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Türkiye şeker pancarı üretim alanlarından elde edilen Beet soil-borne virus izolatlarının kılıf protein genine göre moleküler karakterizasyonu

Year 2022, Volume: 10 Issue: 1, 10 - 18, 22.06.2022
https://doi.org/10.33409/tbbbd.1062915

Abstract

Şeker pancarı (Beta vulgaris L.), Türkiye'de şeker endüstrisinin hammaddesi olup, yaygın olarak yetiştirilmektedir. Pancar bitkisi, plazmodiophorid vektör Polymyxa betae tarafından taşınan bazı toprak kaynaklı virüsler tarafından enfekte edilmektedir. Taksonomik olarak Virgaviridae familyası içinde yer alan ve Pomovirus cinsine ait Beet soil-borne virus (BSBV) ve Beet virus Q (BVQ) şeker pancarında enfeksiyon oluşturan toprak kökenli virüs türleridir. Bu virüslerden BSBV, Türkiye'de ilk olarak 2003 yılında kayıt edilmiş ve daha sonra şeker pancarı üretim alanlarında oldukça yaygın olduğu (% 49.8) belirlenmiştir. Bu çalışmada, BSBV ile bulaşık 10 toprak örneği coğrafik orjinlerine göre rastgele seçilmiş ve bu toprak örneklerinden tuzak bitki testi yöntemiyle elde edilen izolatlar, moleküler yönden analiz edilmiştir. BSBV kılıf protein (CP) genine spesifik primerler ile uygulanan RT-PCR yöntemi ve elde edilen DNA ürünlerinin baz dizi analizi sonrasında, tüm BSBV izolatlarının CP bölgelerinin 495 nükleotit ve 164 amino asit (aa) içerdiği tespit edilmiştir. İlginç bir şekilde, farklı lokasyonlardan elde edilen 9 BSBV izolatı birbirleriyle karşılaştırıldığında, bu izolatların aa düzeyinde % 100 benzer oldukları saptanmıştır. Bununla birlikte, Yozgat ilinden elde edilen YZT-355S izolatının, diğer izolatlarla aa benzerlik oranının % 98.17 olduğu ve 92., 121. ve 122. pozisyonlarda yer alan aa’lerin diğer Türkiye izotları ve daha önce tanımlanan BSBV dünya izolatlarından farklılık sergilediği tespit edilmiştir. Bunun yanı sıra, 24 BSBV izolatının (bu çalışmadan 10 ve GenBank'tan 14) filogenetik analizi, tüm izolatların I, II, III ve IV olmak üzere dört ana grupta toplandığını göstermiştir. Grup I'e ait Türkiye izolatları iki alt gruba (alt grup a ve c) ayrılırken, diğer Türkiye izolatları grup III ve grup IV içerisinde yer almışlardır.

Supporting Institution

Ondokuz Mayıs Üniversitesi BAP (PYO.ZRT.1904.12.015)

Project Number

TÜBİTAK (TOVAG: 110O188)

Thanks

Bu çalışma, Ondokuz Mayıs Üniversitesi BAP (PYO.ZRT.1904.12.015) komisyonu tarafından desteklenmiş olup, çalışmada kullanılan toprak örnekleri TÜBİTAK (TOVAG: 110O188) projesi kapsamında toplanmıştır.

References

  • Adams MJ, Antoniv JF, Kreuze J, 2009. Virgaviridae: a new family of rod-shaped plant viruses. Archives of Virology, 154: 1967-1972.
  • Anonymous, 2020. Food and Agriculture Organization Statistics Division. Available from URL: https://www.fao.org/faostat/en/#data/QCL. (Erişim Tarihi: 20 Ocak 2022)
  • Barbarossa L, Vetten HJ, Kaufmann A, Lesemann DE, Koenig R, 1992. Monoclonal antibodies to beet soil-borne virus. Annals of Applied Biology, 121: 143-150.
  • Borodynko N, Rymelska N, Hasiow-Jaroszewska B, Pospieszny H, 2009. Molecular characterization of three soil-borne sugar beet-infecting viruses based on the coat protein gene. Journal of Plant Pathology, 91 (1): 191-193.
  • Camelo-Garcia VM, Rezende JAM, Nagata T, 2019. First report of beet soil-borne virus on red table beet in Brazil. Plant Disease, 103: 2146.
  • Crutzen F, Mehrvar M, Gilmer D, Bragard C, 2009. A full-length infectious clone of beet soil-borne virus indicates the dispensability of the RNA-2 for virus survival in planta and symptom expression on Chenopodium quioa leaves. Journal of General Virology, 90: 3051-3056.
  • Dijkstra J, De Jager CP. 1998. Practical Plant Virology. Protocols and Exercises. The Netherlands: Department of Virology, Wageningen Agricultural University.
  • Erkan E, Kutluk Yilmaz ND, 2017. Prevalence of Beet virus Q in sugar beet production areas of Turkey. Journal of Turkish Phytopathology, 46: 53-60.
  • Felsenstein, J., 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17 (6): 368-376.
  • Farzadfar S, Pourrahim R, Golnaraghi AR, Shahraeen N. 2002. First report of beet soil-borne virus on sugar beet in Iran. Plant Disease, 86: 187.
  • Gil JF, Adams I, Boonham N, Nielsen SL, Nicolaisen M, 2016. Molecular and biological characterization of two novel pomo-like viruses associated with potato (Solanum tuberosum) fields in Colombia. Archives of Virology, 161: 1601-1610.
  • Henry CM, Jones RAC, Coutts RHA, 1986. Occurrence of a soil-borne virus of sugar beet in England. Plant Pathology, 35: 585-591.
  • Ivanovic M, Macfarlane I, Woods RD, 1983. Viruses of sugar beet associated with Polymyxa betae. Ann. Rep. Rothamstead Exp. Stn., 189-190.
  • Koenig R, Beier C, Commandeur U, Lüth U, Kaufmann A, Lüddecke P, 1996. Beet soil-borne virus RNA-3- a further example of the heterogeneity of the gene content of furovirus genomes and of triple gene block- carrying RNAs. Virology, 216: 202-207.
  • Koenig, R., Loss, S., 1997. Soil-borne virus RNA-1: genetic analysis enabled by a starting sequence generated with primers to highly conserved helicase-encoding domains. Journal of General Virology, 78: 3161-3165. Koenig R, Commandeur U, Loss S, Beiner C, Kaufmann A, Lesemann DE, 1997. Soil-borne virus RNA-2: similarities and dissimilarities to the coat protein gene-carrying RNAs of other furoviruses. Journal of General Virology, 78: 469-477.
  • Koenig R, Pleij C WA, Beier C, Commandeur U, 1998. Genome properties of Beet virus Q, a new furo-like virus from sugar beet, determined from unpurified virus. Journal of General Virology, 79: 2027-2036.
  • Koenig R, Pleij CW, Büttner G, 2000. Structure and variability of the 3' end of beet soil-borne pomovirus: a virus with uncertain pathogenic effects. Archives of Virology, 145: 1173-1181.
  • Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33: 1870-1874.
  • Kutluk Yılmaz ND, Meunier A, Schmit JF, Stas A, Bragard C, 2007. Partial nucleotide sequence analysis of Turkish isolates of Beet necrotic yellow vein virus (BNYVV) RNA-3. Plant Pathology, 56: 311-316.
  • Kutluk Yılmaz ND, Arlı Sökmen M, 2010. Occurrences of sugar beet soilborne viruses transmitted by Polymyxa betae Northern and Central Parts of Turkey. Journal of Plant Pathology, 92 (2): 497-500.
  • Kutluk Yilmaz ND, Arli Sokmen M, Kaya R, Sevik MA, Tunali B, Demirtas S, 2016. The widespread occurrences of Beet soil-borne virus and RNA-5 containing Beet necrotic yellow vein virus isolates in sugar beet production areas in Turkey. European Journal of Plant Pathology, 144: 443-455.
  • Kutluk Yılmaz ND, Arlı-Sökmen M, Kaya R, 2018. P25 pathogenicity factor deletion mutants of Beet necrotic yellow vein virus occurring in sugar beet fields in Turkey. Journal of Plant Diseases and Protection, 125: 89-98.
  • Lennefors L, Savenkov EI, Mukasa SB, Valkonen JPT, 2005. Sequence divergence of four soilborne sugar beet-infecting viruses. Virus Genes 31: 57–64.
  • Lindsten, K, Rush CM, 1994. First report of Beet soilborne virus in the United States. Plant Disease, 78: 316. Lu X, Yamamoto S, Tanaka M, Hibi T, Namba S. 1998. The genome organization of the broad bean necrosis virus (BBNV). Archives of Virology, 143: 1335-1348.
  • McGrann GRD, Grimmer MK, Mutasa-Gottgens ES, Stevens M. 2009. Progress towards the understanding and control of sugar beet rhizomania diseases. Molecular Plant Pathology, 10: 129-141.
  • Mehrvar M, 2009. Diversity of soil-borne sugar beet viruses in Iran: a comprehensive study of Beet necrotic yellow vein virus, Beet black scorch virus and other pomoviruses in Iran. Ph.D. Thesis. Universite Catholique de Louvain, Belgium, 160 pp.
  • Meunier A, Schmit JF, Stas A, Kutluk N, Bragard C, 2003. Multiplex reverse transcription for simultaneous detection of Beet Necrotic Yellow Vein Virus, Beet Soilborne Virus, and Beet Virus Q and their vector Polymyxa betae KESKIN on sugar beet. Applied and Environmental Microbiology, 69 (4): 2356-2360.
  • Moradi Z, Maghdoori H, Nazifi E, Mehrvar M, 2021. Complete genomic characterization of two Beet soil-borne virus isolates from Turkey: Implications of comparative analysis of genome sequences. Plant Pathology Journal, 37 (2): 152-161.
  • Mouhanna AM, Nasrallah A, Langen G, Schlösser E. 2002. Surveys for beet necrotic yellow vein virus (the cause of Rhizomania), other viruses, and soil-borne fungi infecting sugar beet in Syria. Journal of Phytopathology, 150: 657-662.
  • Nakagami R, Chiba S, Yoshida N, Senoo Y, Saito M, Iketani S, Kondo H, Tamada T, 2022. Epidemic progress of beet necrotic yellow vein virus: Evidence from an investigation in Japan spanning half a century. Plant Pathology. 71:715-728.
  • Nouayti F, Tahiri A, Madani I, Blenzar A, Lahlali R, 2019. Detection and prevalence of viruses associated with sugar beet in the Tadla region of Morocco. Journal of Plant Pathology, 101: 173-177.
  • Özgür OE, 2003. Türkiye Şeker Pancarı Hastalıkları (1. Basım). Ankara: Türkiye Şeker Fabrikaları A.Ş. Genel Müdürlüğü Yayınları.
  • Özmen CY, Khabbazi SD, Khabbazi AD, Gürel S, Kaya R, Oğuz MÇ, Turan, F, Rezaei F, Kibar U, Gürel E, Ergül A, 2020. Genome composition analysis of multipartite BNYVV reveals of genetic re-assortment in the isolates of Asia Minor and Thrace. Scientific Reports, 10: 4129.
  • Savenkov, E, Sandragen M, Valkonen JPT, 1999. Complete sequence of RNA 1 and presence of tRNA-like structures in all RNAs of potato mop-top virus, genus Pomovirus. Journal of General Virology, 80: 2779-2784.
  • Savenkov E, 2021. Pomoviruses (Virgaviridae). In: Bamford, D.H, Zuckerman, M. (Eds.) Encyclopedia of Virology (Fourth Edition), Academic Press, Elsevier, Volume 3, pp. 603-611.
  • Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10: 512-526.
  • Thompson JD, Higgins DG, Gibson TJ, 1994. Clustal W: Improving the sensitivity of proggosive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22: 4673-4680.
  • Wang B, Li M, Zhang J, Han C, Li D, Yu J, 2008. First report of beet soil-borne virus on sugar beet in China. Plant Pathology, 57: 389.

Molecular characterization based on coat protein gene of Beet soil-borne virus isolates obtained from the soils of sugar beet growing areas in Turkey

Year 2022, Volume: 10 Issue: 1, 10 - 18, 22.06.2022
https://doi.org/10.33409/tbbbd.1062915

Abstract

Sugar beet (Beta vulgaris L.) is widely grown in Turkey as a raw material for the sugar industry. The beet plant is infected by some soil-borne viruses, which are transmitted by the plasmodiophorid vector Polymyxa betae Keskin. Among the members of the genus Pomovirus in the family Virgaviridae, Beet soil-borne virus (BSBV) and Beet virus Q (BVQ) only infect sugar beet. In Turkey, BSBV was the first reported in 2003 and then was found to be very common (49.8%) in the sugar beet production areas. In the current study, 10 BSBV-infested soil samples were randomly selected according to their geographic origin, and the isolates derived from the soil samples by bait plant technique were molecularly analyzed. RT-PCR performed using BSBV-CP specific primers and sequence analysis revealed that the CP regions of all Turkish BSBV isolates consisted of 495 nucleotides and 164 amino acid (aa) residues. Interestingly, 9 BSBV isolates obtained from different locations had the same aa identity (100%) when those isolates were compared with each other. However, the isolate YZT-355S obtained from Yozgat province shared 98.17% aa identity with the corresponding sequences of other isolates, and had differences at the 92., 121. and 122. aa positions of the CP region when compared with other Turkish and previously identified BSBV isolates in the world. Besides this, phylogenetic analysis of 24 BSBV isolates (10 from this study and 14 retrieved from GenBank) showed that all isolates were clustered in four main groups, I, II, III and IV. Turkish isolates belonged to group I were divided into two subgroup (subgroup a, c) while the other Turkish isolates were clustered into group III and group IV.

Project Number

TÜBİTAK (TOVAG: 110O188)

References

  • Adams MJ, Antoniv JF, Kreuze J, 2009. Virgaviridae: a new family of rod-shaped plant viruses. Archives of Virology, 154: 1967-1972.
  • Anonymous, 2020. Food and Agriculture Organization Statistics Division. Available from URL: https://www.fao.org/faostat/en/#data/QCL. (Erişim Tarihi: 20 Ocak 2022)
  • Barbarossa L, Vetten HJ, Kaufmann A, Lesemann DE, Koenig R, 1992. Monoclonal antibodies to beet soil-borne virus. Annals of Applied Biology, 121: 143-150.
  • Borodynko N, Rymelska N, Hasiow-Jaroszewska B, Pospieszny H, 2009. Molecular characterization of three soil-borne sugar beet-infecting viruses based on the coat protein gene. Journal of Plant Pathology, 91 (1): 191-193.
  • Camelo-Garcia VM, Rezende JAM, Nagata T, 2019. First report of beet soil-borne virus on red table beet in Brazil. Plant Disease, 103: 2146.
  • Crutzen F, Mehrvar M, Gilmer D, Bragard C, 2009. A full-length infectious clone of beet soil-borne virus indicates the dispensability of the RNA-2 for virus survival in planta and symptom expression on Chenopodium quioa leaves. Journal of General Virology, 90: 3051-3056.
  • Dijkstra J, De Jager CP. 1998. Practical Plant Virology. Protocols and Exercises. The Netherlands: Department of Virology, Wageningen Agricultural University.
  • Erkan E, Kutluk Yilmaz ND, 2017. Prevalence of Beet virus Q in sugar beet production areas of Turkey. Journal of Turkish Phytopathology, 46: 53-60.
  • Felsenstein, J., 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17 (6): 368-376.
  • Farzadfar S, Pourrahim R, Golnaraghi AR, Shahraeen N. 2002. First report of beet soil-borne virus on sugar beet in Iran. Plant Disease, 86: 187.
  • Gil JF, Adams I, Boonham N, Nielsen SL, Nicolaisen M, 2016. Molecular and biological characterization of two novel pomo-like viruses associated with potato (Solanum tuberosum) fields in Colombia. Archives of Virology, 161: 1601-1610.
  • Henry CM, Jones RAC, Coutts RHA, 1986. Occurrence of a soil-borne virus of sugar beet in England. Plant Pathology, 35: 585-591.
  • Ivanovic M, Macfarlane I, Woods RD, 1983. Viruses of sugar beet associated with Polymyxa betae. Ann. Rep. Rothamstead Exp. Stn., 189-190.
  • Koenig R, Beier C, Commandeur U, Lüth U, Kaufmann A, Lüddecke P, 1996. Beet soil-borne virus RNA-3- a further example of the heterogeneity of the gene content of furovirus genomes and of triple gene block- carrying RNAs. Virology, 216: 202-207.
  • Koenig, R., Loss, S., 1997. Soil-borne virus RNA-1: genetic analysis enabled by a starting sequence generated with primers to highly conserved helicase-encoding domains. Journal of General Virology, 78: 3161-3165. Koenig R, Commandeur U, Loss S, Beiner C, Kaufmann A, Lesemann DE, 1997. Soil-borne virus RNA-2: similarities and dissimilarities to the coat protein gene-carrying RNAs of other furoviruses. Journal of General Virology, 78: 469-477.
  • Koenig R, Pleij C WA, Beier C, Commandeur U, 1998. Genome properties of Beet virus Q, a new furo-like virus from sugar beet, determined from unpurified virus. Journal of General Virology, 79: 2027-2036.
  • Koenig R, Pleij CW, Büttner G, 2000. Structure and variability of the 3' end of beet soil-borne pomovirus: a virus with uncertain pathogenic effects. Archives of Virology, 145: 1173-1181.
  • Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33: 1870-1874.
  • Kutluk Yılmaz ND, Meunier A, Schmit JF, Stas A, Bragard C, 2007. Partial nucleotide sequence analysis of Turkish isolates of Beet necrotic yellow vein virus (BNYVV) RNA-3. Plant Pathology, 56: 311-316.
  • Kutluk Yılmaz ND, Arlı Sökmen M, 2010. Occurrences of sugar beet soilborne viruses transmitted by Polymyxa betae Northern and Central Parts of Turkey. Journal of Plant Pathology, 92 (2): 497-500.
  • Kutluk Yilmaz ND, Arli Sokmen M, Kaya R, Sevik MA, Tunali B, Demirtas S, 2016. The widespread occurrences of Beet soil-borne virus and RNA-5 containing Beet necrotic yellow vein virus isolates in sugar beet production areas in Turkey. European Journal of Plant Pathology, 144: 443-455.
  • Kutluk Yılmaz ND, Arlı-Sökmen M, Kaya R, 2018. P25 pathogenicity factor deletion mutants of Beet necrotic yellow vein virus occurring in sugar beet fields in Turkey. Journal of Plant Diseases and Protection, 125: 89-98.
  • Lennefors L, Savenkov EI, Mukasa SB, Valkonen JPT, 2005. Sequence divergence of four soilborne sugar beet-infecting viruses. Virus Genes 31: 57–64.
  • Lindsten, K, Rush CM, 1994. First report of Beet soilborne virus in the United States. Plant Disease, 78: 316. Lu X, Yamamoto S, Tanaka M, Hibi T, Namba S. 1998. The genome organization of the broad bean necrosis virus (BBNV). Archives of Virology, 143: 1335-1348.
  • McGrann GRD, Grimmer MK, Mutasa-Gottgens ES, Stevens M. 2009. Progress towards the understanding and control of sugar beet rhizomania diseases. Molecular Plant Pathology, 10: 129-141.
  • Mehrvar M, 2009. Diversity of soil-borne sugar beet viruses in Iran: a comprehensive study of Beet necrotic yellow vein virus, Beet black scorch virus and other pomoviruses in Iran. Ph.D. Thesis. Universite Catholique de Louvain, Belgium, 160 pp.
  • Meunier A, Schmit JF, Stas A, Kutluk N, Bragard C, 2003. Multiplex reverse transcription for simultaneous detection of Beet Necrotic Yellow Vein Virus, Beet Soilborne Virus, and Beet Virus Q and their vector Polymyxa betae KESKIN on sugar beet. Applied and Environmental Microbiology, 69 (4): 2356-2360.
  • Moradi Z, Maghdoori H, Nazifi E, Mehrvar M, 2021. Complete genomic characterization of two Beet soil-borne virus isolates from Turkey: Implications of comparative analysis of genome sequences. Plant Pathology Journal, 37 (2): 152-161.
  • Mouhanna AM, Nasrallah A, Langen G, Schlösser E. 2002. Surveys for beet necrotic yellow vein virus (the cause of Rhizomania), other viruses, and soil-borne fungi infecting sugar beet in Syria. Journal of Phytopathology, 150: 657-662.
  • Nakagami R, Chiba S, Yoshida N, Senoo Y, Saito M, Iketani S, Kondo H, Tamada T, 2022. Epidemic progress of beet necrotic yellow vein virus: Evidence from an investigation in Japan spanning half a century. Plant Pathology. 71:715-728.
  • Nouayti F, Tahiri A, Madani I, Blenzar A, Lahlali R, 2019. Detection and prevalence of viruses associated with sugar beet in the Tadla region of Morocco. Journal of Plant Pathology, 101: 173-177.
  • Özgür OE, 2003. Türkiye Şeker Pancarı Hastalıkları (1. Basım). Ankara: Türkiye Şeker Fabrikaları A.Ş. Genel Müdürlüğü Yayınları.
  • Özmen CY, Khabbazi SD, Khabbazi AD, Gürel S, Kaya R, Oğuz MÇ, Turan, F, Rezaei F, Kibar U, Gürel E, Ergül A, 2020. Genome composition analysis of multipartite BNYVV reveals of genetic re-assortment in the isolates of Asia Minor and Thrace. Scientific Reports, 10: 4129.
  • Savenkov, E, Sandragen M, Valkonen JPT, 1999. Complete sequence of RNA 1 and presence of tRNA-like structures in all RNAs of potato mop-top virus, genus Pomovirus. Journal of General Virology, 80: 2779-2784.
  • Savenkov E, 2021. Pomoviruses (Virgaviridae). In: Bamford, D.H, Zuckerman, M. (Eds.) Encyclopedia of Virology (Fourth Edition), Academic Press, Elsevier, Volume 3, pp. 603-611.
  • Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10: 512-526.
  • Thompson JD, Higgins DG, Gibson TJ, 1994. Clustal W: Improving the sensitivity of proggosive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22: 4673-4680.
  • Wang B, Li M, Zhang J, Han C, Li D, Yu J, 2008. First report of beet soil-borne virus on sugar beet in China. Plant Pathology, 57: 389.
There are 38 citations in total.

Details

Primary Language Turkish
Subjects Agricultural Engineering
Journal Section Articles
Authors

Ebru Erkan 0000-0001-7710-8042

Nazlı Kutluk Yılmaz 0000-0001-7331-9109

Project Number TÜBİTAK (TOVAG: 110O188)
Publication Date June 22, 2022
Published in Issue Year 2022 Volume: 10 Issue: 1

Cite

APA Erkan, E., & Kutluk Yılmaz, N. (2022). Türkiye şeker pancarı üretim alanlarından elde edilen Beet soil-borne virus izolatlarının kılıf protein genine göre moleküler karakterizasyonu. Toprak Bilimi Ve Bitki Besleme Dergisi, 10(1), 10-18. https://doi.org/10.33409/tbbbd.1062915
AMA Erkan E, Kutluk Yılmaz N. Türkiye şeker pancarı üretim alanlarından elde edilen Beet soil-borne virus izolatlarının kılıf protein genine göre moleküler karakterizasyonu. tbbbd. June 2022;10(1):10-18. doi:10.33409/tbbbd.1062915
Chicago Erkan, Ebru, and Nazlı Kutluk Yılmaz. “Türkiye şeker Pancarı üretim alanlarından Elde Edilen Beet Soil-Borne Virus izolatlarının kılıf Protein Genine göre moleküler Karakterizasyonu”. Toprak Bilimi Ve Bitki Besleme Dergisi 10, no. 1 (June 2022): 10-18. https://doi.org/10.33409/tbbbd.1062915.
EndNote Erkan E, Kutluk Yılmaz N (June 1, 2022) Türkiye şeker pancarı üretim alanlarından elde edilen Beet soil-borne virus izolatlarının kılıf protein genine göre moleküler karakterizasyonu. Toprak Bilimi ve Bitki Besleme Dergisi 10 1 10–18.
IEEE E. Erkan and N. Kutluk Yılmaz, “Türkiye şeker pancarı üretim alanlarından elde edilen Beet soil-borne virus izolatlarının kılıf protein genine göre moleküler karakterizasyonu”, tbbbd, vol. 10, no. 1, pp. 10–18, 2022, doi: 10.33409/tbbbd.1062915.
ISNAD Erkan, Ebru - Kutluk Yılmaz, Nazlı. “Türkiye şeker Pancarı üretim alanlarından Elde Edilen Beet Soil-Borne Virus izolatlarının kılıf Protein Genine göre moleküler Karakterizasyonu”. Toprak Bilimi ve Bitki Besleme Dergisi 10/1 (June 2022), 10-18. https://doi.org/10.33409/tbbbd.1062915.
JAMA Erkan E, Kutluk Yılmaz N. Türkiye şeker pancarı üretim alanlarından elde edilen Beet soil-borne virus izolatlarının kılıf protein genine göre moleküler karakterizasyonu. tbbbd. 2022;10:10–18.
MLA Erkan, Ebru and Nazlı Kutluk Yılmaz. “Türkiye şeker Pancarı üretim alanlarından Elde Edilen Beet Soil-Borne Virus izolatlarının kılıf Protein Genine göre moleküler Karakterizasyonu”. Toprak Bilimi Ve Bitki Besleme Dergisi, vol. 10, no. 1, 2022, pp. 10-18, doi:10.33409/tbbbd.1062915.
Vancouver Erkan E, Kutluk Yılmaz N. Türkiye şeker pancarı üretim alanlarından elde edilen Beet soil-borne virus izolatlarının kılıf protein genine göre moleküler karakterizasyonu. tbbbd. 2022;10(1):10-8.