Abstract
The complete genome of plum pox virus strain T isolates from five different Prunus spp., including almond (P. dulcis) and sour cherry (P. ceracus) isolates, was fully sequenced using the primer pairs designed in this study. The five isolates were aligned with other 50 PPV-T isolates whose complete genome sequences were available in GenBank and then subjected to phylogenetic and diversity analyses. Recombination analysis showed no significant signal detected in the five newly sequenced isolates while confirming four recombinant isolates reported in a previous study. Nucleotide and amino acid phylogenetic trees clustered the tested isolates into three major groups: Balkan 1, 2, and 3. Strain T isolates shared high nucleotide and amino acid identities among them. Diversity analysis applied different parameters to found that the sequences of P3 and 6K1 genes were more conserved over other genes. In accordance, the highly variable P1 and CP genes were found to experience weaker purifying pressures, ω = 0.127 and 0.219, respectively, than other genes. The three neutrality tests gave negative values to all genes, suggesting that strain T populations have expanding or bottleneck selections. Genetic make-up of the only known sour cherry isolate is highly identical to isolates from other Prunus spp. Therefore, this study has updated our knowledge of T strain diversity in new hosts and provided a clear picture of genetic variation and host relationships.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The nucleotide sequences of present study are available in the GenBank repository (https://www.ncbi.nlm.nih.gov/genbank/) with the accession number ON745776, ON745777, ON745778, ON745779, and ON745780.
References
Abadkhah M, Hajizadeh M, Koolivand D (2020) Global population genetic structure of Bean common mosaic virus. Arch Phytopathol Plant Prot 53(5–6):266–281. https://doi.org/10.1080/03235408.2020.1743525
Akbaş B, Özdemir I, Değirmenci K, Başaran MS (2013) Movement and dispersal of plum pox virus in Turkey. IOBC-WPRS Bulletin 91:329–336
Cambra M, Capote N, Myrta A, Llácer G (2006) Plum pox virus and the estimated costs associated with sharka disease. EPPO Bulletin 36(2):202–204. https://doi.org/10.1111/j.1365-2338.2006.01027.x
Carbonell A, Maliogka VA, de Jesús PJ, Salvador B, San León D, García JA, Simón-Mateo C (2013) Diverse amino acid changes at specific positions in the N-terminal region of the coat protein allow Plum pox virus to adapt to new hosts. Mol Plant Microbe Interact 26(10):1211–1224. https://doi.org/10.1094/MPMI-04-13-0093-R
Çelik A, Ertunç F (2021) Reverse transcription loop-mediated isothermal amplification (RT-LAMP) of plum pox potyvirus Turkey (PPV-T) strain. J Plant Dis Prot 128(3):663–671. https://doi.org/10.1007/s41348-021-00447-w
Çelik A, Santosa AI, Ertunç F (2022a) The monitoring of plum pox virus in Bursa, Bilecik, and Bolu provinces of Turkey refined MIs status as a variant of strain M. Arch Phytopathol Plant Prot 55(7):874–885. https://doi.org/10.1080/03235408.2022.2052523
Çelik A, Santosa AI, Gibbs AJ, Ertunç F (2022b) Prunus necrotic ringspot virus in Turkey: an immigrant population. Arch Virol 167(2):553–562. https://doi.org/10.1007/s00705-022-05374-1
Chirkov S, Sheveleva A, Ivanov P, Zakubanskiy A (2018) Analysis of genetic diversity of Russian sour cherry Plum pox virus isolates provides evidence of a new strain. Plant Dis 102(3):569–575. https://doi.org/10.1094/PDIS-07-17-1104-RE
Coşkan S, Morca AF, Akbaş B, Çelik A, Santosa AI (2022) Comprehensive surveillance and population study on plum pox virus in Ankara Province of Turkey. J Plant Dis Prot 129(4):981–991. https://doi.org/10.1007/s41348-022-00597-5
Dolan PT, Whitfield ZJ, Andino R (2018) Mechanisms and concepts in RNA virus population dynamics and evolution. Annu Rev Virol 5(1):69–92. https://doi.org/10.1146/annurev-virology-101416-041718
Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133(3):693–709. https://doi.org/10.1093/genetics/133.3.693
García JA, Glasa M, Cambra M, Candresse T (2014) Plum pox virus and sharka: a model potyvirus and a major disease. Mol Plant Pathol 15:226–241. https://doi.org/10.1111/mpp.12083
Gibbs AJ, Hajizadeh M, Ohshima K, Jones RA (2020) The potyviruses: an evolutionary synthesis is emerging. Viruses 12(2):132. https://doi.org/10.3390/v12020132
Gildow F, Damsteegt V, Stone A, Schneider W, Luster D, Levy L (2004) Plum pox in North America: identification of aphid vectors and a potential role for fruit in virus spread. Phytopathology 94(8):868–874. https://doi.org/10.1094/PHYTO.2004.94.8.868
Glasa M, Candresse T (2008) Plum pox virus. In: Mahy BWJ, Van Regenmortel MHV (eds) Encyclopedia of virology. Elsevier, Oxford, pp 238–242
Glasa M, Marie-Jeanne V, Moury B, Kúdela O, Quiot JB (2002) Molecular variability of the P3–6K1 genomic region among geographically and biologically distinct isolates of Plum pox virus. Arch Virol 147:563–575. https://doi.org/10.1007/s007050200006
Glasa M, Prikhodko Y, Predajňa L, Nagyová A, Shneyder Y, Zhivaeva T, Šubr Z, Cambra M, Candresse T (2013) Characterization of Sour Cherry isolates of Plum pox virus from the Volga Basin in Russia reveals a new cherry strain of the virus. Phytopathology 103:972–979. https://doi.org/10.1094/PHYTO-11-12-0285-R
Gürcan K, Ceylan A (2016) Strain identification and sequence variability of plum pox virus in Turkey. Turk J Agric For 40(5):746–760. https://doi.org/10.1094/10.3906/tar-1509-97
İlbağı H, Çıtır A (2014) Detection and partial molecular characterization of Plum pox virus on almond trees in Turkey. Phytoparasitica 42(4):485–491. https://doi.org/10.1007/s12600-014-0385-6
Isac M, Preda S, Marcu M (1998) Aphid species–vectors of plum pox virus. Acta Virol 42(4):233–234
James D, Varga A, Sanderson D (2013) Genetic diversity of Plum pox virus: strains, diseases and related challenges for control. Can J Plant Pathol 35(4):431–441. https://doi.org/10.1080/07060661.2013.828100
Jelkmann W, Sanderson D, Berwarth C, James D (2018) First detection and complete genome characterization of a Cherry (C) strain isolate of plum pox virus from sour cherry (Prunus cerasus) in Germany. J Plant Dis Prot 125(3):267–272. https://doi.org/10.1007/s41348-018-0155-7
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8(3):275–282. https://doi.org/10.1093/bioinformatics/8.3.275
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1:1–5. https://doi.org/10.1093/ve/vev003
Morca AF, Coşkan S, Öncü F (2020) Determination and partial molecular characterization of Plum pox virus in Bolu province. Plant Prot Bull. https://doi.org/10.16955/bitkorb.719732
Moury B, Morel C, Johansen E, Guilbaud L, Souche S, Ayme V, Caranta C, Palloix A, Jacquemond M (2004) Mutations in Potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Mol Plant Microbe Interact 17(3):322–329. https://doi.org/10.1094/mpmi.2004.17.3.322
Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9(9):e108277. https://doi.org/10.1371/journal.pone.0108277
Palmisano F, Minafra A, Myrta A, Boscia D (2015) First report of Plum pox virus strain PPV-T in Albania. J Plant Pathol. https://doi.org/10.4454/JPP.V97I2.025
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Rubio L, Guerri J, Moreno P (2013) Genetic variability and evolutionary dynamics of viruses of the family Closteroviridae. Front Microbiol 4:151. https://doi.org/10.3389/fmicb.2013.00151
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Teber S, Ceylan A, Gürcan K, Candresse T, Ulubaş Serçe Ç, Akbulut M, Kaymak S, Akbaş B (2019) Genetic diversity and molecular epidemiology of the T strain of Plum pox virus. Plant Pathol 68(4):755–763. https://doi.org/10.1111/ppa.12974
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680. https://doi.org/10.1093/nar/22.22.4673
Tokhmechi K, Abadkhah M, Koolivand D (2021) Emerging and population analysis of Grapevine Pinot gris virus isolates from Iran. 3 Biotech 11:368. https://doi.org/10.1007/s13205-021-02914-5
TUIK (2022) Turkish Statistical Institute. Crop production statistic. https://www.tuik.gov.tr/. Accessed 2 Aug 2022
Ulubaş Serçe U, Candresse T, Svanella-Dumas L, Krizbai L, Gazel M, Çağlayan K (2009) Further characterization of a new recombinant group of Plum pox virus isolates, PPV-T, found in orchards in the Ankara province of Turkey. Virus Res 142:121–126. https://doi.org/10.1016/j.virusres.2009.01.022
Acknowledgements
This study was funded by the General Directorate of Agricultural Research and Policies, Directorate of Central Plant Protection Research Institute, and the Head of Rural Service Department, Ankara Metropolitan Municipality. The authors also would like to thank the Ankara Directorate of Provincial Agriculture and Forestry and the Republic of Turkey Ministry of Agriculture and Forestry for their assistance during field surveys.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. BA: conceptualization, investigation, funding acquisition, writing, review and editing. AFM: resources, methodology, investigation, writing, funding acquisition, review and editing. SÇ: investigation, resources, writing. AIS: methodology, formal analysis, writing—original draft. HÇK: investigation, writing—review and editing AÇ: formal analysis, writing—original draft, writing—review and editing. All authors have read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest in the publication.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Akbaş, B., Morca, A.F., Coşkan, S. et al. First complete sequences and genetic variation of plum pox virus T strain in Prunus dulcis and Prunus cerasus. 3 Biotech 13, 332 (2023). https://doi.org/10.1007/s13205-023-03746-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-023-03746-1