.
  • Stillson, P. T. & Z. Szendrei, 2020. Identifying leafhopper targets for controlling Aster Yellows in carrots and celery. Insects, 11 (7): 411.
  • Stolarczyk, J. & J. Janick, 2011. Carrot: history and iconography. Chronica, 51 (2): 13-18.
  • Tamer, A., M. Aydemir & A. Has, 1997. Ankara ve Konya illerinde korunga ve yoncada görülen zararlı ve faydalı böcekler üzerinde faunistik çalışmalar. Bitki Koruma Bülteni, 37 (3): 125-161 (in Turkish with abstract in English).
  • Tamura, K., 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular Biology & Evolution, 9 (4): 678-687.
  • TUIK, 2021. Turkish Statistical Institute. (Web page: https://data.tuik.gov.tr/Kategori/GetKategori?p=tarim-111&dil=1) (Date accessed: 16.12.2021).
  • Weintraub, P. G. & L. A. Beanland, 2006. Insect vectors of phytoplasmas. Annual Review of Entomology, 51: 91-111.
  • Zhao, Y., W. Wei, I. M. Lee, J. Shao, X. Suo & R. E. Davis, 2013. “The iPhyClassifier, an Interactive Online Tool for Phytoplasma Classification and Taxonomic Assignment, 329-338”. In: Phytoplasma. Methods in Molecular Biology (Eds. M. Dickinson & J. Hodgetts), Vol: 938. Humana Press, Totowa, 421 pp.
There are 36 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Filiz Randa Zelyüt 0000-0002-1366-4389

Emre İnak 0000-0003-0411-4198

Emine Demir Özden 0000-0003-4486-003X

Derya Şenal 0000-0003-0897-4486

Filiz Ertunç 0000-0002-0557-6119

Project Number 2017-02.BŞEÜ.06-01
Early Pub Date October 17, 2022
Publication Date January 7, 2023
Submission Date May 20, 2022
Acceptance Date October 10, 2022
Published in Issue Year 2022 Volume: 46 Issue: 4

Cite

APA Randa Zelyüt, F., İnak, E., Demir Özden, E., Şenal, D., et al. (2023). Determination of potential insect vectors and subgroups of aster yellows phytoplasma in the carrot (Daucus carota L.) (Apiaceae) cultivation areas of Ankara and Konya Provinces, Türkiye. Turkish Journal of Entomology, 46(4), 385-398. https://doi.org/10.16970/entoted.1118787
AMA Randa Zelyüt F, İnak E, Demir Özden E, Şenal D, Ertunç F. Determination of potential insect vectors and subgroups of aster yellows phytoplasma in the carrot (Daucus carota L.) (Apiaceae) cultivation areas of Ankara and Konya Provinces, Türkiye. TED. January 2023;46(4):385-398. doi:10.16970/entoted.1118787
Chicago Randa Zelyüt, Filiz, Emre İnak, Emine Demir Özden, Derya Şenal, and Filiz Ertunç. “Determination of Potential Insect Vectors and Subgroups of Aster Yellows Phytoplasma in the Carrot (Daucus Carota L.) (Apiaceae) Cultivation Areas of Ankara and Konya Provinces, Türkiye”. Turkish Journal of Entomology 46, no. 4 (January 2023): 385-98. https://doi.org/10.16970/entoted.1118787.
EndNote Randa Zelyüt F, İnak E, Demir Özden E, Şenal D, Ertunç F (January 1, 2023) Determination of potential insect vectors and subgroups of aster yellows phytoplasma in the carrot (Daucus carota L.) (Apiaceae) cultivation areas of Ankara and Konya Provinces, Türkiye. Turkish Journal of Entomology 46 4 385–398.
IEEE F. Randa Zelyüt, E. İnak, E. Demir Özden, D. Şenal, and F. Ertunç, “Determination of potential insect vectors and subgroups of aster yellows phytoplasma in the carrot (Daucus carota L.) (Apiaceae) cultivation areas of Ankara and Konya Provinces, Türkiye”, TED, vol. 46, no. 4, pp. 385–398, 2023, doi: 10.16970/entoted.1118787.
ISNAD Randa Zelyüt, Filiz et al. “Determination of Potential Insect Vectors and Subgroups of Aster Yellows Phytoplasma in the Carrot (Daucus Carota L.) (Apiaceae) Cultivation Areas of Ankara and Konya Provinces, Türkiye”. Turkish Journal of Entomology 46/4 (January 2023), 385-398. https://doi.org/10.16970/entoted.1118787.
JAMA Randa Zelyüt F, İnak E, Demir Özden E, Şenal D, Ertunç F. Determination of potential insect vectors and subgroups of aster yellows phytoplasma in the carrot (Daucus carota L.) (Apiaceae) cultivation areas of Ankara and Konya Provinces, Türkiye. TED. 2023;46:385–398.
MLA Randa Zelyüt, Filiz et al. “Determination of Potential Insect Vectors and Subgroups of Aster Yellows Phytoplasma in the Carrot (Daucus Carota L.) (Apiaceae) Cultivation Areas of Ankara and Konya Provinces, Türkiye”. Turkish Journal of Entomology, vol. 46, no. 4, 2023, pp. 385-98, doi:10.16970/entoted.1118787.
Vancouver Randa Zelyüt F, İnak E, Demir Özden E, Şenal D, Ertunç F. Determination of potential insect vectors and subgroups of aster yellows phytoplasma in the carrot (Daucus carota L.) (Apiaceae) cultivation areas of Ankara and Konya Provinces, Türkiye. TED. 2023;46(4):385-98.