Genetic diversity and population structure of tomato brown rugose fruit virus (ToBRFV) variants from Antalya province, Turkey


  • Abdullah GÜLLER Bingol University, Faculty of Agriculture, Department of Plant Protection, Bingol (TR)
  • Mustafa USTA Van Yuzuncu Yil University, Faculty of Agriculture, Department of Plant Protection, Van (TR)
  • Filiz RANDA-ZELYÜT Bilecik Şeyh Edebali University, Faculty of Agriculture and Natural Sciences, Department of Plant Protection, 11230 Gulumbe Campus, Bilecik; Bilecik Şeyh Edebali University, Biotechnology Application and Research Centre, 11230 Gulumbe Campus, Bilecik (TR)



genetic diversity, pepper, ToBRFV, tomato, Turkey


In this study, bioinformatic analyses were carried out according to the fully coded CP and MP gene regions of the agent, using six novel tomato brown rugose fruit virus (ToBRFV) variants obtained from the production greenhouses in Antalya, where the infection was first detected in Turkey and global variants. Molecular evolutionary analyses using both CP and MP gene regions showed that all variants were distributed in three major clades. Population dynamics studies for both gene regions have shown that there was very low nucleotide diversity and haplotype diversity. The low haplotype diversity for the CP and MP genes indicated almost no recombination status. A strong negative selection was determined for CP and MP gene regions, dN/dS= 0.0877 and dN/dS=0.2104, respectively. Neutrality test results revealed that ToBRFV populations are in an expansion phase. Pairwise comparisons were performed between populations separated in the geographic hierarchy as American, European, and Asian variants, and the findings showed intense gene flow and high genetic similarity (FST<0,33 and migration rate >1). The results of this study reveal the recent population structure of the virus and suggest that necessary precautions should be taken in the international seed trade against contaminated seeds.


Abrahamian P, Cai W, Nunziata SO, Ling KS, Jaiswal N, Mavrodieva VA, Rivera Y, Nakhla MK (2020). Comparative analysis of tomato brown rugose fruit virus isolates shows limited genetic diversity. Viruses 14(12):2816.

Alfaro-Fernández A, Castillo P, Sanahuja E, Rodríguez-Salido MDC, Font MI (2020). First report of Tomato brown rugose fruit virus in tomato in Spain. Plant Disease.

Amer MA, Mahmoud SY (2020). First report of Tomato brown rugose fruit virus on tomato in Egypt. New Disease Reports 41(24):2044-0588.

Beris D, Malandraki I, Kektsidou O, Theologidis I, Vassilakos N, Varveri C (2020). First report of tomato brown rugose fruit virus infecting tomato in Greece. Plant Disease 104(7):2035.

Camacho-Beltrán E, Pérez-Villarreal A, Leyva-Lópe NE, Rodríguez-Negrete EA, Ceniceros-Ojeda EA, Méndez-Lozano J (2019). Occurrence of Tomato brown rugose fruit virus Infecting tomato crops in Mexico. Plant Disease 103(6):1440-1440.

Caruso AG, Bertacca S, Parrella G, Rizzo R, Davino S, Panno S (2022). Tomato brown rugose fruit virus: A pathogen that is changing the tomato production worldwide. Annals of Applied Biology 181(3):258- 274.

Çağlar BK, Fidan H, Elbeaino T (2013). Detection and molecular characterization of pepper mild mottle virus from Turkey. Journal of Phytopathology 161(6):434-438.

Çelik A, Coşkan S, Morca AF, Santosa AI, Koolivand D (2022). Insight into population structure and evolutionary analysis of the emerging tomato brown rugose fruit virus. Plants 11:3279.

Davino S, Caruso AG, Bertacca S, Barone S, Panno S (2020). Tomato brown rugose fruit virus: Seed transmission rate and efficacy of different seed disinfection treatments. Plants 9:1615.

Dey K, Velez-Climent M, Soria P, Batuman O, Mavrodieva V, Wei G, Zhou J, Adkins S, McVay J (2021). First report of Tomato brown rugose fruit virus infecting tomato in Florida, USA. New Disease Reports 44:e12028.

EPPO (2022). Tomato Brown Rugose Fruit Virus. EPPO Datasheets on Pests Recommended for Regulation. Retrieved 2022 May 20 from:

Fidan H, Sarikaya P, Calis O (2019). First report of Tomato brown rugose fruit virus on tomato in Turkey. New Disease Reports 39:18.

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 20:2170- 2179.

Fraile A, García-Arenal FA (1990). Classification of the tobamoviruses based on comparisons among their 126K proteins. Journal of General Virology 2223-2228.

Fu YX, Li WH (1993). Statistical tests of neutrality of mutations. Genetics 133:693-709.

Gibbs A (1999). Evolution and origins of tobamoviruses. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 354(1383):593-602.

Hak H, Spiegelman Z (2021). The tomato brown rugose fruit virus movement protein overcomes Tm-22 resistance in tomato while attenuating viral transport. Molecular Plant-Microbe Interaction 34:1024-1032.

Hall TA (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95-98.

Hančinský R, Mihálik D, Mrkvová M, Candresse T, Glasa M (2020). Plant viruses infecting Solanaceae family members in the cultivated and wild environments: A review. Plants (Basel) 9(5):667.

Hanssen IM, Lapidot M, Thomma BP (2010). Emerging viral diseases of tomato crop. Molecular Plant-Microbe Interactions 23:539-548.

Hasan ZM, Salem NM, Ismail ID, Akel EH, Ahmad AY (2022). First report of tomato brown rugose fruit virus on greenhouse tomato in Syria. Plant Disease 106:772.

HortiDaily (2020). Retrieved 2023 August 2nd from:

Hudson RR (2000). A new statistic for detecting genetic differentiation. Genetics 155:2011-2014.

Hudson RR, Boos DD, Kaplan NL (1992). A statistical test for detecting geographic subdivision. Molecular Biology Evolution 9:138-151.

Ilyas R, Rohde MJ, Richert-Pöggeler KR, Ziebell H (2022). To be seen or not to be seen: latent infection by Tobamoviruses. Plants (11(16):2166.

Karanfil A, Randa-Zelyüt F, Korkmaz S (2023). Population structure and genetic diversity of tobacco mild green mosaic virus variants in Western Anatolia of Turkey. Physiological and Molecular Plant Pathology 125:102008.

Karanfil A (2021). Prevalence and molecular characterization of cucumber mosaic virus isolates infecting tomato plants in Marmara region of Turkey. Plant Protection Bulletin 61(4):19-25.

King AM, Lefkowitz E, Adams MJ, Carstens EB (2012). Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses; Elsevier: Amsterdam, The Netherlands.

Levitzky N, Smith E, Lachman O, Luria N, Mizrahi Y, Bakelman H, Sela N, Laskar O, Milrot E, Dombrovsky A (2019). The bumblebee Bombus terrestris carries a primary inoculum of Tomato brown rugose fruit virus contributing to disease spread in tomatoes. PLoS One 14:e0210871.

Ling KS, Tian T, Gurung S, Salati R, Gilliard A (2019). First report of tomato brown rugose fruit virus infecting greenhouse tomato in the United States. Plant Disease 103:1439.

Lu JJ, He EQ, Bao WQ, Chen JS, Sun SR, Gao SJ (2021). Comparative genomics reveals insights into genetic variability and molecular evolution among sugarcane yellow leaf virus populations. Scientific Reports 11(1):7149.

Luria N, Smith E, Reingold V, Bekelman I, Lapidot M, Levin I, Elad N, Tam Y, Sela N, Abu-Ras A (2017). A new Israeli Tobamovirus isolate infects tomato plants harboring Tm-22 resistance genes. PLoS One 12:e0170429.

Melcher U, Lewandowski DJ, Dawson WO (2021) Tobamoviruses (Virgaviridae); Elsevier: Amsterdam, The Netherlands, 2021; ISBN 9780123744104

Menzel W, Knierim D, Winter S, Hamacher J, Heupel M (2019). First report of tomato brown rugose fruit virus infecting tomato in Germany. New Disease Reports 39.

Oladokun JO, Halabi MH, Barua P, Nath PD (2019). Tomato brown rugose fruit disease: Current distribution, knowledge and future prospects. Plant Pathology 68:1579-1586.

Panno S, Caruso AG, Davino S (2019). First report of tomato brown rugose fruit virus on tomato crops in Italy. Plant Disease 103:1443.

Pérez M, Porter M, Crandall KA (2008). Methods for analyzing viral evolution. In: Roossinck MJ (Ed). Plant Virus Evolution. Springer, Heidelberg, Berlin, Germany, pp 165-204.

Randa-Zelyüt, F, Fox A, Karanfil A (2023). Population genetic dynamics of southern tomato virus from Turkey. Journal of Plant Pathology 105:211-224.

Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017). DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology Evolution 34:3299-3302.

Salem N, Mansour A, Ciuffo M, Falk BW, Turina M (2016). A new tobamovirus infecting tomato crops in Jordan. Archives of Virology 161:503-506.

Skelton A, Buxton-Kirk A, Ward R, Harju V, Frew L, Fowkes A, ... Fox A (2019). First report of Tomato brown rugose fruit virus in tomato in the United Kingdom. New Diseases Report 40(12):2044-0588.

Tajima F (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.

Tamura K (1992). Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Molecular Biology and Evolution 9:678-687.

Tamura K, Stecher G, Kumar S (2021). MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution.

TurkStat (2022). Retrieved 2023 July 20 from:

van de Vossenberg BTLH, Visser M, Bruinsma M, Koenraadt HMS, Westenberg M, Botermans M (2020). Real-time tracking of Tomato brown rugose fruit virus (ToBRFV) outbreaks in the Netherlands using Nextstrain. PLoS One 15:e0234671.

Wilstermann A, Ziebell H (2019). Tomato brown rugose fruit virus (ToBRFV). JKI Data Sheets Plant Disease Diagnosis 1:1-4.

Wright S (1965). The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395-420.

Yan Z-Y, Ma H-Y, Wang L, Tettey C, Zhao M-S, Geng C, ... Li XD (2021). Identification of genetic determinants of tomato brown rugose fruit virus that enable infection of plants harbouring the Tm- 22 resistance gene. Molecular Plant Pathology 22:1347-1357.

Yan Z-Y, Ma H-Y., Han S-L, Geng C, Tian Y-P, Li X-D (2019). First Report of Tomato brown rugose fruit virus Infecting Tomato in China. Plant Disease 103:2973.

Zhang S, Griffiths JS, Marchand G, Bernards MA, Wang A (2022). Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide. Molecular Plant Pathology 23(9):1262-1277.



How to Cite

GÜLLER, A., USTA, M., & RANDA-ZELYÜT, F. (2023). Genetic diversity and population structure of tomato brown rugose fruit virus (ToBRFV) variants from Antalya province, Turkey. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 51(3), 13356.



Research Articles
DOI: 10.15835/nbha51313356