Stolbur and Clover Proliferation Phytoplasma Infections in Tomato from Bingöl province, Turkey
Year 2020,
Volume: 7 Issue: 4, 855 - 866, 20.10.2020
Abdullah Güller
,
Mustafa Usta
Abstract
Phytoplasma-type symptoms were noted in tomato (Lycopersicum esculentum L.) in Bingöl province of Turkey. The remarkable symptoms include witch’s broom, rosetting, purple curled and crispy leaves, small leaves in the upper branches and excessively elongated calyx. Genomic DNA isolation was performed to identify possible pathogens from the leaves of 11 plants with and without symptom. In the Nested-PCR test performed using universal primer sets, DNA bands of approximately 1200 bp size were obtained in 4 of 11 samples. Randomly chosen two DNA bands primed R16F2n/R16R2 were cloned into an appropriate plasmid vector to further characterizations. The recombinant plasmid DNAs purified were sequenced in both directions. Molecular assays of the 16S rRNA sequence confirmed the existence of the “Canditatus Phytoplasma solani” (16SrXII-A group) (similarity coefficient 1.00) (Accession no: MT279680) and the “Canditatus Phytoplasma trifolii” (16SrVI-A group) (similarity coefficient 1.00) (Accession no: MT279852) in the infected tomato samples. The isolates associated with tomato-phytoplasma were named as ‘Bingöl D11’ and ‘Bingöl D90’ isolates, respectively. The phylogenetic dendrogram created also confirmed where both pathogens belong.
This current paper is documented in the first record of “Ca. P. solani” (16SrXII-A) and “Ca. P. trifolii” (16SrVI-A) in naturally diseased tomato in Bingol of Turkey.
References
- Afat, F. 2004. Çanakkale İlinde Domates Stolbur Hastalığının Yaygınlık Durumunun Belirlenmesi ve Hastalığın Aşı Yoluyla, Küskütle ve Tohumla Taşınma Oranlarının Saptanması. Y. Lisans Tezi. Çanakkale Üniversitesi, Ziraat Fakültesi, Bitki Koruma Bölümü. 58 sayfa.
- Alp, Ş., Usta, M., Sipahioğlu H.M., Güller A. 2016. “First report of “Canditatus Phytoplasma solani” on a new host marigold (Tagetes erecta L.)” Turkish Journal of Agriculture and Forestry, 40: 311-318.
- Al-Subhi, A.M., Hogenhout, S.A., Al-Yahyai, R.A., Al-Sadi, A.M. 2017. Classification of a new phytoplasma subgroup 16SrII-W associated with Crotalaria witches’ broom diseases in Oman based on multigene sequence analysis. BMC Microbiology, 17(1): 221 DOI 10.1186/s12866-017-1130-3.
- Alvarez, E., Mejía, J.F., Contaldo, N., Paltrinieri, S., Duduk, B., Bertaccini, A. 2014. ‘Canditatus Phytoplasma asteris’ strains associated with oil palm lethal wilt in Colombia. Plant Disease, 98: 311-318.
- Amaral-Mello, A.P., Bedendo, I.P., Kitajima, E.W., Ribeiro, .LF., Kobori, R. 2006. Tomato big bud associated with a phytoplasma belonging to group 16Sr III in Brazil, International Journal of Pest Management, 52 (3): 233-237.
- Anfoka, G., Khalil, AB., Fattash, I. 2003. Detection and Molecular Characterization of a Phytoplasma Associated with Big Bud Disease of Tomatoes in Jordan. Journal of Phytopathology, 151(4): 223-227.
- Arocha, Y., Antesana, O., Montellano, E., Franco, P., Plata, G., Jones, P. 2007. ‘Canditatus Phytoplasma lycopersici’, a phytoplasma associated with ‘hoja de perejil’ disease in Bolivia. International Journal of Systematic and Evolutionary Microbiology, 57: 1704–1710.
- Arocha, Y., López, M., Piñol, B., Fernández, M., Picornell, S., Almeida, R., Palenzuela, I., Wilson, M.R., Jones, P. 2005. ‘Canditatus Phytoplasma graminis’ and ‘Canditatus Phytoplasma caricae’, two novel phytoplasmas associated with diseases of sugarcane, weeds and papaya in Cuba. International Journal of Systematic and Evolutionary Microbiology, 55: 2451–2463.
- Azza, G.F., Eman, A.H.M. 2016. Detection of stolbur phytoplasma in tomato by a specific DNA hybridization. Research Journal of Biotechnology, 11 (6): 30-34.
- Belli, G., Bianco, P.A., Conti, M. 2010. Grapevine yellows in Italy: past, present and future. Journal of Plant Pathology, 92(2): 303-326.
- Bertaccini, A., Franova, J., Botti, S., Tabanelli, D. 2005 Molecular characterization of phytoplasmas in lilies with fasciation in the Czech Republic. FEMS Microbiology Letters, 249: 79–85.
- Bertaccini, A., Duduk, B., Paltrinieri, S., Contaldo, N. 2014. Phytoplasmas and phytoplasma diseases: a severe threat to agriculture. American Journal of Plant Sciences, 5: 1763–1788.
- Canik, D., Dikilitas, M., Ertunc, F. 2009. Molecular detection of Pear Decline Phytoplasma in pear trees and their biochemical responses. 87. In: Proceedings 21st Int Conference on Virus and Other Graft Transmissible Diseases of Fruit Crops, July, 5-10, Neustadt, Germany.
- Canik, D., Ertunc, F. 2007. Distribution and molecular characterization of Apple Proliferation phytoplasma in Turkey. Bulletin of Insectology, 60(2): 335-336.
- Canik, D., Ertunç, F., Paltrinieri, S., Contaldo, N., Bertaccini, A. 2011. Identification of different phytoplasmas infecting grapevine in Turkey. Bulletin of Insectology, 64: 225-S22.
- Contaldo, N, Bertaccini, A., Paltrinieri, S., Windsor, H.M., David Windsor, G. 2012. Axenic culture of plant pathogenic phytoplasmas. Phytopathologia Mediterranea, 51: 607–617.
- Çağlar, B.K., Elbeaino, T. 2013. A novel phytoplasma associated with witches’ broom disease of Ligustrum ovalifolium in Turkey. The Journal of Plant Pathology, 137: 113-117.
- Çağlar, B.K., Elbeaino, T., Küsek, M., Pehlivan, D., Fidan, H., Portakaldalı, M. 2010. Stolbur Phytoplasma Infections in Potato and Tomato Plants from Different Locations in Turkey. The Journal of Plant Pathology, 39: 1-3.
- Çağlayan, K., Gazel, M., Ulubaş Serçe, Ç., Bozkurt, I.A., Elçi, E. 2011. Phytoplasma diseases of stone fruit trees in Turkey and their containment. Phytopathogenic Mollicutes, 1(2): 95-97.
- Çarpar, H., Sertkaya, G. 2015. Doğu Akdeniz Bölgesi’nde Fitoplazma Hastalıklarının Durumu. Mustafa Kemal Üniversitesi Ziraat Fakültesi Dergisi, 20(2): 76-82.
- Davis, R., Zhao, Y., Dally, E.L., Lee I.M., Jomantiene, R., Douglas, S.M. 2013. ‘Canditatus Phytoplasma pruni’, a novel taxon associated with X-disease of stone fruits, Prunus spp.: multilocus characterization based on 16S rRNA, secY, and ribosomal protein genes. International Journal of Systematic and Evolutionary Microbiology, 63: 766-776.
- Davoodi, A., Panjekeh, N., Moslemkhani, K., Taheri, A. 2019. Detection and molecular characterization of tomato big bud disease in Qazvin province. Journal of Crop Protection, 8(4): 379-388.
- Del Serreno, P., Marzachì, C., Bragaloni, M., Galeffi, P. 2001. Phytoplasma infection of tomato in central Italy. Phytopathologia Mediterranea, 40: 137-142.
- Deng, S., Hiruki, C. 1991. Amplification of 16S rRNA gene genes from culturable and nonculturable mollicutes. The Journal of Microbiological Methods, 14: 53-61.
- Dong, J., Zhang, L., Li, W.H., Zhang, Z.K., McBeath, J.H. 2013. ‘Canditatus Phytoplasma aurantifolia’-related strain associated with tomato yellows disease in China. Journal of General Plant Pathology, 79(5). DOI: 10.1007/s10327-013-0463-5.
- Ember, I., Acs, Z., Munyaneza, JE., Crosslin, JM., Kolber, M. 2011. Survey and molecular detection of phytoplasmas associated with potato in Romania and southern. European Journal of Plant Pathology, 130(3): 367-377.
- Flower, C.E., Hayes-Plazolles, N., Slavicek, J.M. 2018. First Report of ‘Canditatus Phytoplasma trifolii’-Related Strain of 16SrVIA Phytoplasma Subgroup, Associated with Elm Yellows Disease in American Elm (Ulmus americana L.) in Ohio, U.S.A. Disease Notes, 102 (2): 438.
- Gazel, M., Çağlayan, K., Başpınar, H., Mejia, J.F., Paltrinieri, S., Bertaccini, A., Contaldo, N. 2016. Detection and Identification of Phytoplasmas in Pomegranate Trees with Yellows Symptoms. Journal of Phytopathology, 164: 136-140.
- Gazel, M., Ulubaş Serçe, Ç., Çağlayan, K., Öztürk, H. 2007. Detection of ‘Canditatus Phytoplasma pyri’ in Turkey. Bulletin of Insectology, 60 (2): 125-126.
Ghayeb Zamharir, M., Aldaghi, M, 2018. First report of a 'Canditatus Phytoplasma trifolii'-related strain associated with soybean bud proliferation and seed pod abortion in Iran. New Disease Reports, 37: 15. DOI: 10.5197/j.2044-0588.2018.037.015.
- Gopala, Rao GP. 2018. Molecular characterization of phytoplasma associated with four important ornamental plant species in India and identification of natural potential spread sources. 3 Biotech, 8(2):116. doi:10.1007/s13205-018-1126-1.
- Hiruki, C., Wang, K.R. 2004. Clover Proliferation Phytoplasma: ‘Canditatus Phytoplasma trifolii’. International Journal of Systematic and Evolutionary Microbiology, 54: 1349-1353.
- Hull, R. 1972. Mycoplasma and Plant Disease. PANS, 18 (2): 154-164.
- Jovic, J., Cvrkovic, T., Mitrovic, M., Krnjajic, S., Petrovic, A., Redinbaugh, M. G., Pratt, R. C., Hogenhout, S.A., Toševski, I. 2009. Stolbur phytoplasma transmission to maize by Reptalus panzeri and the disease cycle of maize redness in Serbia. Phytopathology, 99(9): 1053-1061.
- Kanatiwela-de Silva, C., Damayanthi, M., de Silva, N., Wijesekera, R., Dickinson, M., Weerakoon, D., Udagama, P. 2019. Immunological detection of the Weligama coconut leaf wilt disease associated phytoplasma: Development and validation of a polyclonal antibody based indirect ELISA. PLoS ONE, 14(4): e0214983.
- Krawczyk, K., Pospieszny, H., Kamasa, J. 2010. Identification of New Members of Canditatus Phytoplasma asteris Affecting Tomato Plants in Poland. Journal of Phytopathology, 158: 496–502.
- Kumari, S., Nagendran, K., Rai, A.B., Singh, B., Rao, G.P., Bertaccini, A. 2019. Global Status of Phytoplasma Diseases in Vegetable Crops. Frontiers in Microbiology, 10:1349. doi: 10.3389/fmicb.2019.01349.
- Lee, I.M., Gundersen-Rindal, D.E., Davis, R.E., Bartoszyk, I.M. 1998. Revised classification scheme of phytoplasmas based on RFLP analyses of 16S rRNA and ribosomal protein gene sequences. International Journal of Systematic and Evolutionary Microbiology, 48: 1153-1169.
- Liu, Z., Zhao, J., Liu, M. 2016. Photosynthetic responses to phytoplasma infection in Chinese jujube. Plant Physiology and Biochemistry, 105: 12–20.
- Lou, B., Bai, X., Bail Y., Deng, C., RoyChowdhury, M., Chen, C., Song, Y. 2013. Detection and Molecular Characterization of a 16SrII-A phytoplasma in Grapefruit (Citrus paradisi) with Huanglongbinglike Symptoms in China. Journal of Phytopathology, 162: 387-395.
- Mitrovic, M., Jakovljevic, M., Jovic, J., Krstic, O., Kosovac, A., Trivellone, V., Jermini, M., Toševski, I., Cvrkovic, T. 2016. 'Canditatus Phytoplasma solani' genotypes associated with potato stolbur in Serbia and the role of Hyalesthes obsoletus and Reptalus panzeri (Hemiptera, Cixiidae) as natural vectors. European Journal of Plant Pathology, 144(3): 619-630.
- Musetti, R., Buxa, S.V., De Marco, F., Loschi, A., Polizzotto, R., Kogel, K.H., van Bel A.J. 2013. Phytoplasma-triggered Ca2+ influx is involved in sieve-tube blockage. Molecular Plant-Microbe Interactions, 26: 379–386.
- Nogay, A., Ternar, Ş. 1986. Marmara Bölgesi’nde Domateslerde Görülen Stolbur Hastalığı Üzerinde Araştırmalar. E107.845 No’lu Proje Nihai Raporu. Ziraai Araştırma Enstitüsü. İSTANBUL.
- Nogay, A., Ternar, Ş., Ünal, E. 1988. Marmara Bölgesinde Domateslerde Görülen Stolbur Hastalığı Üzerinde Araştırmalar. Bitki Koruma Bülteni, 28 (1-2): 79-98.
- Oksal, H.D., Apak, F.K., Oksal, E., Tursun, N., Sipahioğlu, H.M. 2017. Detection and molecular characterization of two 'Canditatus Phytoplasma trifolii' isolates infecting peppers at the same ecological niche. International Journal of Agriculture and Biology, 19(6): 1372-1378.
- Olivier, C., Séguin-Swartz, G., Galka, B., Olfert, O. 2011. Aster yellows in leafhoppers and field crops in Saskatchewan, Canada, 2001–2008. The Americas Journal of Plant Science and Biotechnology, 141: 425–462.
- Olmos, A., Cambra, M., Esteban, O., Gorris, M.T., Terrada, E. 1999. New device and method for capture, reverse transcription and nested PCR in a single closed tube. Nucleic Acids Research, 27: 1564-1565.
- Oshima, K., Maejima, K., Namba, S. 2013. Genomic and evolutionary aspects of phytoplasmas. Frontiers in Microbiology, 4: 230.
- Özdemir, N., Saygılı, H. 2012. A Study On The Transmission With The Seed Of Stolbur Disease In Western Anatolia Tomato Areas. Journal of Agricultural Faculty of Uludag University. 26 (1): 63-72.
- Özdemir, N. 2008. Batı Anadolu bölgesi domates üretim alanlarında görülen stolbur hastalığının yaygınlığının belirlenmesi, tanılanması ve taşınma yolları üzerinde çalışmalar. Doktora tezi, Ege Üniversitesi, Ziraat Fakültesi, Bitki Koruma Bölümü, 133 sayfa.
- Özdemir, N., Saygılı, H., Sahin, F., Karsavuran, Y., Bayrak, O.F., Oral, B. 2007. Host range and genetic characterization of a phytoplasma causing tomato stolbur disease in Turkey. Second International Symposium on Tomato Diseases (8-12 October, 2007, Kusadası, Turkey) Program and Abstract Book, p. 67.
- Özdemir, Z. 2017. “Phytoplasmas of sesame and Orosius orientalis are genetically diverse based on 16S rDNA sequencing and PCR-RFLP in Turkey”, Archives of Phytopathology and Plant Protection, 50 (13-14): 674-686.
- Pérez-López, E., Dumonceaux, T. J., Olivier, C. Y., LunaRodríguez, M. 2014. Identification of ‘Canditatus phytoplasma phoenicium’ in periwinkle from Cuba. Revista Mexexicana de Fitopatología, 32: 47.
- Pracros, P., Renaudin, J., Eveillard, S., Mouras, A., Hernould, M. 2006. Tomato Flower Abnormalities Induced by Stolbur Phytoplasma Infection Are Associated with Changes of Expression of Floral Development Genes. Molecular Plant-Microbe Interactions, 19(1): 62-68.
- Quaglino, F., Zhao, Y., Casati, P., Bulgari, D., Bianco, P.A., Wei, W., Davis, R.E. 2013. 'Canditatus Phytoplasma solani', a novel taxon associated with stolbur- and bois noir-related diseases of plants. International Journal of Systematic and Evolutionary Microbiology, 63(8): 2879- 2894.
- Reveles‐Torres, L.R., Velásquez‐Valle, R., Salas‐Muñoz, S., Mauricio‐Castillo, J.A., Caren, K., Esqueda‐Dávila, J., Herrera, M.D. 2018. Canditatus Phytoplasma trifolii (16SrVI) infection modifies the polyphenols concentration in pepper (Capsicum annuum) plant tissues. Journal of Phytopathology, DOI: 10.1111/jph.12717.
- Sahtiyancı, Ş. 1972. Marmara Bölgesi virus vektörleri üzerine araştırmalar. Zirai Mücadele Araştırma Yıllıkları, 113-114.
- Salehi, M., Izadpanah, K., Siampour, M. 2008. First Report of 'Canditatus Phytoplasma trifolii'-Related Strain Associated with Safflower Phyllody Disease in Iran. Plant Disease. 92(4): 649.
- Santos-Cervantesa, M.E., Chávez-Medinaa, J.A., Fierro-Coronadoa, J.A., Ruelas-Ayalaa, R.D., Barreras-Sotoa, M.A., Méndez-Lozanoa, J., Leyva-Lópeza, N.E. 2007. First report of Canditatus ‘Phytoplasma asteris’ infecting tomatillo (Physalis ixocarpa) in Sinaloa, México. Plant Pathology, 56: 721
- Schneider, B., Cousin, M., Klinkong, S., Seemüller, E. 1995. Taxonomic relatedness and phylogenetic positions of phytoplasmas associated with diseases of faba bean, sunhemp, sesame, soybean and eggplant. Z Pflanzenkr Pflanzenschutz, 102: 225–232.
- Schneider, B., Gibb, K.S., Padovan, A.C., Davis, R.I., De La Rue, S. 1999. Comparison and characterisation of tomato big bud and sweet potato little leaf-group phytoplasmas. Journal of Phytopathology, 147: 31–40.
- Seemuller, E., Kiss, E., Sule, S., Schneider, B. 2010. Multiple infection of apple trees by distinct strains of ‘Canditatus Phytoplasma mali’ and its pathological relevance. Phytopathology, 100: 863–870.
- Serçe, Ç.U., Yılmaz, S. 2019. First report of ‘Canditatus Phytoplasma trifolii’ (16SrVI group) infecting cabbage (Brassica oleracea) in Turkey. Journal of Plant Pathology, https://doi.org/10.1007/s42161-019-00443-y.
- Sertkaya, G., Martini, M., Musetti, R., Osler, R. 2007. Detection and molecular characterization of phytoplasmas infecting sesame and solanaceous crops in Turkey. Bulletin of Insectology, 60: 141‒142.
- Shahryari, F., Allahverdipour, T., Rabiei, Z. 2019. Phytoplasmas associated with grapevine yellows disease in Iran: first report of a 'Canditatus Phytoplasma trifolii'-related strain and further finding of a 'Ca. P. solani'-related strain. New Disease Reports, 40: 17.
- Shaw, M.E., Kirkpatrick B.C. 1993. The beet leafhopper-transmitted virescence agent causes tomato big bud disease in California. Plant Disease, 77: 290‒295.
- Singh, J., Rani, A., Kumar, P., Baranwal, V.K., Saroj, P.L, Sirohi, A. 2012. First report of a 16SrII-D phytoplasma 'Canditatus Phytoplasma australasia' associated with a tomato disease in India. New Disease Reports, 26: 14.
- Şahin, F., Özdemir, N., Oral, B., Saygılı, H., Karsavuran, Y., Bayrak, O.F. 2007. Identification of a phytoplasma causing tomato stolbur disease in Turkey. APS. SON. Joint Meeting. Phytopathology S103. July 28- August 1.
- Tanrıkut, S. 1953. Domates yetiştiriciliği için tehlikeli bir hastalık. Bitki Koruma Bülteni, 5: 22-28.
- Tsplenkov, E.E., Fedotina V.L. 1973. Nature and classification of two forms of Tomato Stolbur. Biologlcheskie. Havkl 16: 100-106 (Rev. Pl. Path., 52: 4217).
- Ulubas-Serce, C., Gazel, M., Caglayan, K., Bas, M., Son, L. 2006. Phytoplasma diseases of fruit trees in germplasm and commercial orchards. EPPO Bulletin, 36: 216-217.
- Ulubas-Serce, C., Kaya, K., Gazel, M., Caglayan, K., Sauvion, N. 2012. Psyllid vectors of AP Group (16SrX) phytoplasmas infecting grapevine in Turkey. 104. In: Book of Abstracts, 22th International Conference on Virus and Other Graft Transmissible Diseases of Fruit Crops, 3-8 June, Rome. 38.
- Ulubaş Serçe, Ç., Yılmaz, S. 2019. First report of ‘Canditatus Phytoplasma trifolii’ (16SrVI group) infecting cabbage (Brassica oleracea) in Turkey. Journal of Plant Pathology, https://doi.org/10.1007/s42161-019-00443-y.
- Usta, M., Güller, A., Sipahioğlu, H.M. 2017. Detection and Characterization of two Phytoplasma lineages on Cucumber (Cucumis sativus L.) with Same Symptomatology based on Virtual RFLP and Nucleotide Sequence Analysis of 16S rDNA. Yuzuncu Yil University Journal of Agricultural Sciences, 27(3): 299-308.
- Usta, M., Güller, A., Sipahioğlu, H.M. 2018. Molecular analysis of „ Canditatus Phytoplasma trifolii‟ and, Canditatus Phytoplasma solani‟ associated with phytoplasma diseases of tomato (PDT) in Turkey. International Journal of Agriculture and Biology, 20: 1991-1996.
- Valente, V., Musil M., Misiga S. 1961. Investlgations of European yellow styp viruses 1. the stolbur virus. Phytopathology, 42: 1-38.
- Vellios, E., Lioliopoulou, F. 2007. Detection and characterization of phytoplasmas infecting tomato plants in Greece. Bulletin of Insectology. 60(2): 157-158.
- Wei, W., Davis, R.E, Lee, I.M., Zhao, Y. 2007. Computer simulated RFLP analysis of 16S rRNA genes: identification of ten new phytoplasma groups. International Journal of Systematic and Evolutionary Microbiology, 57: 1855-1867.
- Weintraub, P.G, Beanland, L. 2006. Insect vectors of phytoplasmas. Annual Review of Entomology, 51: 91–111.
- Weintraub, P.G, Jones, P. 2009. Phytoplasmas, Genomes, Plant Hosts and Vectors. Cab International, United Kingdom. 10.1079/9781845935306.0000.
- Weisburg, W.G., Tully, J.G., Rose, D.L., Petzel, J.P., Oyaizu, H., Yang, D., Mandelco, L., Sechrest, J., Lawrence, T.G., Van Etten, J. 1989. A phylogenetic analysis of the mycoplasmas: basis for their classification. Journal of Bacteriology, 171: 6455-6467.
- Wu, Y., Hao, X., Li, Z., Gu, P., An, F., Xiang, J., Wang, H., Luo, Z., Liu, J., Xiang, Y. 2010. Identification of the phytoplasma associated with wheat blue dwarf disease in China. Plant Disease. 94: 977-985.
- Xu, X., Mou, H.Q., Zhu, S.F., Liao, X.L., Zhao, W.J. 2013. Detection and Characterization of Phytoplasma Associated with Big Bud Disease of Tomato in China. Journal of Phytopathology, 161: 430–433.
- Yavuz, Ş., Gazel, M., Çağlayan, K. 2019. Determination of apple proliferation phytoplasma disease (Canditatus Phytoplasma mali) in apple orchards in Adana and İçel provinces. Mustafa Kemal University Journal of Agricultural Sciences, 24 (1): 15-20.
- Yorgancı, Ü., Öncüer, C., Karsavuran, Y. 1991. “Batı Anadolu sanayi domatesi yetiştirme alanlarında stolbur hastalığının yaygınlık oranı ve ortaya çıkış nedenleri üzerinde araştırmalar, s. 315-319”. VI. Türkiye Fitopatoloji Kongresi (7-11 Ekim 1991, İzmir) Bildirileri, Türkiye Fitopatoloji Derneği Yayınları No. 6, 434 s.
- Zambon, Y., Canel, A., Bertaccini, A., Contaldo, N. 2018. Molecular Diversity of Phytoplasmas Associated with Grapevine Yellows Disease in North-Eastern Italy. Phytopathology, 108(2): 206-214.
- Zhang, L., Li, Z., Du, C., Fu, Z., Wu, Y. 2012. Detection and Identification of Group 16SrVI Phytoplasma in Willows in China. Journal of Phytopathology, 160: 755-757.
- Zhao, Y., Wei W., Lee I.M., Shao J., Suo X., Davis R.E. 2009. Construction of an interactive online phytoplasma classification tool, iPhyClassifier, and its application in analysis of the peach X-disease phytoplasma group (16SrIII). International Journal of Systematic and Evolutionary Microbiology, 59: 2582-2593.
Stolbur and Clover Proliferation Phytoplasma Infections in Tomato from Bingöl province, Turkey
Year 2020,
Volume: 7 Issue: 4, 855 - 866, 20.10.2020
Abdullah Güller
,
Mustafa Usta
Abstract
Bingöl ilinde yetiştiriciliği yapılan domates (Lycopersicum esculentum L.) tarlalarında fitoplazma benzeri belirtiler görülmüştür. Dikkat çeken belirtiler arasında cadı süpürgesi, rozetleme, mor renkli kıvrılmış ve gevrek yapraklar, üst dallarda küçük yapraklılık ve aşırı uzamış kaliks yer almaktadır. Toplanan 8 simptomlu ve simptomsuz bitkinin yapraklarından muhtemel patojeni belirleyebilmek için genomic DNA izolasyonu yapıldı. Universal primer setleri kullanılarak gerçekleştirilen Nested-PCR testinde, 8 örneğin 4’ünde beklenen yaklaşık 1200 bp büyüklüğünde DNA bandları elde edilmiştir. R16F2n/R16R2 primerleri ile band veren örneklerden rastgele ikisi seçilerek uygun bir plasmid vektörde klonlanmıştır. Saflaştırılan rekombinant plasmid DNA’sı çift yönlü olarak dizilenmiştir. 16S rDNA dizisinin moleküler analizleri, infekteli domates örneklerinde ‘Canditatus Phytoplasma solani’ (16SrXII-A grup) (benzerlik katsayısı 1.00) (Ulaşım no: MT279680) ve ‘Canditatus Phytoplasma trifolii’(16SrVI-A grup) (benzerlik katsayısı 1.00) (Ulaşım no: MT279852) doğrulamıştır. Domates fitoplazma ile ilişkili izolatlar ‘Bingöl D11’ diğerine ise ‘Bingöl D90’ izolatı olarak isimlendirilmiştir. Oluşturulan filogenetik dendrogram da her iki patojenin ait olduğu yeri doğrulamıştır.
Mevcut bu çalışma Bingöl ilinde domatesi doğal olarak enfekte eden "Ca. P. solani" ve "Ca. P. trifolii" nin ilk raporudur.
References
- Afat, F. 2004. Çanakkale İlinde Domates Stolbur Hastalığının Yaygınlık Durumunun Belirlenmesi ve Hastalığın Aşı Yoluyla, Küskütle ve Tohumla Taşınma Oranlarının Saptanması. Y. Lisans Tezi. Çanakkale Üniversitesi, Ziraat Fakültesi, Bitki Koruma Bölümü. 58 sayfa.
- Alp, Ş., Usta, M., Sipahioğlu H.M., Güller A. 2016. “First report of “Canditatus Phytoplasma solani” on a new host marigold (Tagetes erecta L.)” Turkish Journal of Agriculture and Forestry, 40: 311-318.
- Al-Subhi, A.M., Hogenhout, S.A., Al-Yahyai, R.A., Al-Sadi, A.M. 2017. Classification of a new phytoplasma subgroup 16SrII-W associated with Crotalaria witches’ broom diseases in Oman based on multigene sequence analysis. BMC Microbiology, 17(1): 221 DOI 10.1186/s12866-017-1130-3.
- Alvarez, E., Mejía, J.F., Contaldo, N., Paltrinieri, S., Duduk, B., Bertaccini, A. 2014. ‘Canditatus Phytoplasma asteris’ strains associated with oil palm lethal wilt in Colombia. Plant Disease, 98: 311-318.
- Amaral-Mello, A.P., Bedendo, I.P., Kitajima, E.W., Ribeiro, .LF., Kobori, R. 2006. Tomato big bud associated with a phytoplasma belonging to group 16Sr III in Brazil, International Journal of Pest Management, 52 (3): 233-237.
- Anfoka, G., Khalil, AB., Fattash, I. 2003. Detection and Molecular Characterization of a Phytoplasma Associated with Big Bud Disease of Tomatoes in Jordan. Journal of Phytopathology, 151(4): 223-227.
- Arocha, Y., Antesana, O., Montellano, E., Franco, P., Plata, G., Jones, P. 2007. ‘Canditatus Phytoplasma lycopersici’, a phytoplasma associated with ‘hoja de perejil’ disease in Bolivia. International Journal of Systematic and Evolutionary Microbiology, 57: 1704–1710.
- Arocha, Y., López, M., Piñol, B., Fernández, M., Picornell, S., Almeida, R., Palenzuela, I., Wilson, M.R., Jones, P. 2005. ‘Canditatus Phytoplasma graminis’ and ‘Canditatus Phytoplasma caricae’, two novel phytoplasmas associated with diseases of sugarcane, weeds and papaya in Cuba. International Journal of Systematic and Evolutionary Microbiology, 55: 2451–2463.
- Azza, G.F., Eman, A.H.M. 2016. Detection of stolbur phytoplasma in tomato by a specific DNA hybridization. Research Journal of Biotechnology, 11 (6): 30-34.
- Belli, G., Bianco, P.A., Conti, M. 2010. Grapevine yellows in Italy: past, present and future. Journal of Plant Pathology, 92(2): 303-326.
- Bertaccini, A., Franova, J., Botti, S., Tabanelli, D. 2005 Molecular characterization of phytoplasmas in lilies with fasciation in the Czech Republic. FEMS Microbiology Letters, 249: 79–85.
- Bertaccini, A., Duduk, B., Paltrinieri, S., Contaldo, N. 2014. Phytoplasmas and phytoplasma diseases: a severe threat to agriculture. American Journal of Plant Sciences, 5: 1763–1788.
- Canik, D., Dikilitas, M., Ertunc, F. 2009. Molecular detection of Pear Decline Phytoplasma in pear trees and their biochemical responses. 87. In: Proceedings 21st Int Conference on Virus and Other Graft Transmissible Diseases of Fruit Crops, July, 5-10, Neustadt, Germany.
- Canik, D., Ertunc, F. 2007. Distribution and molecular characterization of Apple Proliferation phytoplasma in Turkey. Bulletin of Insectology, 60(2): 335-336.
- Canik, D., Ertunç, F., Paltrinieri, S., Contaldo, N., Bertaccini, A. 2011. Identification of different phytoplasmas infecting grapevine in Turkey. Bulletin of Insectology, 64: 225-S22.
- Contaldo, N, Bertaccini, A., Paltrinieri, S., Windsor, H.M., David Windsor, G. 2012. Axenic culture of plant pathogenic phytoplasmas. Phytopathologia Mediterranea, 51: 607–617.
- Çağlar, B.K., Elbeaino, T. 2013. A novel phytoplasma associated with witches’ broom disease of Ligustrum ovalifolium in Turkey. The Journal of Plant Pathology, 137: 113-117.
- Çağlar, B.K., Elbeaino, T., Küsek, M., Pehlivan, D., Fidan, H., Portakaldalı, M. 2010. Stolbur Phytoplasma Infections in Potato and Tomato Plants from Different Locations in Turkey. The Journal of Plant Pathology, 39: 1-3.
- Çağlayan, K., Gazel, M., Ulubaş Serçe, Ç., Bozkurt, I.A., Elçi, E. 2011. Phytoplasma diseases of stone fruit trees in Turkey and their containment. Phytopathogenic Mollicutes, 1(2): 95-97.
- Çarpar, H., Sertkaya, G. 2015. Doğu Akdeniz Bölgesi’nde Fitoplazma Hastalıklarının Durumu. Mustafa Kemal Üniversitesi Ziraat Fakültesi Dergisi, 20(2): 76-82.
- Davis, R., Zhao, Y., Dally, E.L., Lee I.M., Jomantiene, R., Douglas, S.M. 2013. ‘Canditatus Phytoplasma pruni’, a novel taxon associated with X-disease of stone fruits, Prunus spp.: multilocus characterization based on 16S rRNA, secY, and ribosomal protein genes. International Journal of Systematic and Evolutionary Microbiology, 63: 766-776.
- Davoodi, A., Panjekeh, N., Moslemkhani, K., Taheri, A. 2019. Detection and molecular characterization of tomato big bud disease in Qazvin province. Journal of Crop Protection, 8(4): 379-388.
- Del Serreno, P., Marzachì, C., Bragaloni, M., Galeffi, P. 2001. Phytoplasma infection of tomato in central Italy. Phytopathologia Mediterranea, 40: 137-142.
- Deng, S., Hiruki, C. 1991. Amplification of 16S rRNA gene genes from culturable and nonculturable mollicutes. The Journal of Microbiological Methods, 14: 53-61.
- Dong, J., Zhang, L., Li, W.H., Zhang, Z.K., McBeath, J.H. 2013. ‘Canditatus Phytoplasma aurantifolia’-related strain associated with tomato yellows disease in China. Journal of General Plant Pathology, 79(5). DOI: 10.1007/s10327-013-0463-5.
- Ember, I., Acs, Z., Munyaneza, JE., Crosslin, JM., Kolber, M. 2011. Survey and molecular detection of phytoplasmas associated with potato in Romania and southern. European Journal of Plant Pathology, 130(3): 367-377.
- Flower, C.E., Hayes-Plazolles, N., Slavicek, J.M. 2018. First Report of ‘Canditatus Phytoplasma trifolii’-Related Strain of 16SrVIA Phytoplasma Subgroup, Associated with Elm Yellows Disease in American Elm (Ulmus americana L.) in Ohio, U.S.A. Disease Notes, 102 (2): 438.
- Gazel, M., Çağlayan, K., Başpınar, H., Mejia, J.F., Paltrinieri, S., Bertaccini, A., Contaldo, N. 2016. Detection and Identification of Phytoplasmas in Pomegranate Trees with Yellows Symptoms. Journal of Phytopathology, 164: 136-140.
- Gazel, M., Ulubaş Serçe, Ç., Çağlayan, K., Öztürk, H. 2007. Detection of ‘Canditatus Phytoplasma pyri’ in Turkey. Bulletin of Insectology, 60 (2): 125-126.
Ghayeb Zamharir, M., Aldaghi, M, 2018. First report of a 'Canditatus Phytoplasma trifolii'-related strain associated with soybean bud proliferation and seed pod abortion in Iran. New Disease Reports, 37: 15. DOI: 10.5197/j.2044-0588.2018.037.015.
- Gopala, Rao GP. 2018. Molecular characterization of phytoplasma associated with four important ornamental plant species in India and identification of natural potential spread sources. 3 Biotech, 8(2):116. doi:10.1007/s13205-018-1126-1.
- Hiruki, C., Wang, K.R. 2004. Clover Proliferation Phytoplasma: ‘Canditatus Phytoplasma trifolii’. International Journal of Systematic and Evolutionary Microbiology, 54: 1349-1353.
- Hull, R. 1972. Mycoplasma and Plant Disease. PANS, 18 (2): 154-164.
- Jovic, J., Cvrkovic, T., Mitrovic, M., Krnjajic, S., Petrovic, A., Redinbaugh, M. G., Pratt, R. C., Hogenhout, S.A., Toševski, I. 2009. Stolbur phytoplasma transmission to maize by Reptalus panzeri and the disease cycle of maize redness in Serbia. Phytopathology, 99(9): 1053-1061.
- Kanatiwela-de Silva, C., Damayanthi, M., de Silva, N., Wijesekera, R., Dickinson, M., Weerakoon, D., Udagama, P. 2019. Immunological detection of the Weligama coconut leaf wilt disease associated phytoplasma: Development and validation of a polyclonal antibody based indirect ELISA. PLoS ONE, 14(4): e0214983.
- Krawczyk, K., Pospieszny, H., Kamasa, J. 2010. Identification of New Members of Canditatus Phytoplasma asteris Affecting Tomato Plants in Poland. Journal of Phytopathology, 158: 496–502.
- Kumari, S., Nagendran, K., Rai, A.B., Singh, B., Rao, G.P., Bertaccini, A. 2019. Global Status of Phytoplasma Diseases in Vegetable Crops. Frontiers in Microbiology, 10:1349. doi: 10.3389/fmicb.2019.01349.
- Lee, I.M., Gundersen-Rindal, D.E., Davis, R.E., Bartoszyk, I.M. 1998. Revised classification scheme of phytoplasmas based on RFLP analyses of 16S rRNA and ribosomal protein gene sequences. International Journal of Systematic and Evolutionary Microbiology, 48: 1153-1169.
- Liu, Z., Zhao, J., Liu, M. 2016. Photosynthetic responses to phytoplasma infection in Chinese jujube. Plant Physiology and Biochemistry, 105: 12–20.
- Lou, B., Bai, X., Bail Y., Deng, C., RoyChowdhury, M., Chen, C., Song, Y. 2013. Detection and Molecular Characterization of a 16SrII-A phytoplasma in Grapefruit (Citrus paradisi) with Huanglongbinglike Symptoms in China. Journal of Phytopathology, 162: 387-395.
- Mitrovic, M., Jakovljevic, M., Jovic, J., Krstic, O., Kosovac, A., Trivellone, V., Jermini, M., Toševski, I., Cvrkovic, T. 2016. 'Canditatus Phytoplasma solani' genotypes associated with potato stolbur in Serbia and the role of Hyalesthes obsoletus and Reptalus panzeri (Hemiptera, Cixiidae) as natural vectors. European Journal of Plant Pathology, 144(3): 619-630.
- Musetti, R., Buxa, S.V., De Marco, F., Loschi, A., Polizzotto, R., Kogel, K.H., van Bel A.J. 2013. Phytoplasma-triggered Ca2+ influx is involved in sieve-tube blockage. Molecular Plant-Microbe Interactions, 26: 379–386.
- Nogay, A., Ternar, Ş. 1986. Marmara Bölgesi’nde Domateslerde Görülen Stolbur Hastalığı Üzerinde Araştırmalar. E107.845 No’lu Proje Nihai Raporu. Ziraai Araştırma Enstitüsü. İSTANBUL.
- Nogay, A., Ternar, Ş., Ünal, E. 1988. Marmara Bölgesinde Domateslerde Görülen Stolbur Hastalığı Üzerinde Araştırmalar. Bitki Koruma Bülteni, 28 (1-2): 79-98.
- Oksal, H.D., Apak, F.K., Oksal, E., Tursun, N., Sipahioğlu, H.M. 2017. Detection and molecular characterization of two 'Canditatus Phytoplasma trifolii' isolates infecting peppers at the same ecological niche. International Journal of Agriculture and Biology, 19(6): 1372-1378.
- Olivier, C., Séguin-Swartz, G., Galka, B., Olfert, O. 2011. Aster yellows in leafhoppers and field crops in Saskatchewan, Canada, 2001–2008. The Americas Journal of Plant Science and Biotechnology, 141: 425–462.
- Olmos, A., Cambra, M., Esteban, O., Gorris, M.T., Terrada, E. 1999. New device and method for capture, reverse transcription and nested PCR in a single closed tube. Nucleic Acids Research, 27: 1564-1565.
- Oshima, K., Maejima, K., Namba, S. 2013. Genomic and evolutionary aspects of phytoplasmas. Frontiers in Microbiology, 4: 230.
- Özdemir, N., Saygılı, H. 2012. A Study On The Transmission With The Seed Of Stolbur Disease In Western Anatolia Tomato Areas. Journal of Agricultural Faculty of Uludag University. 26 (1): 63-72.
- Özdemir, N. 2008. Batı Anadolu bölgesi domates üretim alanlarında görülen stolbur hastalığının yaygınlığının belirlenmesi, tanılanması ve taşınma yolları üzerinde çalışmalar. Doktora tezi, Ege Üniversitesi, Ziraat Fakültesi, Bitki Koruma Bölümü, 133 sayfa.
- Özdemir, N., Saygılı, H., Sahin, F., Karsavuran, Y., Bayrak, O.F., Oral, B. 2007. Host range and genetic characterization of a phytoplasma causing tomato stolbur disease in Turkey. Second International Symposium on Tomato Diseases (8-12 October, 2007, Kusadası, Turkey) Program and Abstract Book, p. 67.
- Özdemir, Z. 2017. “Phytoplasmas of sesame and Orosius orientalis are genetically diverse based on 16S rDNA sequencing and PCR-RFLP in Turkey”, Archives of Phytopathology and Plant Protection, 50 (13-14): 674-686.
- Pérez-López, E., Dumonceaux, T. J., Olivier, C. Y., LunaRodríguez, M. 2014. Identification of ‘Canditatus phytoplasma phoenicium’ in periwinkle from Cuba. Revista Mexexicana de Fitopatología, 32: 47.
- Pracros, P., Renaudin, J., Eveillard, S., Mouras, A., Hernould, M. 2006. Tomato Flower Abnormalities Induced by Stolbur Phytoplasma Infection Are Associated with Changes of Expression of Floral Development Genes. Molecular Plant-Microbe Interactions, 19(1): 62-68.
- Quaglino, F., Zhao, Y., Casati, P., Bulgari, D., Bianco, P.A., Wei, W., Davis, R.E. 2013. 'Canditatus Phytoplasma solani', a novel taxon associated with stolbur- and bois noir-related diseases of plants. International Journal of Systematic and Evolutionary Microbiology, 63(8): 2879- 2894.
- Reveles‐Torres, L.R., Velásquez‐Valle, R., Salas‐Muñoz, S., Mauricio‐Castillo, J.A., Caren, K., Esqueda‐Dávila, J., Herrera, M.D. 2018. Canditatus Phytoplasma trifolii (16SrVI) infection modifies the polyphenols concentration in pepper (Capsicum annuum) plant tissues. Journal of Phytopathology, DOI: 10.1111/jph.12717.
- Sahtiyancı, Ş. 1972. Marmara Bölgesi virus vektörleri üzerine araştırmalar. Zirai Mücadele Araştırma Yıllıkları, 113-114.
- Salehi, M., Izadpanah, K., Siampour, M. 2008. First Report of 'Canditatus Phytoplasma trifolii'-Related Strain Associated with Safflower Phyllody Disease in Iran. Plant Disease. 92(4): 649.
- Santos-Cervantesa, M.E., Chávez-Medinaa, J.A., Fierro-Coronadoa, J.A., Ruelas-Ayalaa, R.D., Barreras-Sotoa, M.A., Méndez-Lozanoa, J., Leyva-Lópeza, N.E. 2007. First report of Canditatus ‘Phytoplasma asteris’ infecting tomatillo (Physalis ixocarpa) in Sinaloa, México. Plant Pathology, 56: 721
- Schneider, B., Cousin, M., Klinkong, S., Seemüller, E. 1995. Taxonomic relatedness and phylogenetic positions of phytoplasmas associated with diseases of faba bean, sunhemp, sesame, soybean and eggplant. Z Pflanzenkr Pflanzenschutz, 102: 225–232.
- Schneider, B., Gibb, K.S., Padovan, A.C., Davis, R.I., De La Rue, S. 1999. Comparison and characterisation of tomato big bud and sweet potato little leaf-group phytoplasmas. Journal of Phytopathology, 147: 31–40.
- Seemuller, E., Kiss, E., Sule, S., Schneider, B. 2010. Multiple infection of apple trees by distinct strains of ‘Canditatus Phytoplasma mali’ and its pathological relevance. Phytopathology, 100: 863–870.
- Serçe, Ç.U., Yılmaz, S. 2019. First report of ‘Canditatus Phytoplasma trifolii’ (16SrVI group) infecting cabbage (Brassica oleracea) in Turkey. Journal of Plant Pathology, https://doi.org/10.1007/s42161-019-00443-y.
- Sertkaya, G., Martini, M., Musetti, R., Osler, R. 2007. Detection and molecular characterization of phytoplasmas infecting sesame and solanaceous crops in Turkey. Bulletin of Insectology, 60: 141‒142.
- Shahryari, F., Allahverdipour, T., Rabiei, Z. 2019. Phytoplasmas associated with grapevine yellows disease in Iran: first report of a 'Canditatus Phytoplasma trifolii'-related strain and further finding of a 'Ca. P. solani'-related strain. New Disease Reports, 40: 17.
- Shaw, M.E., Kirkpatrick B.C. 1993. The beet leafhopper-transmitted virescence agent causes tomato big bud disease in California. Plant Disease, 77: 290‒295.
- Singh, J., Rani, A., Kumar, P., Baranwal, V.K., Saroj, P.L, Sirohi, A. 2012. First report of a 16SrII-D phytoplasma 'Canditatus Phytoplasma australasia' associated with a tomato disease in India. New Disease Reports, 26: 14.
- Şahin, F., Özdemir, N., Oral, B., Saygılı, H., Karsavuran, Y., Bayrak, O.F. 2007. Identification of a phytoplasma causing tomato stolbur disease in Turkey. APS. SON. Joint Meeting. Phytopathology S103. July 28- August 1.
- Tanrıkut, S. 1953. Domates yetiştiriciliği için tehlikeli bir hastalık. Bitki Koruma Bülteni, 5: 22-28.
- Tsplenkov, E.E., Fedotina V.L. 1973. Nature and classification of two forms of Tomato Stolbur. Biologlcheskie. Havkl 16: 100-106 (Rev. Pl. Path., 52: 4217).
- Ulubas-Serce, C., Gazel, M., Caglayan, K., Bas, M., Son, L. 2006. Phytoplasma diseases of fruit trees in germplasm and commercial orchards. EPPO Bulletin, 36: 216-217.
- Ulubas-Serce, C., Kaya, K., Gazel, M., Caglayan, K., Sauvion, N. 2012. Psyllid vectors of AP Group (16SrX) phytoplasmas infecting grapevine in Turkey. 104. In: Book of Abstracts, 22th International Conference on Virus and Other Graft Transmissible Diseases of Fruit Crops, 3-8 June, Rome. 38.
- Ulubaş Serçe, Ç., Yılmaz, S. 2019. First report of ‘Canditatus Phytoplasma trifolii’ (16SrVI group) infecting cabbage (Brassica oleracea) in Turkey. Journal of Plant Pathology, https://doi.org/10.1007/s42161-019-00443-y.
- Usta, M., Güller, A., Sipahioğlu, H.M. 2017. Detection and Characterization of two Phytoplasma lineages on Cucumber (Cucumis sativus L.) with Same Symptomatology based on Virtual RFLP and Nucleotide Sequence Analysis of 16S rDNA. Yuzuncu Yil University Journal of Agricultural Sciences, 27(3): 299-308.
- Usta, M., Güller, A., Sipahioğlu, H.M. 2018. Molecular analysis of „ Canditatus Phytoplasma trifolii‟ and, Canditatus Phytoplasma solani‟ associated with phytoplasma diseases of tomato (PDT) in Turkey. International Journal of Agriculture and Biology, 20: 1991-1996.
- Valente, V., Musil M., Misiga S. 1961. Investlgations of European yellow styp viruses 1. the stolbur virus. Phytopathology, 42: 1-38.
- Vellios, E., Lioliopoulou, F. 2007. Detection and characterization of phytoplasmas infecting tomato plants in Greece. Bulletin of Insectology. 60(2): 157-158.
- Wei, W., Davis, R.E, Lee, I.M., Zhao, Y. 2007. Computer simulated RFLP analysis of 16S rRNA genes: identification of ten new phytoplasma groups. International Journal of Systematic and Evolutionary Microbiology, 57: 1855-1867.
- Weintraub, P.G, Beanland, L. 2006. Insect vectors of phytoplasmas. Annual Review of Entomology, 51: 91–111.
- Weintraub, P.G, Jones, P. 2009. Phytoplasmas, Genomes, Plant Hosts and Vectors. Cab International, United Kingdom. 10.1079/9781845935306.0000.
- Weisburg, W.G., Tully, J.G., Rose, D.L., Petzel, J.P., Oyaizu, H., Yang, D., Mandelco, L., Sechrest, J., Lawrence, T.G., Van Etten, J. 1989. A phylogenetic analysis of the mycoplasmas: basis for their classification. Journal of Bacteriology, 171: 6455-6467.
- Wu, Y., Hao, X., Li, Z., Gu, P., An, F., Xiang, J., Wang, H., Luo, Z., Liu, J., Xiang, Y. 2010. Identification of the phytoplasma associated with wheat blue dwarf disease in China. Plant Disease. 94: 977-985.
- Xu, X., Mou, H.Q., Zhu, S.F., Liao, X.L., Zhao, W.J. 2013. Detection and Characterization of Phytoplasma Associated with Big Bud Disease of Tomato in China. Journal of Phytopathology, 161: 430–433.
- Yavuz, Ş., Gazel, M., Çağlayan, K. 2019. Determination of apple proliferation phytoplasma disease (Canditatus Phytoplasma mali) in apple orchards in Adana and İçel provinces. Mustafa Kemal University Journal of Agricultural Sciences, 24 (1): 15-20.
- Yorgancı, Ü., Öncüer, C., Karsavuran, Y. 1991. “Batı Anadolu sanayi domatesi yetiştirme alanlarında stolbur hastalığının yaygınlık oranı ve ortaya çıkış nedenleri üzerinde araştırmalar, s. 315-319”. VI. Türkiye Fitopatoloji Kongresi (7-11 Ekim 1991, İzmir) Bildirileri, Türkiye Fitopatoloji Derneği Yayınları No. 6, 434 s.
- Zambon, Y., Canel, A., Bertaccini, A., Contaldo, N. 2018. Molecular Diversity of Phytoplasmas Associated with Grapevine Yellows Disease in North-Eastern Italy. Phytopathology, 108(2): 206-214.
- Zhang, L., Li, Z., Du, C., Fu, Z., Wu, Y. 2012. Detection and Identification of Group 16SrVI Phytoplasma in Willows in China. Journal of Phytopathology, 160: 755-757.
- Zhao, Y., Wei W., Lee I.M., Shao J., Suo X., Davis R.E. 2009. Construction of an interactive online phytoplasma classification tool, iPhyClassifier, and its application in analysis of the peach X-disease phytoplasma group (16SrIII). International Journal of Systematic and Evolutionary Microbiology, 59: 2582-2593.