Molecular characterization of a novel Betanucleorhabdovirus infecting sugar beet in Iran
DOI:
https://doi.org/10.2298/ABS250903028AKeywords:
beet betanucleorhabdovirus 1, phylogenetic analysis, natural host rangeAbstract
Paper description:
- Sugar beet (Beta vulgaris) is an important crop mostly cultivated as a source of sugar worldwide. It is exposed to potential virus infection.
- We discovered a novel betanucleorhabdovirus in sugar beet grown in Iran and named it beet betanucleorhabdovirus 1 (BNRV1).
- BNRV1 was most closely related to tomato betanucleorhabdovirus 2, tomato betanucleorhabdovirus 1, and sambucus betanucleorhabdoviruses 1-5.
- Chenopodium album, Malva neglecta, and Carthamus oxyacanthus plants were infected with BNRV1.
Abstract: We report the characterization and genetic variations of a novel betanucleorhabdovirus infecting sugar beet in Iran. Pairwise comparison of the obtained betanucleorhabdovirus sequence with betanucleorhabdoviruses from GenBank showed that it shares the highest nucleotide identity with tomato betanucleorhabdovirus 2 (TBRV2) and Sambucus betanucleorhabdovirus 4. The obtained sequence contained six open reading frames (ORFs) in antigenomic sense flanked by complementary 3′ leader and 5′ trailer sequences (3'-N-P-P3-M-G-L-5'). In the phylogenetic tree, the detected isolate was clustered with the betanucleorhabdoviruses and was most closely related to TBRV2, tomato betanucleorhabdovirus 1, and Sambucus betanucleorhabdovirus 1 to 5. The genome organization, phylogenetic relationships, and sequence similarities to other betanucleorhabdoviruses suggest that the virus is a new member of the genus Betanucleorhabdovirus, which we propose to name beet betanucleorhabdovirus 1 (BNRV1). The virus’s partial spread and host-range investigations revealed that sugar beet fields in northeast Iran were infected by BNRV1, which also infects Chenopodium album, Malva neglecta, and Carthamus oxyacanthus weeds. Low values of Ks*, Kst*, Z*, and Snn indicate no substantial genetic differentiation between populations of this virus. Selection pressures on a portion of the BNRV1 N gene analyzed were negative, showing purifying selection was occurring. The magnitude of negative selection in the BNRV1 N gene was consistent with what has been reported for other betanucleorhabdoviruses.
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References
Samuel A. Dines L. Lockhart and Wiseman’s Crop Husbandry Including Grassland. Woodhead Publishing. 2023;694p.
Dohm JC, Minoche AE, Holtgräwe D, Capella-Gutiérrez S, Zakrzewski F, Tafer H, Rupp O, Sörensen TR, Stracke R, Reinhardt R, Goesmann A, Kraft T, Schulz B, Stadler PF, Schmidt T, Gabaldón T, Lehrach H, Weisshaar B, Himmelbauer H. The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature. 2014;505:546-9. https://doi.org/10.1038/nature12817
Brar NS, Dhillon BS, Saini KS, Sharma PK. Agronomy of sugar beet cultivation. Agric Rev. 2015;36:184-97. https://doi.org/10.5958/0976-0741.2015.00022.7
Mall AK, Srivastava S, Mulet JM, Popović V, Misra V. Sugar Beet Special Issue: Biotechnology and Breeding Techniques for Stress-Resistant Sugar Beet. Sugar Tech. 2024;26:1195-8. https://doi.org/10.1007/s12355-024-01501-1
Walker PJ, Freitas-Astúa J, Bejerman N, Blasdell KR, Breyta R, Dietzgen RG, Fooks AR, Kondo H, Kurath G, Kuzmin IV, Ramos-González PL, Shi M, Stone DM, Tesh RB, Tordo N, Vasilakis N, Whitfield AE, Ictv Report Consortium. ICTV Virus Taxonomy Profile: Rhabdoviridae 2022. J Gen Virol. 2022;103:001689. https://doi.org/10.1099/jgv.0.001689
Wu LP, Yang T, Liu HW, Postman J, Li R. Molecular characterization of a novel rhabdovirus infecting blackcurrant identified by high-throughput sequencing. Arch Virol. 2018;163:1363-6. https://doi.org/10.1007/s00705-018-3709-x
Dietzgen RG, Kondo H, Goodin MM, Kurath G, Vasilakis N. The family Rhabdoviridae: mono- and bipartite negative-sense RNA viruses with diverse genome organization and common evolutionary origins. Virus Res. 2017;227:158-70. https://doi.org/10.1016/j.virusres.2016.10.010
Bejerman N, Dietzgen RG, Debat H. Illuminating the Plant Rhabdovirus Landscape through Metatranscriptomics Data. Viruses. 2021;13(7):1304. https://doi.org/10.3390/v13071304
Belete MT, Igori D, Kim SE, Lee SH, Moon JS. Complete genome sequence of cnidium virus 1, a novel betanucleorhabdovirus infecting Cnidium officinale. Arch Virol. 2022;167:973-7. https://doi.org/10.1007/s00705-021-05348-9
Rivarez MPS, Pecman A, Bačnik K, Maksimović O, Vučurović A, Seljak G, Mehle N, Gutiérrez-Aguirre I, Ravnikar, M, Kutnjak D. In-depth study of tomato and weed viromes reveals undiscovered plant virus diversity in an agroecosystem. Microbiome. 2023;11:60. https://doi.org/10.1186/s40168-023-01500-6
Gaafar YZA, Richert-Poggeler KR, Maass C, Vetten HJ, Ziebell H. Characterisation of a novel nucleorhabdovirus infecting alfalfa (Medicago sativa). Virol J. 2019;16:55. https://doi.org/10.1186/s12985-019-1147-3
Baek D, Lim S, Ju HJ, Kim HR, Lee SH, Moon JS. The complete genome sequence of apple rootstock virus A, a novel nucleorhabdovirus identified in apple rootstocks. Arch Virol. 2019;164:2641-4. https://doi.org/10.1007/s00705-019-04348-0
Jackson AO, Dietzgen RG, Fang RX, Goodin MM, Hogenhout SA, Deng M, Bragg JN. Plant rhabdoviruses.In: Mahy BWJ; Van Regenmortel MHV, editors. Encyclopedia of Virology. Amsterdam, Netherlands: Elsevier; 2008 p. 187-96. https://doi.org/10.1016/B978-012374410-4.00492-1
Wang Q, Ma X, Qian S, Zhou X, Sun K, Chen X, Zhou X, Jackson AO, Li Z. Rescue of a Plant Negative-Strand RNA Virus from Cloned cDNA: Insights into Enveloped Plant Virus Movement and Morphogenesis. PLoS Pathog. 2015;11:e1005223. https://doi.org/10.1371/journal.ppat.1005223
Sidharthan VK, Baranwal VK. Mining of the water hyssop (Bacopa monnieri) transcriptome reveals genome sequences of two putative novel rhabdoviruses and a solendovirus. Arch Virol. 2021;166:1985-1990. https://doi.org/10.1007/s00705-021-05061-7
Hu J, Miao T, Que K, Rahman MS, Zhang L, Dong X, Ji P, Dong J. Identification, molecular characterization and phylogenetic analysis of a novel nucleorhabdovirus infecting Paris polyphylla var. yunnanensis. Sci Rep. 2023;13:10040. https://doi.org/10.1038/s41598-023-37022-2
Jackson AO, Christie SR. Purification and some physiochemical properties of Sonchus yellow net virus. Virology. 1977;77:344-55. https://doi.org/10.1016/0042-6822(77)90431-7
Jackson AO, Wagner JDO. Procedures for plant rhabdovirus purification, polyribosome isolation, and replicase extraction. Methods Mol Biol. 1998;81:77-97. https://doi.org/10.1385/0-89603-385-6:77
Weiland JJ, Sharma Poudel R, Flobinus A, Cook DE, Secor GA, Bolton MD. RNAseq Analysis of Rhizomania-Infected Sugar Beet Provides the First Genome Sequence of Beet Necrotic Yellow Vein Virus from the USA and Identifies a Novel Alphanecrovirus and Putative Satellite Viruses. Viruses. 2020;12(6):626. https://doi.org/10.3390/v12060626
Barbas III CF, Burton DR, Scott JK, Silverman GJ. Quantitation of DNA and RNA. Cold Spring Harb Protoc. 2007;pdb.ip47. https://doi.org/10.1101/pdb.ip47
Aiyar A. The Use of CLUSTAL W and CLUSTAL X for Multiple Sequence Alignment. In: Misener S, Krawetz SA, editors. Bioinformatics Methods and Protocols. Totowa, NJ: Humana Press; 2000. p. 221-41. (Methods in Molecular Biology™. Vol. 132). https://doi.org/10.1385/1-59259-192-2:221
Hall TA. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95-98.
Martin DP, Varsani A, Roumagnac P, Botha, G, Maslamoney S, Schwab T, Kelz Z, Kumar V, Murrell B. RDP5: A computer program for analyzing recombination in, and removing signals of recombination from, nucleotide sequence datasets. Virus Evol. 2021;7: veaa087. https://doi.org/10.1093/ve/veaa087
Kosugi S, Hasebe M, Tomita M, Yanagawa H. Systematic identification of yeast cell cycle-dependent nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci U S A. 2009;106:10171-6. https://doi.org/10.1073/pnas.0900604106
Nei M, Kumar S. Molecular Evolution and Phylogenetics. Oxford University Press, New York. 2000.
Le SQ, Gascuel O. An Improved General Amino Acid Replacement Matrix. Mol Biol Evol. 2008;25:1307-20. https://doi.org/10.1093/molbev/msn067
Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol. 2021;38:3022-7. https://doi.org/10.1093/molbev/msab120
Muhire BM, Varsani A, Martin DP. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One. 2014;9:e108277. https://doi.org/10.1371/journal.pone.0108277
Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol. 1992;9:678-87. https://doi.org/10.1093/oxfordjournals.molbev.a040752
Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299-302. https://doi.org/10.1093/molbev/msx248
Nei M. Molecular evolutionary genetics. New York: Columbia University Press; 1987. 512 p.
Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975;7:256-76. https://doi.org/10.1016/0040-5809(75)90020-9
Hudson RR, Slatkin, M, Maddison WP. Estimation of levels of gene flow from DNA sequence data. Genetics. 1992b;132:583-9. https://doi.org/10.1093/genetics/132.2.583
Hudson RR, Boos DD, Kaplan NL. A statistical test for detecting geographic subdivision. Mol Biol Evol. 1992a;9:138-51. https://doi.org/10.1093/oxfordjournals.molbev.a040703
Hudson RR. A new statistic for detecting genetic differentiation. Genetics. 2000;155:2011-4. https://doi.org/10.1093/genetics/155.4.2011
Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986;3:418-26. https://doi.org/10.1093/oxfordjournals.molbev.a040410
Šafářová D, Candresse T, Veselská J, Navrátil M. Novel Betanucleorhabdoviruses Infecting Elderberry (Sambucus nigra L.): Genome Characterization and Genetic Variability. Pathogens. 2024;13(6):445. https://doi.org/10.3390/pathogens13060445
Hartl DL, Clark AG. Principles of Population Genetics. 3rd ed. Sunderland: Sinauer Associates Inc. . 1997. 519 p.
Govindajuru RD. Variation in gene flow levels among predominantly selfpollinated plants. J Evol Biol. 1989;2:173-81. https://doi.org/10.1046/j.1420-9101.1989.2030173.x
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