Research Article
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Molecular characterization and comparative genomic analysis of two triamitovirus isolates hosted by the hypogean fungus Tuber excavatum Vittad.

Year 2024, Volume: 25 Issue: 2, 169 - 176, 15.10.2024

Elifnaz Bora , Ilgaz Akata , Emre Keskin , Ergin Sahin

https://doi.org/10.23902/trkjnat.1478899

Abstract

The connections between viruses and their hosts are complex and can arise from any combination of different evolutionary events including “codivergence”, “switching”, and “duplication” of the pathogen. Mycoviruses, a diverse virus group whose members specifically infect fungal hosts, are subject to similar evolutionary processes. In this study, we present the identification and complete genome characterization of the second isolate of a mitovirus, commonly known as Tuber excavatum mitovirus, officially named Triamitovirus tuex1. This mycovirus infects the hypogean, ectomyrrhizal fungus Tuber excavatum Vittad.. Both Triamitovirus tuex1 isolates, Tekirdağ (identified by us) and Lammspringe, were found in the fruiting bodies of T. excavatum isolates collected from Türkiye and Germany, respectively. Comparative genomic analyses revealed that the two virus isolates share 85.33% sequence similarity in their whole genomes, with their protein encompassing RNA-dependent RNA polymerase (RdRp) domain showing an identity rate of 94.60%. The most diverse part of the viral genomes was found to be the 5’ untranslated regions (UTRs), with a sequence similarity of 78.53%, while the 3’ UTRs were the most conserved, with 91.53% sequence similarity. Considering the shared host species, the emergence of these Triamitovirus tuex1 isolates appears to reflect a duplication pattern (intra-host divergence) resulting from adaptive radiation.

Keywords

Mycovirus Mitovirus Virus evolution Truffle Tuber excavatum

Ethical Statement

Since the article does not contain any studies with human or animal subject, its approval to the ethics committee was not required.

Supporting Institution

The Turkish Scientific and Technological Research Council (TÜBİTAK)

Project Number

121Z924

References

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  • 2. 2. Akata, I., Edis, G., Keskin, E. & Sahin, E. 2023. Diverse partitiviruses hosted by the ectomycorrhizal agaric Hebeloma mesophaeum and the natural transmission of a partitivirus between phylogenetically distant, sympatric fungi. Virology, 581: 63-70. https://doi.org/10.1016/j.virol.2023.03.002
  • 3. 3. Ayllon, M.A. & Vainio, EJ. 2023. Mycoviruses as a part of the global virome: Diversity, evolutionary links and lifestyle. Advances in Virus Research, 115: 1-86. https://doi.org/10.1016/bs.aivir.2023.02.002
  • 4. 4. Bruenn, J.A., Warner, B.E. & Yerramsetty, P. 2015. Widespread mitovirus sequences in plant genomes. PeerJ, 3: e876. https://doi.org/10.7717/peerj.876
  • 5. 5. Castellano, M.A. & Türkoğlu, A. 2012. New Records of Truffle Taxa in Tuber and Terfezia from Turkey. Turkish Journal of Botany, 36: 295-298. https://doi.org/10.3906/bot-1106-10
  • 6. 6. Darissa, O., Willingmann, P. & Adam, G. 2010. Optimized approaches for the sequence determination of double-stranded RNA templates. Journal of Virological Methods, 169(2): 397-403. https://doi.org/10.1016/j.jviromet.2010.08.013
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  • 9. 9. Fan, L., Cao, J.Z. & Li, Y. 2013. A reassessment of excavated Tuber species from China based on morphology and ITS rDNA sequence data. Mycotaxon, 124(1): 155-163. https://doi.org/10.5248/124.155
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  • 18. 18. Koonin, E.V., Dolja, V.V., Krupovic, M., Varsani, A., Wolf, Y. I., Yutin, N., Zerbini, F.M. & Kuhn, J.H. 2020. Global organization and proposed megataxonomy of the virus world. Microbiology and Molecular Biology Reviews, 84(2): 10-1128. https://doi.org/10.1128/mmbr.00061-19
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  • 20. 20. LaTourrette, K. & Garcia-Ruiz, H. 2022. Determinants of virus variation, evolution, and host adaptation. Pathogens, 11(9): 1039. https://doi.org/10.3390/pathogens11091039
  • 21. 21. Lin, Y.H., Fujita, M., Chiba, S., Hyodo, K., Andika, I.B., Suzuki, N. & Kondo, H. 2019. Two novel fungal negative-strand RNA viruses related to mymonaviruses and phenuiviruses in the shiitake mushroom (Lentinula edodes). Virology, 533: 125-136. https://doi.org/10.1016/j.virol.2019.05.008
  • 22. 22. Madeira, F., Park, Y.M., Lee, J., Buso, N., Gur, T., Madhusoodanan, N., Basutkar, P., Tivey, A.R.N., Potter, S.C., Finn, R.D. & Lopez, R. 2019. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Research, 47(W1): W636-W641. https://doi.org/10.1093/nar/gkz268
  • 23. 23. Nibert, M.L., Vong, M., Fugate, K.K. & Debat, H.J. 2018. Evidence for contemporary plant mitoviruses. Virology, 518: 14-24. https://doi.org/10.1016/j.virol.2018.02.005
  • 24. 24. Parvez, M.K. & Parveen, S. 2017. Evolution and emergence of pathogenic viruses: past, present, and future. Intervirology, 60(1-2): 1-7. https://doi.org/10.1159/000478729
  • 25. 25. Petrzik, K., Sarkisova, T., Starý, J., Koloniuk, I., Hrabáková, L. & Kubešová, O. 2016. Molecular characterization of a new monopartite dsRNA mycovirus from mycorrhizal Thelephora terrestris (Ehrh.) and its detection in soil oribatid mites (Acari: Oribatida). Virology, 489: 12-19. https://doi.org/10.1016/j.virol.2015.11.009
  • 26. 26. Sahin, E. & Akata, I. 2019. Complete genome sequence of a novel mitovirus from the ectomycorrhizal fungus Geopora sumneriana. Archives of Virology, 164: 2853-2857. https://doi.org/10.1007/s00705-019-04367-x
  • 27. 27. Sahin, E. & Akata, I. 2021. Full-length genome characterization of a novel alphapartitivirus detected in the ectomycorrhizal fungus Hygrophorus penarioides. Virus Genes, 57(1): 94-99. https://doi.org/10.1007/s11262-020-01814-9
  • 28. 28. Sahin, E., Akata, I. & Keskin, E. 2020. Novel and divergent bipartite mycoviruses associated with the ectomycorrhizal fungus Sarcosphaera coronaria. Virus Research, 286: 198071. https://doi.org/10.1016/j.virusres.2020.198071
  • 29. 29. Sahin, E., Akata, I. & Keskin, E. 2021a. Molecular characterization of a new endornavirus inhabiting the ectomycorrhizal fungus Hygrophorus penarioides. Brazilian Journal of Microbiology, 52(3): 1167-1172. https://doi.org/10.1007/s42770-021-00500-8
  • 30. 30. Sahin, E., Keskin, E. & Akata, I. 2021b. Novel and diverse mycoviruses co-inhabiting the hypogeous ectomycorrhizal fungus Picoa juniperi. Virology, 552: 10-19. https://doi.org/10.1016/j.virol.2020.09.009
  • 31. 31. Sahin, E., Ozbey Saridogan, B.G., Keskin, E. & Akata, I. 2023. Identification and complete genome sequencing of a novel betapartitivirus naturally infecting the mycorrhizal desert truffle Terfezia claveryi. Virus Genes, 59(2): 254-259. https://doi.org/10.1007/s11262-023-01972-6
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  • 33. 33. Stielow, J.B., Bratek, Z., Klenk, H.P., Winter, S. & Menzel, W. 2012. A novel mitovirus from the hypogeous ectomycorrhizal fungus Tuber excavatum. Archives of Virology, 157: 787-790. https://doi.org/10.1007/s00705-012-1228-8
  • 34. 34. Sutela, S. & Vainio, E.J. 2020. Virus population structure in the ectomycorrhizal fungi Lactarius rufus and L. tabidus at two forest sites in Southern Finland. Virus Research, 285: 197993. https://doi.org/10.1016/j.virusres.2020.197993
  • 35. 35. Varsani, A. & Krupovic, M. 2021. Family Genomoviridae: 2021 taxonomy update. Archives of Virology, 166: 2911-2926. https://doi.org/10.1007/s00705-021-05183-y
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  • 37. 37. Wang L., He, H., Wang, S., Chen, X., Qui, D., Kondo, H. & Guo, L. 2018. Evidence for a novel negative-stranded RNA mycovirus isolated from the plant pathogenic fungus Fusarium graminearum. Virology, 518: 232-240. https://doi.org/10.1016/j.virol.2018.03.008
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Year 2024, Volume: 25 Issue: 2, 169 - 176, 15.10.2024

Elifnaz Bora , Ilgaz Akata , Emre Keskin , Ergin Sahin

https://doi.org/10.23902/trkjnat.1478899

Abstract

Virüsler ile konakları arasındaki bağlantılar karmaşıktır ve “kodivergens (birlikte ıraksama)”, “değişim” ve “patojenin çoğaltılması” gibi farklı evrimsel olayların herhangi bir kombinasyonundan kaynaklanabilir. Mikovirüsler, özel olarak mantar konaklarını enfekte eden, çeşitlilik gösteren bir virüs grubudur ve benzer evrimsel süreçlere tabidir. Bu çalışmada, Tuber excavatum mitovirüsü olarak bilinen ve resmi olarak Triamitovirus tuex1 olarak adlandırılan bir mitovirüsün ikinci izolatının tanımlanması ve tüm genom nitelemesi sunulmaktadır. Bu mikovirüs, hipogean, ektomikorizal mantar Tuber excavatum Vittad.'ı enfekte eder. Sırasıyla Türkiye ve Almanya'dan toplanan Tekirdağ (bizim tarafımızdan tanımlanan) ve Lammspringe Triamitovirus tuex1 izolatlarının her ikisi de, T. excavatum meyvelerinde tanımlandı. Karşılaştırmalı genom analizleri, her iki virüs izolatının da tüm genomlarında %85,33'lük bir dizi benzerliği paylaştığını ve RNA bağımlı RNA polimeraz (RdRp) alanını (domain) içeren proteinlerinin %94,60'lık bir benzerlik oranına sahip olduğunu ortaya koymuştur. Viral genomların en çok farklılık gösteren kısmının %78,53'lük bir dizi benzerliği gösteren 5' translasyonu yapılmayan bölgeler (UTR’ler) olduğu, 3' UTR’lerin ise %91,53'lük bir dizi benzerliği ile en çok korunmuş kısımlar olduğu bulunmuştur. Konak türlerin ortak olması göz önünde bulundurulduğunda, bu Triamitovirus tuex1 izolatlarının ortaya çıkışları, adaptif radyasyondan kaynaklanan bir çoğaltma modelini (konak-içi çeşitlenmesi) yansıtıyor gibi görünmektedir.

Project Number

121Z924

References

  • 1. Akata, I., Sevindik, M. & Şahin, E. 2020. Tuber fulgens Quél., a new record for Turkish truffles. Turkish Journal of Agriculture-Food Science and Technology, 8(11): 2472-2475. https://doi.org/10.24925/turjaf.v8i11.2472-2475.3884
  • 2. 2. Akata, I., Edis, G., Keskin, E. & Sahin, E. 2023. Diverse partitiviruses hosted by the ectomycorrhizal agaric Hebeloma mesophaeum and the natural transmission of a partitivirus between phylogenetically distant, sympatric fungi. Virology, 581: 63-70. https://doi.org/10.1016/j.virol.2023.03.002
  • 3. 3. Ayllon, M.A. & Vainio, EJ. 2023. Mycoviruses as a part of the global virome: Diversity, evolutionary links and lifestyle. Advances in Virus Research, 115: 1-86. https://doi.org/10.1016/bs.aivir.2023.02.002
  • 4. 4. Bruenn, J.A., Warner, B.E. & Yerramsetty, P. 2015. Widespread mitovirus sequences in plant genomes. PeerJ, 3: e876. https://doi.org/10.7717/peerj.876
  • 5. 5. Castellano, M.A. & Türkoğlu, A. 2012. New Records of Truffle Taxa in Tuber and Terfezia from Turkey. Turkish Journal of Botany, 36: 295-298. https://doi.org/10.3906/bot-1106-10
  • 6. 6. Darissa, O., Willingmann, P. & Adam, G. 2010. Optimized approaches for the sequence determination of double-stranded RNA templates. Journal of Virological Methods, 169(2): 397-403. https://doi.org/10.1016/j.jviromet.2010.08.013
  • 7. 7. De Vienne, D.M., Refrégier, G., López‐Villavicencio, M., Tellier, A., Hood, M.E. & Giraud, T.J.N.P. 2013. Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytologist, 198(2): 347-385. https://doi.org/10.1111/nph.12150
  • 8. 8. Elena, S.F. & Sanjuán, R. 2007. Virus evolution: insights from an experimental approach. Annual Review of Ecology, Evolution, and Systematics, 38: 27-52. https://doi.org/10.1146/annurev.ecolsys.38.091206.095637
  • 9. 9. Fan, L., Cao, J.Z. & Li, Y. 2013. A reassessment of excavated Tuber species from China based on morphology and ITS rDNA sequence data. Mycotaxon, 124(1): 155-163. https://doi.org/10.5248/124.155
  • 10. 10. Fonseca, P., Ferreira, F., da Silva, F., Oliveira, L.S., Marques, J.T., Goes-Neto, A., Aguiar, E. & Gruber, A. 2020. Characterization of a novel mitovirus of the sand fly Lutzomyia longipalpis using genomic and virus-host interaction signatures. Viruses, 13(1): 9. https://doi.org/10.3390/v13010009
  • 11. 11. Ghabrial, S.A., Castón, J.R., Jiang, D., Nibert, M.L. & Suzuki, N. 2015. 50-plus years of fungal viruses. Virology, 479: 356-368. https://doi.org/10.1016/j.virol.2015.02.034
  • 12. 12. Göker, M., Scheuner, C., Klenk, H.P., Stielow, J.B. & Menzel, W. 2011. Codivergence of mycoviruses with their hosts. PLoS One 6(7): e22252. https://doi.org/10.1371/journal.pone.0022252
  • 13. 13. Guo, M., Shen, G., Wang, J., Liu, M., Bian, Y. & Xu, Z. 2021. Mycoviral diversity and characteristics of a negative-stranded RNA virus LeNSRV1 in the edible mushroom Lentinula edodes. Virology, 555: 89-101. https://doi.org/10.1016/j.virol.2020.11.008
  • 14. 14. Hillman, B.I. & Cai, G. 2013. The family narnaviridae: simplest of RNA viruses. Advances in Virus Research, 86: 149-176. https://doi.org/10.1016/B978-0-12-394315-6.00006-4
  • 15. 15. Hough, B., Steenkamp, E., Wingfield, B. & Read, D. 2023. Fungal viruses unveiled: a comprehensive review of mycoviruses. Viruses, 15(5): 1202. https://doi.org/10.3390/v15051202
  • 16. 16. Johnson, K.P., Adams, R.J., Page, R.D. & Clayton, D.H. 2003. When do parasites fail to speciate in response to host speciation? Systematic Biology, 52(1): 37-47. https://doi.org/10.1080/10635150390132704
  • 17. 17. Klassen, G.J. 1992. Coevolution: a history of the macroevolutionary approach to studying host-parasite associations. The Journal of Parasitology, 78: 573-587. https://doi.org/10.2307/3283532
  • 18. 18. Koonin, E.V., Dolja, V.V., Krupovic, M., Varsani, A., Wolf, Y. I., Yutin, N., Zerbini, F.M. & Kuhn, J.H. 2020. Global organization and proposed megataxonomy of the virus world. Microbiology and Molecular Biology Reviews, 84(2): 10-1128. https://doi.org/10.1128/mmbr.00061-19
  • 19. 19. 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. https://doi.org/10.1093/molbev/msy096
  • 20. 20. LaTourrette, K. & Garcia-Ruiz, H. 2022. Determinants of virus variation, evolution, and host adaptation. Pathogens, 11(9): 1039. https://doi.org/10.3390/pathogens11091039
  • 21. 21. Lin, Y.H., Fujita, M., Chiba, S., Hyodo, K., Andika, I.B., Suzuki, N. & Kondo, H. 2019. Two novel fungal negative-strand RNA viruses related to mymonaviruses and phenuiviruses in the shiitake mushroom (Lentinula edodes). Virology, 533: 125-136. https://doi.org/10.1016/j.virol.2019.05.008
  • 22. 22. Madeira, F., Park, Y.M., Lee, J., Buso, N., Gur, T., Madhusoodanan, N., Basutkar, P., Tivey, A.R.N., Potter, S.C., Finn, R.D. & Lopez, R. 2019. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Research, 47(W1): W636-W641. https://doi.org/10.1093/nar/gkz268
  • 23. 23. Nibert, M.L., Vong, M., Fugate, K.K. & Debat, H.J. 2018. Evidence for contemporary plant mitoviruses. Virology, 518: 14-24. https://doi.org/10.1016/j.virol.2018.02.005
  • 24. 24. Parvez, M.K. & Parveen, S. 2017. Evolution and emergence of pathogenic viruses: past, present, and future. Intervirology, 60(1-2): 1-7. https://doi.org/10.1159/000478729
  • 25. 25. Petrzik, K., Sarkisova, T., Starý, J., Koloniuk, I., Hrabáková, L. & Kubešová, O. 2016. Molecular characterization of a new monopartite dsRNA mycovirus from mycorrhizal Thelephora terrestris (Ehrh.) and its detection in soil oribatid mites (Acari: Oribatida). Virology, 489: 12-19. https://doi.org/10.1016/j.virol.2015.11.009
  • 26. 26. Sahin, E. & Akata, I. 2019. Complete genome sequence of a novel mitovirus from the ectomycorrhizal fungus Geopora sumneriana. Archives of Virology, 164: 2853-2857. https://doi.org/10.1007/s00705-019-04367-x
  • 27. 27. Sahin, E. & Akata, I. 2021. Full-length genome characterization of a novel alphapartitivirus detected in the ectomycorrhizal fungus Hygrophorus penarioides. Virus Genes, 57(1): 94-99. https://doi.org/10.1007/s11262-020-01814-9
  • 28. 28. Sahin, E., Akata, I. & Keskin, E. 2020. Novel and divergent bipartite mycoviruses associated with the ectomycorrhizal fungus Sarcosphaera coronaria. Virus Research, 286: 198071. https://doi.org/10.1016/j.virusres.2020.198071
  • 29. 29. Sahin, E., Akata, I. & Keskin, E. 2021a. Molecular characterization of a new endornavirus inhabiting the ectomycorrhizal fungus Hygrophorus penarioides. Brazilian Journal of Microbiology, 52(3): 1167-1172. https://doi.org/10.1007/s42770-021-00500-8
  • 30. 30. Sahin, E., Keskin, E. & Akata, I. 2021b. Novel and diverse mycoviruses co-inhabiting the hypogeous ectomycorrhizal fungus Picoa juniperi. Virology, 552: 10-19. https://doi.org/10.1016/j.virol.2020.09.009
  • 31. 31. Sahin, E., Ozbey Saridogan, B.G., Keskin, E. & Akata, I. 2023. Identification and complete genome sequencing of a novel betapartitivirus naturally infecting the mycorrhizal desert truffle Terfezia claveryi. Virus Genes, 59(2): 254-259. https://doi.org/10.1007/s11262-023-01972-6
  • 32. 32. Stielow, B., Klenk, H.P., Winter, S. & Menzel, W. 2011. A novel Tuber aestivum (Vittad.) mitovirus. Archives of Virology, 156: 1107-1110. https://doi.org/10.1007/s00705-011-0998-8
  • 33. 33. Stielow, J.B., Bratek, Z., Klenk, H.P., Winter, S. & Menzel, W. 2012. A novel mitovirus from the hypogeous ectomycorrhizal fungus Tuber excavatum. Archives of Virology, 157: 787-790. https://doi.org/10.1007/s00705-012-1228-8
  • 34. 34. Sutela, S. & Vainio, E.J. 2020. Virus population structure in the ectomycorrhizal fungi Lactarius rufus and L. tabidus at two forest sites in Southern Finland. Virus Research, 285: 197993. https://doi.org/10.1016/j.virusres.2020.197993
  • 35. 35. Varsani, A. & Krupovic, M. 2021. Family Genomoviridae: 2021 taxonomy update. Archives of Virology, 166: 2911-2926. https://doi.org/10.1007/s00705-021-05183-y
  • 36. 36. Walker, P.J., Siddell, S.G., Lefkowitz, E.J., Mushegian, A.R., Adriaenssens, E.M., Dempsey, D.M., Dutilh, B.E., Harrach, B., Harrison, R.L., Hendrickson, R.C., Junglen, S., Knowles, N.J., Kropinski, A.M., Krupovic, M., Kuhn, J.H., Nibert, M., Orton, R.J., Rubino, L., Sabanadzovic, S., Simmonds, P., Smith, D.B., Varsani, A., Zerbini, F.M. & Davison, A.J. 2020. Changes to virus taxonomy and the statutes ratified by the International Committee on Taxonomy of Viruses (2020). Archives of Virology, 165: 2737-2748. https://doi.org/10.1007/s00705-020-04752-x
  • 37. 37. Wang L., He, H., Wang, S., Chen, X., Qui, D., Kondo, H. & Guo, L. 2018. Evidence for a novel negative-stranded RNA mycovirus isolated from the plant pathogenic fungus Fusarium graminearum. Virology, 518: 232-240. https://doi.org/10.1016/j.virol.2018.03.008
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There are 38 citations in total.

Details

Primary Language English
Subjects Genomics and Transcriptomics, Phylogeny and Comparative Analysis, Molecular Evolution, Virology
Journal Section Research Article/Araştırma Makalesi
Authors

Elifnaz Bora 0009-0009-6047-6776

Ilgaz Akata 0000-0002-1731-1302

Emre Keskin 0000-0002-7279-313X

Ergin Sahin 0000-0003-1711-738X

Project Number 121Z924
Early Pub Date September 24, 2024
Publication Date October 15, 2024
Submission Date May 5, 2024
Acceptance Date September 12, 2024
Published in Issue Year 2024 Volume: 25 Issue: 2

Cite

APA Bora, E., Akata, I., Keskin, E., Sahin, E. (2024). Molecular characterization and comparative genomic analysis of two triamitovirus isolates hosted by the hypogean fungus Tuber excavatum Vittad. Trakya University Journal of Natural Sciences, 25(2), 169-176. https://doi.org/10.23902/trkjnat.1478899
AMA Bora E, Akata I, Keskin E, Sahin E. Molecular characterization and comparative genomic analysis of two triamitovirus isolates hosted by the hypogean fungus Tuber excavatum Vittad. Trakya Univ J Nat Sci. October 2024;25(2):169-176. doi:10.23902/trkjnat.1478899
Chicago Bora, Elifnaz, Ilgaz Akata, Emre Keskin, and Ergin Sahin. “Molecular Characterization and Comparative Genomic Analysis of Two Triamitovirus Isolates Hosted by the Hypogean Fungus Tuber Excavatum Vittad”. Trakya University Journal of Natural Sciences 25, no. 2 (October 2024): 169-76. https://doi.org/10.23902/trkjnat.1478899.
EndNote Bora E, Akata I, Keskin E, Sahin E (October 1, 2024) Molecular characterization and comparative genomic analysis of two triamitovirus isolates hosted by the hypogean fungus Tuber excavatum Vittad. Trakya University Journal of Natural Sciences 25 2 169–176.
IEEE E. Bora, I. Akata, E. Keskin, and E. Sahin, “Molecular characterization and comparative genomic analysis of two triamitovirus isolates hosted by the hypogean fungus Tuber excavatum Vittad”., Trakya Univ J Nat Sci, vol. 25, no. 2, pp. 169–176, 2024, doi: 10.23902/trkjnat.1478899.
ISNAD Bora, Elifnaz et al. “Molecular Characterization and Comparative Genomic Analysis of Two Triamitovirus Isolates Hosted by the Hypogean Fungus Tuber Excavatum Vittad”. Trakya University Journal of Natural Sciences 25/2 (October 2024), 169-176. https://doi.org/10.23902/trkjnat.1478899.
JAMA Bora E, Akata I, Keskin E, Sahin E. Molecular characterization and comparative genomic analysis of two triamitovirus isolates hosted by the hypogean fungus Tuber excavatum Vittad. Trakya Univ J Nat Sci. 2024;25:169–176.
MLA Bora, Elifnaz et al. “Molecular Characterization and Comparative Genomic Analysis of Two Triamitovirus Isolates Hosted by the Hypogean Fungus Tuber Excavatum Vittad”. Trakya University Journal of Natural Sciences, vol. 25, no. 2, 2024, pp. 169-76, doi:10.23902/trkjnat.1478899.
Vancouver Bora E, Akata I, Keskin E, Sahin E. Molecular characterization and comparative genomic analysis of two triamitovirus isolates hosted by the hypogean fungus Tuber excavatum Vittad. Trakya Univ J Nat Sci. 2024;25(2):169-76.

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