Determination of Viruses Infecting Pepper in Turkey

Öz

Various viruses cause infection in pepper (Capsicum annuum L.) and can lead to significant crop losses. In this study, 616 pepper samples exhibiting virus-like symptoms were collected in 2018 from pepper production areas in Antalya, Manisa, Çanakkale Samsun and Bursa province, where most of Turkey's pepper production is carried out. Samples were tested using polyclonal antisera of Alfalfa mosaic virus (AMV), Cucumber mosaic virus (CMV), Impatiens necrotic spot virus (INSV), Pepper mild mottle virus (PMMoV), Potato virus Y (PVY), Tobacco etch virus (TEV), Tobacco mosaic virus (TMV), Tomato chlorotic spot virus (TSCV), Tomato mosaic virus (ToMV) and Tomato spotted wilt virus (TSWV) by Double antibody sandwich-enzyme linked immunosorbent assay DAS-ELISA. Based on the serological test results, TSWV, CMV, PMMoV, PVY and AMV were detected in 55, 22.2, 0.5, 0.5 and 0.3 % of the total tested samples, respectively. Mixed infections involving different combination of viruses were found in 6.5 % of samples. TSWV+CMV dual infection was the most common (4.5 %) among mixed-infected samples, followed by TSWV+PVY (0.6 %), TSWV+PMMoV (0.5 %), PMMoV+CMV (0.3 %). Also, TSWV+CMV+PVY (0.3 %) and TSWV+CMV+PMMoV (0.2 %) triple infections were determined in the tested samples. However, ToMV, TMV, TEV, TCSV and INSV were not detected in any of the pepper samples tested in this study. To our knowledge, this is the first report of PMMoV on pepper in the Aegean and Marmara Regions of Turkey. 

Anahtar Kelimeler

• Capsicum annuum L.
• Survey
• Incidence
• DAS-ELISA,

Türkiye’de Biberde Enfeksiyon Oluşturan Virüslerin Belirlenmesi

Öz

Biber (Capsicum annuum L.)’de çok sayıda virüs enfeksiyona neden olmakta ve önemli ürün kayıplarına yol açmaktadır. Bu çalışma kapsamında, 2018 yılında Türkiye biber üretiminin büyük bir bölümünün gerçekleştirildiği Antalya, Manisa, Çanakkale, Samsun ve Bursa illerinde biber yetiştirilen alanlardan virüs-benzeri simptom sergileyen 616 adet biber örneği toplanmıştır. Bu örnekler daha sonra Alfalfa mosaic virus (AMV), Cucumber mosaic virus (CMV), Impatiens necrotic spot virus (INSV), Pepper mild mottle virus (PMMoV), Potato virus Y (PVY), Tobacco etch virus (TEV), Tobacco mosaic virus (TMV), Tomato chlorotic spot virus (TCSV), Tomato mosaic virus (ToMV) ve Tomato spotted wilt virus (TSWV) poliklonal antiserumları kullanılarak Double antibody sandwich-enzyme linked immunosorbent assay (DAS-ELISA) yöntemi ile test edilmiştir. Test sonuçlarına göre örneklerin % 55’inin TSWV, % 22.2’sinin CMV, %0.5’inin PMMoV, %0.5’inin PVY ve %0.3’ünün ise AMV ile tekli enfekteli olduğu belirlenmiştir. İncelenen örneklerin % 6.5’inin ise birden fazla virüs ile karışık enfekteli olduğu tespit edilmiştir. Karışık enfeksiyonlu örnekler içerisinde en yaygın olarak TSWV+CMV ikili enfeksiyonuna (% 4.5) rastlanılırken, bunu sırası ile; TSWV+PVY (% 0.6), TSWV+PMMoV (% 0.5), PMMoV+CMV (% 0.3) izlemiştir. Ayrıca, test edilen örneklerde TSWV+CMV+PVY (% 0.3) ve TSWV+CMV+PMMoV (% 0.2) üçlü karışık enfeksiyonu belirlenmiştir. Bununla birlikte, çalışmada test edilen biber örneklerinin hiçbirisinde ToMV, TMV, TEV, TCSV ve INSV tespit edilememiştir. Bu çalışmada tespit edilen PMMoV, Ege ve Marmara Bölgesi için ilk kayıt niteliğindedir.

Anahtar Kelimeler

• Capsicum annuum L
• DAS-ELISA
• Sürvey
• Bulunma oranı
• Capsicum annuum L.
• Survey
• Incidence

Kaynakça

1. Adkins, S,. 2000. Tomato spotted wilt virus -positive steps towards negative success. Molecular Plant Pathology, 1, 151-157.
2. Arogundade, O., Balogun, O. S., Kumar, P. L. 2019. Seed transmissibility of Cucumber mosaic virus in Capsicum species. International Journal of Vegetable Science, 25(2): 146-153. doi:10.1080/19315260.2018.1487498
3. Arlı-Sökmen, M., Mennan, H., Sevik, M.A., Ecevit, O., 2005. Occurrence of viruses in field- grown pepper crops and some of their reservoir weed hosts in Samsun, Turkey. Phytoparasitica, 33(4): 347-358. doi:10.1007/BF02981301
4. Avilla, C., Collar, J. L., Duque, M., Fereres, A., 1997. Yield of bell pepper (Capsicum annuum) inoculated with CMV and/or PVY at different time intervals/Ertrag von Paprika (Capsicum annuum). Journal of Plant Diseases and Protection, 104(1):1-8.
5. Beşkeçili, M., Güneş, N., Gümüş, M., 2021. Antalya ili Demre ilçesi biber yetiştiriciliğinde Tomato spotted wilt virus (TSWV) ve Cucumber mosaic virus (CMV) etmenlerinin yaygınlığının belirlenmesi. Ege Üniversitesi Ziraat Fakültesi Dergisi, 58(3): 399-405. doi:10.20289/zfdergi.799432
6. Boiteux, L.S., Nagata, T., Dutra, W.P., Fonseca, M.E.N., 1993. Sources of resistance to tomato spotted wilt virus (TSWV) in cultivated and wild species of Capsicum. Euphytica, 67, 89-94.
7. Buzkan, N., Demir, M., Öztekin, V., Mart, C., Çağlar, B. K., Yılmaz., M. A., 2006. Evaluation of the status of capsicum viruses in the main growing regions of Turkey, EPPO Bulletin, 36(1): 15-19.
8. Buzkan, N., Arpacı, B.B., Simon, V., Fakhfakh, H., Moury, B., 2013. High prevalence of poleroviruses in field-grown pepper in Turkey and Tunisia. Archives Virology, 158(4): 881-885. doi:10.1007/s00705-012-1553-y

9. Clark, M.R., Adams, A.M., 1977. Characteristics of the microplate method of enzyme linked immunosorbent assay for the detection of plant viruses. Journal of General Virology, 34, 475-483. doi: 10.1099/0022-1317-34-3-475
10. Çağlar, B. K., Fidan, H., Elbeaino, T., 2013. Detection and molecular characterization of Pepper mild mottle virus from Turkey. Journal of Phytopathology, 161(6). 434-438. doi: 10.1111/jph.12068
11. Çelik, N., Özalp, R., Göçmen, M., 2012. Antalya ili örtü altı biber yetiştiriciliğinde Patates Y Virüsü (PVY) patotiplerinin belirlenmesi ve bazı biber çeşitlerinin PVY’ye karşı reaksiyonları. Bitki Koruma Bülteni, 52(3): 235-246.
12. Çiçek, Y., Yorgancı, Ü., 1991. Studies on the incidence of Tobacco Mosaic Virus on certified seed of tomato, pepper and eggplant in Aegean Region. The Journal of Turkish Phytopathology, 20(2-3): 57-65.
13. Deligoz, I., Arlı Sokmen, M., Sarı S., 2014. First report of resistance breaking strain of Tomato spotted wilt virus (Tospovirus; Bunyaviridae) on resistant sweet pepper cultivars in Turkey. New Disease Reports, 30, 26. doi:10.5197/j.2044-0588.2014.030.026
14. Deligöz, İ., Arlı Sökmen, M., 2020. Samsun ilinde biber alanlarında enfeksiyon oluşturan Potato virus Y patotiplerinin belirlenmesi ve moleküler karakterizasyonu. Anadolu Tarım Bilimleri Dergisi, 35(3): 483-495. doi:/10.7161/omuanajas.697731
15. Erkan, S., 1986. Potato virus Y on pepper in Turkey. Phytopathologia Mediterranea, 26, 149-150.
16. FAO, 2020. Food and Agriculture Organization of the United Nations. www.fao.org. URL: https://www.fao.org/faostat/en/#data/QCL/visualize (Erişim:27.05.2022).
17. Ferrand, L., García, M. L., Resende, R. O., Balatti, P. A., Dal Bó, E., 2015. First report of a resistance-breaking isolate of Tomato spotted wilt virus infecting sweet pepper harboring the Tsw gene in Argentina. Plant Disease, 99(12): 1869-1870. doi:10.1094/PDIS-02-15-0207-PDN
18. Fidan, H., 2016. Antalya’da örtü altı domates ve biber alanlarında dayanıklılık kıran Tomato spotted wilt virus (TSWV) izolatları. VI. Türkiye Bitki Koruma Kongresi, 560, 5-8 Eylül, Konya.
19. Fidan, H., Sarikaya, P., Yildiz, K., Topkaya, B., Erkis, G., Calis, O., 2021. Robust molecular detection of the new Tomato brown rugose fruit virus in infected tomato and pepper plants from Turkey. Journal of Integrative Agriculture, 20 (8): 2170-2179. doi:10.1016/S2095-3119(20)63335-4
20. Green, S. K., Kim, J. S., 1991. Characteristics and control of viruses infecting peppers: a literature review. Asian Vegetable Research and Development Center. Technical Bulletin No:18, 60p.
21. Güldür, M.E., Ozaslan, M., Baloglu, S., Yılmaz, M.A., 1994. Pepper mild mottle virus in pepper in Turkey. Proceedings of 9th Congress of the Mediterranean Phytopathological Union, 465-467. 18-24 September, Kusadasi.
22. Güldür, M.E., Çaglar, B.K., 2006. Outbreaks of Pepper mild mottle virus in greenhouses in Sanlıurfa, Turkey. Journal of Plant Pathology, 88(3): 337–340.
23. Güneş, N., Gümüş, M., 2019. Detection and characterization of Tomato spotted wilt virus and Cucumber mosaic virus on pepper growing areas in Antalya. Journal of Agricultural Sciences, 25(3): 259-271. doi: 10.15832/ankutbd.499144
24. Keleş Öztürk, P., Baloğlu, S., 2019. Doğu Akdeniz Bölgesi’nde açık alanda yetiştirilen biberlerde bazı virüslerin serolojik ve moleküler tanısı. Alatarım, 18(1): 1-11.
25. Kenyon, L., Kumar, S., Tsai, W. S., Hughes, J. D. A., 2014. Virus diseases of peppers (Capsicum spp.) and their control. Advances in Virus Research, 90, 297-354. doi:10.1016/B978-0-12-801246-8.00006-8
26. Margaria, P., Ciuffo, M., Turina, M., 2004. Resistance breaking strain of Tomato spotted wilt virüs (Tospovirus, Bunyaviridae) on resistant pepper cultivars in Almeria. Spain, Plant Patholology, 53, 795. doi:10.1111/j.1365-3059.2004.01082.x
27. Margaria, P., Ciuffo, M., Pacifico, D., Turina, M., 2007. Evidence that the nonstructural protein of Tomato spotted wilt virüs is the avirulence determinant in the interaction with resistant pepper carrying the Tsw gene. Molecular Plant-Microbe Interactions, 20(5): 547-558. doi: 10.1094/MPMI-20-5-0547
28. McDonald, B., 2010. How can we achieve durable disease resistance in agricultural ecosystems?. New Phytologist, 185 (1): 3-5. doi: 10.1111/j.1469-8137.2009.03108.x
29. Moury, B., Verdin, E., 2012. Viruses of pepper crops in the Mediterranean basin: a remarkable stasis. In Loebenstein, G., Lecoq, H. (Eds). Advances in virus research. Academic Press, 84, 127-162. doi: 10.1016/B978-0-12-394314-9.00004-X
30. Murphy, J. F., Bowen, K. L., 2006. Synergistic disease in pepper caused by the mixed infection of Cucumber mosaic virus and Pepper mottle virus. Phytopathology, 96(3): 240-247. doi: 10.1094/PHYTO-96-0240
31. Nilon, A., Robinson, K., Pappu, H. R., Mitter, N., 2021. Current status and potential of RNA interference for the management of tomato spotted wilt virus and thrips vectors. Pathogens, 10(3): 320. doi:10.3390/pathogens10030320
32. Özaslan, M., Baç, B., Aytekin, T. Sıgırcı, Z., 2006. Identification of pepper viruses by das-elisa assays in Gaziantep-Turkey. Plant Pathology Journal, 5(1): 11-14. doi: 10.3923/ppj.2006.11.14
33. Özdemir, S., Erilmez, S., 2007. Denizli ilinde yetiştirilen biber, patlıcan ve marul üretim alanlarında bazı viral etmenlerin saptanması. Türkiye II. Bitki Koruma Kongresi, 114, 27-29 Ağustos, Isparta.
34. Palukaitis, P, Roossinck, M.J., Dietzgen, R.G., Francki, R.I.B., 1992. Cucumber mosaic virus. Advances in Virus Research, 41, 281-349. doi: 10.1016/S0065-3527(08)60039-1
35. Parisi, M., Daniela, A., Pasquale, T., 2020. Overview of biotic stresses in pepper (Capsicum spp.): Sources of genetic resistance, molecular breeding and genomics. International Journal of Molecular Sciences, 21(7): 2587. doi: 10.3390/ijms21072587
36. Pernezny, K., Robert, P.D., Murphy, J.F., Goldberg, N.P., 2003. Compendium of pepper diseases. The American Phytopatholgical Society, St. Paul, MN, 1, 24-25.
37. Pink, D.A.C., Hand, P., 2003. Plant resistance and strategies for breeding resistant varieties. Plant Protection Science, 38, 9-14.
38. Rodriguez-Alvarado, G., Fernandez-Pavia, S., Creamer, R., Liddell, C., 2002. Pepper mottle virus causing disease in chile peppers in southern New Mexico. Plant Disease, 86(6): 603-605. doi: 10.1094/PDIS.2002.86.6.603
39. Roggero, P., Masenga, V., Tavella L., 2002. Field isolates of Tomato spotted wilt virus overcoming resistance in pepper and their spread to other hosts in Italy. Plant Diseases, 86(9): 950-954. doi:10.1094/PDIS.2002.86.9.950
40. Sevik, M. A., 2011. Occurrence of pepper mild mottle virus in greenhousegrown pepper (Capsicum annuum L.) in the West Mediterranean region of Turkey. African Journal of Biotechnology, 10(25): 4976-4979.
41. TÜİK, 2020. Türkiye İstatistik Kurumu. www.tuik.gov.tr. URL: https://biruni.tuik.gov.tr/medas/?kn=92&locale=tr (Erişim Tarihi:6.06.2020).
42. Uzunoğulları, N., Gümüş, M., 2015. Marmara Bölgesi'nde bazı kültür bitkilerinde doğal enfeksiyona neden olan hıyar mozaik virüsü (Cucumber mosaic virus, CMV)' nün tespiti. Trakya University Journal of Natural Sciences, 16(1): 9-15.
43. Whitfeld, A.E, Ullman, D.E, German, T.L., 2005. Tospovirus thrips interactions. Annual Review of Phytopathology, 43, 459–489. doi: 10.1146/annurev.phyto.43.040204.140017
44. Wijkamp, I., 1995. Virus-Vector Relationships in The Transmission of Tospoviruses, Doctoral Thesis, Wageningen s.143.
45. Yılmaz, M.A., Davis, R.F., 1985. Identification of viruses infecting vegetable crops along the mediterranean sea coast in Turkey. Journal Turkish Phytopathology, 14(1): 1-8.
46. Yoon, J. Y., Her, N. H., Cho, I. S., Chung, B. N., Choi, S. K., 2021. First report of a resistance-breaking strain of Tomato spotted wilt orthotospovirus infecting Capsicum annuum carrying the Tsw resistance gene in South Korea. Plant Disease, 105(8): 2259. doi:10.1094/PDIS-09-20-1952-PD