Molecular characterization of Beet necrotic yellow vein virus isolates from sugar beet production areas of Türkiye according to coat protein gene
Yıl 2025,
Cilt: 13 Sayı: 1, 21 - 32, 15.06.2025
Ebru Erkan
,
Nazlı Dide Kutluk Yılmaz
Öz
Beet necrotic yellow vein virus (BNYVV), which is causes the disease known as 'rhizomania' and is transmitted by the soil-borne vector Polymyxa betae, is the most destructive and prevelant soil-borne virus in sugar beet production areas. In this study, 17 soil samples known to be infested with BNYVV were collected from different regions of Türkiye. Initially, BNYVV isolates were propagated using the bait plant test method. The coat protein (CP) gene is synthesized from the RNA-2 segment of BNYVV. In this study, nucleotide sequences of the CP gene region were obtained from 16 BNYVV isolates. BLAST analysis and phylogenetic tree comparisons with global isolates revealed that BNYVV isolates from Türkiye are located into two distinct groups. In the first group, IGR-9 and ERC-52 isolates exhibited an A (P) type CP structure, showing the highest similarity (99.65%) with HXL291CP-1 (China), Pithiviers (France), and IR-GR1 (Iran), respectively. Meanwhile, the remaining 14 BNYVV isolates in the second group showed the highest similarity (99.65%-100%) to A-type CP-containing isolates from Spain, the USA, and Serbia.
Proje Numarası
PYO.ZRT.1904.12.015 ve TOVAG: 110O188
Kaynakça
-
Abe H, Tamada T, 1986. Association of Beet necrotic yellow vein virus with isolates of Polymyxa betae Keskin. Japanese Journal of Phytopathology, 52, 235-247.
-
Biancardi E, Lewellen RT, 2016. Introduction: Pest and Diseases. Rhizomania. Biancardi, E. Tamada, T. (ed.), Switzerland, Springer.
-
Bragard C, Adkins S, Ali A, Gilmer D, Li D, Macfarlane S, Melcher U, Ratti C, Ryu KH, Wong SM, 2023. Rename all existing species in families Benyviridae and Virgaviridae to comply with the binomial species format. (https://ictv.global/taxonomy/taxondetails?
taxnode_id=202402733&taxon_name=Benyvirus%20necrobetae)
-
Chiba S, Kondo H, Miyanishi M, Andika IB, Han CG, Tamada T, 2011. The evolutionary history of beet necrotic yellow vein virus deduced from genetic variation, geographical origin and spread, and the breaking of host resistance. Mol. Plant-Microbe Interact, 24, 207-221.
-
Felsenstein J, 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17 (6), 368-376.
-
Gilmer D, Ratti C, 2017. ICTV Virus Taxonomy Profile: Benyviridae, Journal of General Virology, ICTV Report Consortium.
-
Kajiyama T, Yoshizawa A, Yoshida T, Yanagisawa A, Yoshimura Y, Ohtsuchi K, Abe H, Niura T, 1990. Response of sugar beet varieties to rhizomania disease of sugar beet. I. The yield and quality of sugar beet. Proceedings of Japanese Society of Sugar Beet Technologists, 32, 53-58.
-
Kaya R, 2009. Distribution of rhizomania disease in sugar beet growing areas of Turkey. Tarım Bilimleri Dergisi, 15 (4), 332-340.
-
Koch F, 1987. Bericht über eine in verschiedene zuckerrübenanbaugebiete der Turkseker in Anatolien und Thrazien zum stadium von wurzelerkrankungen. KWS Kleinwanzlebener Saatzucht, AG, Einbeck, Germany.
-
Koenig R, Jarausch W, Li Y, Commandeur U, Burgermeister W, Gehrke M, Luddecke P, 1991. Effect of recombinant beet necrotic yellow vein virus with different RNA compositions on mechanically inoculated sugar beets. Journal of General Virology, 72, 2243-2246.
-
Koenig R, Lüddecke P, Haeberle AM, 1995. Detection of beet necrotic yellow vein virus strains, variants and mixed infections by examining single-strand conformation polymorphisms of immunocapture RT-PCR products. Journal of General Virology, 76, 2051-2055.
-
Koenig R, Haeberle AM, Commandeur U, 1997. Detection and characterization of a distinct type of beet necrotic yellow vein virus RNA 5 in a sugar beet growing area in Europa. Archives of Virology, 142, 1499-1504.
-
Koenig R, Lennefors BL, 2000. Molecular analyses of European A, B and P type sources of Beet necrotic yellow vein virus and detection of the rare P type in Kazakhstan. Archives of Virology, 145, 1561- 1570.
-
Koenig R, Kastirr U, Holtschulte B, Deml G, Varrelmann M, 2008. Distribution of various types and P25 subtypes of Beet necrotic yellow vein virus in Germany and other European countries. Archives of Virology, 153, 2139-2144.
-
Kruse M, Koenig R, Hoffman A, Kaufmann A, Commandeur U, Solevyev AG, Savenkov I, Burgermeister W, 1994. Restriction fragment length polymorphism analysis of reverse transcription-PCR products reveals the existence of two major strain groups of Beet necrotic yellow vein virus. Journal of General Virology, 75, 1835-1842.
-
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, Sökmen, M, Erkan E, 2010. Orta Karadeniz Bölgesi şeker pancarı üretim alanlarından elde edilen Beet necrotic yellow vein virus izolatlarının moleküler farklılıklarının ve patojenitelerinin belirlenmesi. TÜBİTAK Hızlı Destek Projesi, TOVAG 108O585, Kesin Sonuç Raporu.
-
Kutluk Yılmaz 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, Arli-Sokmen 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.
-
Kutluk Yılmaz ND, Kaya R, Değer T, 2019. Beet necrotic yellow vein virus’ün patojenite ile ilişkili P25 proteininde delesyon belirlenen yeni varyantları üzerine araştırmalar. TÜBİTAK-TOVAG 215O495 No’lu Proje Kesin Sonuç Raporu, 206s.
-
Lennefors BL, Savenkov EI, Mukasa SB, Valkonen, JPT, 2004. Sequence divergence of four soilborne sugar beet-infecting viruses. Virus Genes, 31, 1, 57-64.
-
Li M, Liu T, Wang B, Han CG, Li DW, Yu JL, 2008. Phylogenetic analysis of Beet necrotic yellow vein virus isolates from China. Virus Genes, 36, 429-432.
-
Liebe S, Varrelmann M, 2022. Ongoing evaluation of Beet necrotic yellow vein virus towards Rz1-resistance breaking in Europe. Plant Pathology, 71, 1647-1659.
-
Meunier A, Schmit J-F, 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. App. Environ. Microbiol., 2356-2360.
-
Miyanishi M, Kusume T, Saito M, Tamada T, 1999. Evidence for three groups of sequence variants of Beet necrotic yellow vein virus RNA 5. Archives of Virology, 144, 879-892.
-
Nassaj Hosseini SM, Shams-Bakhsh M, Mehrvar M, Salmanian AH, 2013. Evolutionary characterization and genetic structure of Iranian isolates of Beet necrotic yellow vein virus population based on p25 protein. Journal of Agricultural Science and Technology, 15, 829-842.
-
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.
-
Rahim MD, Andika IB, Han C, Kondo H, Tamada T, 2007. RNA4-encoded P31 of Beet necrotic yellow vein virus is involved in efficient vector transmission, symptom severity and silencing suppression in roots. Journal of General Virology, 88, 1611-1619.
-
Rush CM, Heidel GB, 1995. Furovirus diseases of sugar beets in the United States. Plant Dis., 79 (9), 868-875.
-
Saito M, Kiguchi T, Kusume T, Tamada T, 1996. Complete nucleotide sequence of the Japanese isolate S of Beet necrotic yellow vein virus RNA and comparison with European isolates. Archives of Virology, 141, 2163-2175
-
Schirmer A, Link D, Cognat V, Beuve M, Meunier A, Bragard C, Gilmer D, Lemaire O, 2005. Phylogenetic analysis of isolates of Beet necrotic yellow vein virus collected worldwide. Journal of Gen. Virol., 86, 2897-2911.
-
Strausbaugh CA, 2018. Incidence, distribution, and pathogenicity of fungi causing root rot in Idaho long-term sugar beet storage piles. Plant Disease, 102, 2296-2307.
-
Strausbaugh CA, Eujayl IA, 2018. Influence of Beet necrotic yellow vein virus and freezing temperatures on sugar beet roots in storage. Plant Disease, 102, 932-937.
-
Tamada T, Abe H, 1989. Evidence that Beet necrotic yellow vein virus RNA-4 is essential for efficient transmission by the fungus Polymyxa betae. Journal of General Virology, 70, 3391-3398.
-
Tamada T, Shirako Y, Abe H, Saito M, Kiguchi T, Harada T, 1989. Production and pathogenicity of isolates of Beet necrotic yellow vein virus with different numbers of RNA components. Journal of General Virology, 70, 3399-3409.
-
Tamada T, Kusume T, Uchino H, Kiguchi T, Saito M, 1996. Evidence that Beet necrotic yellow vein virus RNA 5 is involved in symptom development of sugar beet roots. Proc. 3rd Symp. Int. Work. Group Plant Viruses Fungal Vectors, pp: 49-52.
-
Tamada T, 2002. Beet necrotic yellow vein virus. CMI/AAB description of plant viruses. Association of Applied Biologists. Wellesbourne UK.
-
Tamada T, Kondo H, Chiba S, 2016. "Genetic diversity of Beet necrotic yellow vein virus". Rhizomania. Editörler: Biancardi, E., Tamada, T. Switzerland: Springer.
-
Tamada, T., Uchino, H., Kusume, T., Iketani-Saito, M., Chiba, S., Andika, I. B. et al. (2021). Pathogenetic roles of beet necrotic yellow vein virus RNA5 in the exacerbation of symptoms and yield reduction, development of scab-like symptoms, and Rz1-resistance breaking in sugar beet. Plant Pathology, 70, 219-232.
-
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 progrosive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680.
-
Ward E, Koenig R, Budge G, Garrido C, McGrath C, Stubbley H, and Boonham, N. (2007). Occurrence of two different types of RNA-5 containing Beet necrotic yellow vein virus in the UK. Archives of Virology, 152, 59-73.
-
Von Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB, 2000. Virus Taxonomy. Classification and Nomenculture of Viruses, 7th Report of the International on Taxonomy of Viruses, Academic Press, pp: 904-922.
-
Yardımcı N, Çulal Kılıç H, 2011. Identification of Beet necrotic yellow vein virus in lakes district: A major beet growing area in Turkey. Indian Journal of Virology, 22 (2), 127-130.
-
Zhuo N, Jiang N, Zhang C, Zhang ZY, Zhang GZ, Han CG, Wang Y, 2015. Genetic diversity and population structure of Beet necrotic yellow vein virus in China. Virus Res., 205, 54-62.
Türkiye şeker pancarı üretim alanlarına ait Beet necrotic yellow vein virus izolatlarının kılıf protein genine göre moleküler karakterizasyonu
Yıl 2025,
Cilt: 13 Sayı: 1, 21 - 32, 15.06.2025
Ebru Erkan
,
Nazlı Dide Kutluk Yılmaz
Öz
Şeker pancarı üretim alanlarında sıklıkla rastlanan, en fazla zarar oluşturan toprak kökenli virüs türü Beet necrotic yellow vein virus (BNYVV) olup 'rhizomania' olarak bilinen hastalığa neden olmakta ve toprak kökenli vektör Polymyxa betae ile taşınmaktadır. Bu çalışmada, Türkiye’nin farklı bölgelerinden elde edilen ve BNYVV ile bulaşık olduğu daha önce belirlenen 17 toprak örneği kullanılmıştır. Öncelikle, tuzak bitki testi yöntemine göre BNYVV izolatlarının yeniden çoğaltımı sağlanmıştır. Kılıf protein (CP) geni BNYVV’nin RNA-2 segmentinden sentezlenmektedir. Bu çalışmada 16 BNYVV izolatının CP gen bölgesinin nükleotit dizileri elde edilmiştir. Bu izolatların dünya izolatları ile BLAST analizi ve elde edilen filogenetik analizler sonucu, ülkemize ait BNYVV izolatlarının iki farklı gruba ayrıldıkları saptanmıştır. İlk grupta yer alan IGR-9 ve ERC-52 izolatlarının, A (P) tipi CP yapısına sahip Çin, Fransa ve İran’a ait bahsedildiği sıraya göre, HXL291CP-1, Pithiviers ve IR-GR1 izolatlarıyla %99.65 oran ile en yüksek benzerliğe sahip olduğu belirlenmiştir. İkinci grupta yer alan diğer 14 BNYVV izolatı ise, A-tip karakterde CP içeren İspanya, ABD ve Sırbistan’a ait BNYVV izolatları ile en yüksek benzerlik göstermişlerdir (%99.65-%100).
Destekleyen Kurum
Ondokuz Mayıs Üniversitesi Proje Yönetim Ofisi ve TÜBİTAK
Proje Numarası
PYO.ZRT.1904.12.015 ve TOVAG: 110O188
Teşekkür
Bu çalışma, Ondokuz Mayıs Üniversitesi Proje Yönetim Ofisi (PYO.ZRT.1904.12.015) tarafından desteklenmiş olup, çalışmada kullanılan toprak örnekleri TÜBİTAK (TOVAG: 110O188) projesi kapsamında toplanmıştır.
Kaynakça
-
Abe H, Tamada T, 1986. Association of Beet necrotic yellow vein virus with isolates of Polymyxa betae Keskin. Japanese Journal of Phytopathology, 52, 235-247.
-
Biancardi E, Lewellen RT, 2016. Introduction: Pest and Diseases. Rhizomania. Biancardi, E. Tamada, T. (ed.), Switzerland, Springer.
-
Bragard C, Adkins S, Ali A, Gilmer D, Li D, Macfarlane S, Melcher U, Ratti C, Ryu KH, Wong SM, 2023. Rename all existing species in families Benyviridae and Virgaviridae to comply with the binomial species format. (https://ictv.global/taxonomy/taxondetails?
taxnode_id=202402733&taxon_name=Benyvirus%20necrobetae)
-
Chiba S, Kondo H, Miyanishi M, Andika IB, Han CG, Tamada T, 2011. The evolutionary history of beet necrotic yellow vein virus deduced from genetic variation, geographical origin and spread, and the breaking of host resistance. Mol. Plant-Microbe Interact, 24, 207-221.
-
Felsenstein J, 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17 (6), 368-376.
-
Gilmer D, Ratti C, 2017. ICTV Virus Taxonomy Profile: Benyviridae, Journal of General Virology, ICTV Report Consortium.
-
Kajiyama T, Yoshizawa A, Yoshida T, Yanagisawa A, Yoshimura Y, Ohtsuchi K, Abe H, Niura T, 1990. Response of sugar beet varieties to rhizomania disease of sugar beet. I. The yield and quality of sugar beet. Proceedings of Japanese Society of Sugar Beet Technologists, 32, 53-58.
-
Kaya R, 2009. Distribution of rhizomania disease in sugar beet growing areas of Turkey. Tarım Bilimleri Dergisi, 15 (4), 332-340.
-
Koch F, 1987. Bericht über eine in verschiedene zuckerrübenanbaugebiete der Turkseker in Anatolien und Thrazien zum stadium von wurzelerkrankungen. KWS Kleinwanzlebener Saatzucht, AG, Einbeck, Germany.
-
Koenig R, Jarausch W, Li Y, Commandeur U, Burgermeister W, Gehrke M, Luddecke P, 1991. Effect of recombinant beet necrotic yellow vein virus with different RNA compositions on mechanically inoculated sugar beets. Journal of General Virology, 72, 2243-2246.
-
Koenig R, Lüddecke P, Haeberle AM, 1995. Detection of beet necrotic yellow vein virus strains, variants and mixed infections by examining single-strand conformation polymorphisms of immunocapture RT-PCR products. Journal of General Virology, 76, 2051-2055.
-
Koenig R, Haeberle AM, Commandeur U, 1997. Detection and characterization of a distinct type of beet necrotic yellow vein virus RNA 5 in a sugar beet growing area in Europa. Archives of Virology, 142, 1499-1504.
-
Koenig R, Lennefors BL, 2000. Molecular analyses of European A, B and P type sources of Beet necrotic yellow vein virus and detection of the rare P type in Kazakhstan. Archives of Virology, 145, 1561- 1570.
-
Koenig R, Kastirr U, Holtschulte B, Deml G, Varrelmann M, 2008. Distribution of various types and P25 subtypes of Beet necrotic yellow vein virus in Germany and other European countries. Archives of Virology, 153, 2139-2144.
-
Kruse M, Koenig R, Hoffman A, Kaufmann A, Commandeur U, Solevyev AG, Savenkov I, Burgermeister W, 1994. Restriction fragment length polymorphism analysis of reverse transcription-PCR products reveals the existence of two major strain groups of Beet necrotic yellow vein virus. Journal of General Virology, 75, 1835-1842.
-
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, Sökmen, M, Erkan E, 2010. Orta Karadeniz Bölgesi şeker pancarı üretim alanlarından elde edilen Beet necrotic yellow vein virus izolatlarının moleküler farklılıklarının ve patojenitelerinin belirlenmesi. TÜBİTAK Hızlı Destek Projesi, TOVAG 108O585, Kesin Sonuç Raporu.
-
Kutluk Yılmaz 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, Arli-Sokmen 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.
-
Kutluk Yılmaz ND, Kaya R, Değer T, 2019. Beet necrotic yellow vein virus’ün patojenite ile ilişkili P25 proteininde delesyon belirlenen yeni varyantları üzerine araştırmalar. TÜBİTAK-TOVAG 215O495 No’lu Proje Kesin Sonuç Raporu, 206s.
-
Lennefors BL, Savenkov EI, Mukasa SB, Valkonen, JPT, 2004. Sequence divergence of four soilborne sugar beet-infecting viruses. Virus Genes, 31, 1, 57-64.
-
Li M, Liu T, Wang B, Han CG, Li DW, Yu JL, 2008. Phylogenetic analysis of Beet necrotic yellow vein virus isolates from China. Virus Genes, 36, 429-432.
-
Liebe S, Varrelmann M, 2022. Ongoing evaluation of Beet necrotic yellow vein virus towards Rz1-resistance breaking in Europe. Plant Pathology, 71, 1647-1659.
-
Meunier A, Schmit J-F, 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. App. Environ. Microbiol., 2356-2360.
-
Miyanishi M, Kusume T, Saito M, Tamada T, 1999. Evidence for three groups of sequence variants of Beet necrotic yellow vein virus RNA 5. Archives of Virology, 144, 879-892.
-
Nassaj Hosseini SM, Shams-Bakhsh M, Mehrvar M, Salmanian AH, 2013. Evolutionary characterization and genetic structure of Iranian isolates of Beet necrotic yellow vein virus population based on p25 protein. Journal of Agricultural Science and Technology, 15, 829-842.
-
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.
-
Rahim MD, Andika IB, Han C, Kondo H, Tamada T, 2007. RNA4-encoded P31 of Beet necrotic yellow vein virus is involved in efficient vector transmission, symptom severity and silencing suppression in roots. Journal of General Virology, 88, 1611-1619.
-
Rush CM, Heidel GB, 1995. Furovirus diseases of sugar beets in the United States. Plant Dis., 79 (9), 868-875.
-
Saito M, Kiguchi T, Kusume T, Tamada T, 1996. Complete nucleotide sequence of the Japanese isolate S of Beet necrotic yellow vein virus RNA and comparison with European isolates. Archives of Virology, 141, 2163-2175
-
Schirmer A, Link D, Cognat V, Beuve M, Meunier A, Bragard C, Gilmer D, Lemaire O, 2005. Phylogenetic analysis of isolates of Beet necrotic yellow vein virus collected worldwide. Journal of Gen. Virol., 86, 2897-2911.
-
Strausbaugh CA, 2018. Incidence, distribution, and pathogenicity of fungi causing root rot in Idaho long-term sugar beet storage piles. Plant Disease, 102, 2296-2307.
-
Strausbaugh CA, Eujayl IA, 2018. Influence of Beet necrotic yellow vein virus and freezing temperatures on sugar beet roots in storage. Plant Disease, 102, 932-937.
-
Tamada T, Abe H, 1989. Evidence that Beet necrotic yellow vein virus RNA-4 is essential for efficient transmission by the fungus Polymyxa betae. Journal of General Virology, 70, 3391-3398.
-
Tamada T, Shirako Y, Abe H, Saito M, Kiguchi T, Harada T, 1989. Production and pathogenicity of isolates of Beet necrotic yellow vein virus with different numbers of RNA components. Journal of General Virology, 70, 3399-3409.
-
Tamada T, Kusume T, Uchino H, Kiguchi T, Saito M, 1996. Evidence that Beet necrotic yellow vein virus RNA 5 is involved in symptom development of sugar beet roots. Proc. 3rd Symp. Int. Work. Group Plant Viruses Fungal Vectors, pp: 49-52.
-
Tamada T, 2002. Beet necrotic yellow vein virus. CMI/AAB description of plant viruses. Association of Applied Biologists. Wellesbourne UK.
-
Tamada T, Kondo H, Chiba S, 2016. "Genetic diversity of Beet necrotic yellow vein virus". Rhizomania. Editörler: Biancardi, E., Tamada, T. Switzerland: Springer.
-
Tamada, T., Uchino, H., Kusume, T., Iketani-Saito, M., Chiba, S., Andika, I. B. et al. (2021). Pathogenetic roles of beet necrotic yellow vein virus RNA5 in the exacerbation of symptoms and yield reduction, development of scab-like symptoms, and Rz1-resistance breaking in sugar beet. Plant Pathology, 70, 219-232.
-
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 progrosive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680.
-
Ward E, Koenig R, Budge G, Garrido C, McGrath C, Stubbley H, and Boonham, N. (2007). Occurrence of two different types of RNA-5 containing Beet necrotic yellow vein virus in the UK. Archives of Virology, 152, 59-73.
-
Von Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB, 2000. Virus Taxonomy. Classification and Nomenculture of Viruses, 7th Report of the International on Taxonomy of Viruses, Academic Press, pp: 904-922.
-
Yardımcı N, Çulal Kılıç H, 2011. Identification of Beet necrotic yellow vein virus in lakes district: A major beet growing area in Turkey. Indian Journal of Virology, 22 (2), 127-130.
-
Zhuo N, Jiang N, Zhang C, Zhang ZY, Zhang GZ, Han CG, Wang Y, 2015. Genetic diversity and population structure of Beet necrotic yellow vein virus in China. Virus Res., 205, 54-62.