First Insight into Genetic Variation and Population Structure of The Emerging Citrus chlorotic dwarf-associated virus (CCDaV, genus Citlodavirus)

Year 2022, , 591 - 601, 30.09.2022

Filiz Randa Zelyüt , Adyatma Irawan Santosa , Ali Karanfil , Jose Cleydson Ferreira Sılva

https://doi.org/10.29133/yyutbd.1123999

Abstract

Citrus spp. is widely planted in tropical and subtropical regions, including in Turkey and other Mediterranean countries. Due to its widespread vector and climate change, Citrus chlorotic dwarf-associated virus (CCDaV), a member of the newly formed genus Citlodavirus, is one of the emerging viruses that can be a serious constraint to Citrus crops production in the coming years. Therefore, in-silico analysis on all available isolates in NCBI GenBank was performed to provide the first insight into the genetic population and evolution of CCDaV, which may contribute to its control. CCDaV phylogroups based on full genome, complete movement protein, and complete coat protein sequences were found to be not associated with isolate origins or host species, and all isolates also shared a high genetic identity among them. However, neutrality tests indicated that the current populations are expanding, driven by new mutations. Low Fixation index (FST) values (0.00000-0.36207) confirmed no genetic separation among different ORFs of isolates from three countries. The constructed TimeTree suggested that CCDaV emergence was very recent compared to the other three members of the genus Citlodavirus. Therefore, the obtained results of this study could also expand our knowledge on other even more obscure citladovirus and even other plant DNA viruses, which are still less studied than RNA viruses.

Keywords

Divergence time, Phylogenetic analysis, Plant DNA virus evolution, Population structure

References

• Catara, A. F., Bar-Joseph, M., & Licciardello, G. (2021). Exotic and emergent citrus viruses relevant to the Mediterranean region. Agriculture, 11(9), 839. doi:10.3390/agriculture11090839
• Chare, E. R., & Holmes, E. C. (2006). A phylogenetic survey of recombination frequency in plant RNA viruses. Archives of Virology, 151(5), 933-946. doi:10.1007/s00705-005-0675-x
• Coşkan, S., Morca, A. F., Akbaş, B., Çelik, A., & Santosa, A. I. (2022). Comprehensive surveillance and population study on plum pox virus in Ankara Province of Turkey. Journal of Plant Diseases and Protection, (online first). doi:10.1007/s41348-022-00597-5
• Çelik, A., Santosa, A. I., Gibbs, A. J., & Ertunç, F. (2022). Prunus necrotic ringspot virus in Turkey: an immigrant population. Archives of Virology, 167(2), 553-562. doi:10.1007/s00705-022-05374-1
• Fontenele, R. S., Abreu, R. A., Lamas, N. S., Alves-Freitas, D. M. T., Vidal, A. H., Poppiel, R. R., Melo, F. L., Lacorte, C., Martin, D. P., Campos, M. A., Varsani, A., & Ribeiro, S. G. (2018). Passion fruit chlorotic mottle virus: Molecular characterization of a new divergent Geminivirus in Brazil. Viruses, 10(4), 169. doi:10.3390/v10040169
• Fu, Y. X., & Li, W. H. (1993). Statistical tests of neutrality of mutations. Genetics, 133(3), 693-709. doi:10.1093/genetics/133.3.693
• Gibbs, A., Gibbs, M., Ohshima, K., & Garcia-Arenal, F. (2008). More about plant virus evolution: past, present, and future. In E. Domingo, C. R. Parrish, & J. J. Holland (Eds.), Origin and Evolution of Viruses 2nd ed (pp. 229-249). Elsevier: London. doi:10.1016/B978-0-12-374153-0.00011-4
• Guo, J., Lai, X. P., Li, J. X., Yue, J. Q., Zhang, S. Y., Li, Y. Y., Gao, J. Y., Wang, Z. R., Duan, H. F., & Yang, J. D. (2015). First report on citrus chlorotic dwarf associated virus on lemon in Dehong prefecture, Yunnan, China. Plant Disease, 99(9), 1287. doi:10.1094/PDIS-01-15-0011-PDN
• Hudson, R. R. (2000). A new statistic for detecting genetic differentiation. Genetics, 155(4), 2011-2014. doi:10.1093/genetics/155.4.2011
• Hudson, R. R., Boos, D. D., & Kaplan, N. L. (1992). A statistical test for detecting geographic subdivision. Molecular Biology and Evolution, 9(1), 138-151. doi:10.1093/oxfordjournals.molbev.a040703
• Karanfil, A., & Korkmaz, S. (2019). Geographic distribution and molecular characterization of Turkish isolates of the citrus chlorotic dwarf-associated virus. Journal of Plant Pathology, 101(3), 621-628. doi:10.1007/s42161-019-00250-5
• Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120 doi:10.1007/bf01731581
• Korkmaz, S., Cinar, A., Kersting, U., & Garnsey, S. M. (1995). Citrus chlorotic dwarf: a new whitefly- transmitted virus like disease of citrus in Turkey. Plant Disease, 79, 1074. doi:10.1094/PD-79-1074C
• Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547-1549. doi:10.1093/molbev/msy096
• Kurtuluş, O., Dönmez, D., Biçen, B., Şimşek, Ö., Çimen, B., Yeşiloğlu, T., Küden, A., & Kaçar, Y. A. (2021). Bazı turunçgil melezlerinin in vitro koşullarda mikroçoğaltım ve köklenme performanslarının araştırılması (in Turkish). Yuzuncu Yil University Journal of Agricultural Sciences, 31(1), 19-29. doi:10.29133/yyutbd.810784
• Loconsole, G., Saldarelli, P., Doddapaneni, H., Savino, V., & Giovanni, P. M. (2012). Identification of a single-stranded DNAvirus-associated with citrus chlorotic dwarf disease, a new member in the family Geminiviridae. Virology, 432(1), 162-172. doi:10.1016/j.virol.2012.06.005
• Martin, D. P., Murrell, B., Golden, M., Khoosal, A., & Muhire, B. (2015). RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evolution, 1(1), vev003. doi:10.1093/ve/vev003
• Mello, B. (2018). Estimating TimeTrees with MEGA and the TimeTree resource. Molecular Biology and Evolution, 35(9), 2334-2342. doi:10.1093/molbev/msy133
• Morca, A. F., Çelik, A., Coşkan, S., Santosa, A. I., & Akbaş, B. (2022). Population analysis on tomato spotted wilt virus isolates inducing various symptoms on tomato, pepper, and Chenopodium album in Turkey. Physiological and Molecular Plant Pathology, 118, 101786. doi:10.1016/j.pmpp.2022.101786
• Muhire, B. M., Varsani, A., & Martin, D. P. (2014). SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE, 9(9), e108277. doi:10.1371/journal.pone.0108277
• Ng, T. F. F., Duffy, S., Polston, J. E., Bixby, E., Vallad, G. E., & Breitbart, M. (2011). Exploring the diversity of plant DNA viruses and their satellites using vector-enabled metagenomics on whiteflies. PLoS ONE, 6(4), e19050. doi:10.1371/journal.pone.0019050
• Qiu, Y., Zhang, S., Yu, H., Xuan, Z., Yang, L., Zhan, B., Zerbini, F. M., & Cao, M. (2020). Identification and characterization of two novel Geminiviruses associated with paper mulberry (Broussonetia papyrifera) leaf curl disease. Plant Disease, 104(11), 3010-3018. doi:10.1094/PDIS-12-19-2597-RE
• Randa-Zelyüt, F., & Ertunç, F. (2021). Population genetic analysis of lettuce big-vein disease viruses and their vector fungi Olpidium virulentus in Ankara province, Turkey. Physiological and Molecular Plant Pathology, 113, 101593. doi:10.1016/j.pmpp.2020.101593
• Roossinck, M. J., & Ali, A. (2007). Mechanisms of plant virus evolution and identification of genetic bottlenecks: impact on disease management. In Z. K. Punja, S. H. de Boer, & H. Sanfaçon (Eds.), Biotechnology and plant disease management (pp. 109-124). CABI: Oxfordshire, UK. doi:10.1079/9781845932886.0000
• Roumagnac, P., Lett, J-M., Fiallo Olivé, E., Navas Castillo, J., Zerbini, F. M., Martin, D. P., & Varsani, A. (2021). Establishment of five new genera in the family Geminiviridae: Citlodavirus, Maldovirus, Mulcrilevirus, Opunvirus, and Topilevirus. Archives of Virology, 167(2), 695-710. doi:10.1007/s00705-021-05309-2
• Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., & Sanchez-Gracia, A. (2017). DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution, 34(12), 3299-3302. doi:10.1093/molbev/msx248
• Santosa, A. I., & Ertunç, F. (2021). Reactions of fifteen onion cultivars commonly cultivated in Turkey to Leek yellow stripe virus (LYSV). Yuzuncu Yil University Journal of Agricultural Sciences, 31(1), 71-79. doi:10.29133/yyutbd.748558
• Sanz, A. I., Fraile, A., Gallego, J. M., Malpica, J. M., & Garcia-Arenal, F. (1999). Genetic variability of natural populations of Cotton leaf curl geminivirus, a single-stranded DNA virus. Journal of Molecular Evolution, 49, 672-681. doi:10.1007/PL00006588
• Sokhandan-Bashir, N., & Melcher, U. (2012). Population genetic analysis of Grapevine fanleaf virus. Archives of Virology, 157(10), 1919-1929. doi:10.1007/s00705-012-1381-0
• Stobbe, A., & Roossinck, M. J. (2016). Plant Virus Diversity and Evolution. In A. Wang, & X. Zhou (Eds.), Current Research Topics in Plant Virology, (pp. 197-215). Springer. doi:10.1007/978-3-319-32919-2_8
• Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123(3), 585-595. doi:10.1093/genetics/123.3.585
• 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(3), 512-526. doi:10.1093/oxfordjournals.molbev.a040023
• Tokhmechi, K., Abadkhah, M., & Koolivand, D. (2021). Emerging and population analysis of Grapevine Pinot gris virus isolates from Iran. 3 Biotech, 11(8), 368. doi:10.1007/s13205-021-02914-5
• Yang, Z., Zhang, L., Zhao, J., Li, T., Liu, Q., Cao, M., & Zhou, Y. (2020). First report of citrus chlorotic dwarf-associated virus on pomelo in Nakhon, Thailand. Plant Disease, 104(4), 1262. doi:PDIS-10-19-2093-PDN
• Zhang, S., Shen, P., Li, M., Tian, X., Zhou, C., & Cao, M. (2018). Discovery of a novel geminivirus associated with camellia chlorotic dwarf disease. Archives of Virology, 163, 1709-1712 doi:10.1007/s00705-018-3780-3
• Zhou, Y., Zhang, Y., Liu, Y., Chen, H., Li, T., & Zhou, C. (2017). Distribution and molecular characterization of citrus chlorotic dwarf-associated virus in China. Australasian Plant Pathology, 46, 227-229. doi:10.1007/s13313-017-0480-5