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Molecular phylogenetic analysis shows that causal agent of maize rough dwarf disease in Iran is closer to rice black-streaked dwarf virus

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Abstract

Maize rough dwarf disease (MRDD) is one of the most important viral diseases around the world. Rice black-streaked dwarf virus (RBSDV) and maize rough dwarf virus (MRDV) cause MRDD in East Asia and Mediterranean regions, respectively. RBSDV and MRDV are similar in many features such as host range, disease symptoms, vector, and serological relationships, which make it hard to differentiate them based on serological and biological properties. However, molecular analyses as powerful tools could be used for differentiating species of fijiviruses. In this study, the complete genome sequence, genetic variation of 13 isolates using the nucleotide sequence of segment 10 ORF, and host range of MRDD causal agent in Iran were determined. Whole-genome comparisons and phylogenetic analysis showed that Iranian isolate shared high nucleotide sequence identities ranging from 86.5–91.3% and closest evolutionary relationship to the RBSDV Chinese isolates. The Iranian isolates showed over 99% homology based on amino acid sequence of ORF10 and were grouped in one clade through phylogenetic analysis. The results revealed that ORF10 of MRDD causal agent was under negative selection. Iranian isolate of MRDD was experimentally transmitted to maize, rice, barley, wheat, millet, oat, rye, and some grasses by Loadelphax striatellus with about 32% efficiency. The results of this study revealed that the MRDD causal agent in Iran had the closest genetic similarity to RBSDV demonstrating it is closer to RBSDV than MRDV.

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References

  • Achon, M. A., Serrano, L., Sabater, J., & Porta, C. (2015). Understanding the epidemiological factors that intensify the incidence of maize rough dwarf disease in Spain. Annals of Applied Biology, 166, 311–320.

    Article  CAS  Google Scholar 

  • Ali, A., Li, H., Schneider, W. L., Sherman, D. J., Gray, S., Smith, D., & Roossinck, M. J. (2006). Analysis of genetic bottlenecks during horizontal transmission of cucumber mosaic virus. Journal of Virology, 80, 8345–8350.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andorf, C. M., Cannon, E. K., Portwood, J. L., Gardiner, J. M., Harper, L. C., Schaeffer, M. L., Braun, B. L., Campbell, D. A., Vinnakota, A. G., & Sribalusu, V. V. (2016). MaizeGDB update: New tools, data and interface for the maize model organism database. Nucleic Acids Research, 44, 1195–1201.

    Article  CAS  Google Scholar 

  • Anzola, J. V., Xu, Z., Asamizu, T., & Nuss, D. L. (1987). Segment-specific inverted repeats found adjacent to conserved terminal sequences in wound tumour virus genome and defective interfering RNAs. Proceedings of the National Academy of Sciences of the United States of America, 84, 8301–8305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Attoui, H., Mertens, P. P. C., Becnel, J., Belaganahalli, S., Bergoin, M., Brussaard, C. P., et al. (2012) Family Reoviridae. In a. M. Q. King, M. J. Adams, E. B. Carstens, E. J. Lefkowitz (Eds) virus taxonomy: Classification and nomenclature of viruses. Ninth report of the international committee on taxonomy of viruses (pp. 541–637). London and San Diego: Academic press.

  • Azuhata, F., Uyeda, I., Kimura, I., & Shikata, E. (1993). Close similarity between genome structures of rice black-streaked dwarf and maize rough dwarf viruses. Journal of General Virology, 74, 1227–1232.

    Article  CAS  PubMed  Google Scholar 

  • Bai, F. W., Yan, J., Qu, Z. C., Zhang, H. W., Xu, J., Ye, M. M., & Shen, D. L. (2002). Phylogenetic analysis reveals that a dwarfing disease on different cereal crops in China is due to Rice black streaked dwarf virus (RBSDV). Virus Genes, 25, 201–206.

    Article  CAS  PubMed  Google Scholar 

  • Boccardo, G. & Milne, R. G. (1984) Plant reovirus group. CMI/AAB Descriptions of Plant Viruses, No. 294.

  • Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bong-Choon, L., Yeon-Kyu, H., Sung-Jun, H., Sung-Tae, P., & Key-Woon, L. (2005). Occurrence and detection of Rice black-streaked dwarf virus in Korea. Plant Pathology Journal, 21, 172–173.

    Article  Google Scholar 

  • Capella-Gutiérrez, S., Silla-Martínez, J. M., & Gabaldón, T. (2009). trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25, 1972–1973.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Distefano, A. J., Conci, L. R., Munoz Hidalgo, M., Guzman, F. A., Hopp, H. E., & del Vas, M. (2003). Sequence and phylogenetic analysis of genome segments S1, S2, S3 and S6 of mal de Río Cuarto virus, a newly accepted Fijivirus species. Virus Research, 92, 113–121.

    Article  CAS  PubMed  Google Scholar 

  • Dovas, C. I., Eythymiou, K., & Katis, N. I. (2004). First report of maize rough dwarf virus (MRDV) on maize crops in Greece. Plant Pathology, 53, 238.

    Article  Google Scholar 

  • Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giraldo, P., Benavente, E., Manzano-Agugliaro, F., & Gimenez, E. (2019). Worldwide research trends on wheat and barley: A Bibliometric comparative analysis. Agronomy, 9, 352. https://doi.org/10.3390/agronomy9070352.

    Article  Google Scholar 

  • Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., & Zeng, Q. (2011). Trinity: Reconstructing a full-length transcriptome without a genome from RNA-Seq data. National Biotechnology, 29, 644–652.

    Article  CAS  Google Scholar 

  • Hengmu, Z., Jianping, C., Juanli, L., & Michael, J. A. (2001). Sequence analysis shows that a dwarfing disease on rice, wheat and maize in China is caused by Rice black-streaked dwarf virus. European Journal of Plant Pathology, 107, 563–567.

    Article  Google Scholar 

  • Hortamani, M., Massah, A., & Izadpanah, K. (2018). Maize Iranian mosaic virus shows a descending transcript accumulation order in plant and insect hosts. Archives of Virology, 163, 887–893.

    Article  CAS  PubMed  Google Scholar 

  • Isogai, M., Uyeda, I., & Choi, J. K. (2001). Molecular diagnostic of Rice black-streaked dwarf virus in Japan and Korea. Plant Pathology Journal, 17, 164–168.

    Google Scholar 

  • Izadpanah, K., Ahmadi, A. A., & Jafari, S. A. (1983). Maize rough dwarf in Fars. Iranian Journal of Plant Pathology, 19, 25–29.

    Google Scholar 

  • Kamran, R., Izadpanah, K., & Ebrahim-Nesbat, F. (2000). Rice black-gall dwarf in Fars. Iranian Journal of Plant Pathology, 36, 281–295.

    Google Scholar 

  • King, A. M. Q., Adams, M. J., Carstens, E. B., & Leftkowitc, E. J. (2011). Ninth report of the international committee on taxonomy of viruses. Amsterdam: Academic Press.

    Google Scholar 

  • Kuribayashi, K., & Shinkai, A. (1952). On the new disease of Rice black-streaked dwarf (in Japanese). Annual Phytopathological Society of Japan, 16, 41.

    Google Scholar 

  • Lenardon, S. L., March, G. J., Nome, S. F., & Ornaghi, J. A. (1998). Recent outbreak of "mal de Rio Cuarto" virus on corn in Argentina. Plant Disease, 82, 448.

    Article  CAS  PubMed  Google Scholar 

  • Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., & Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078–2079.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li, Y. Q., Jia, M. G., Jiang, Z. D., Zhou, T., & Fan, Z. F. (2012). Molecular variation and recombination in RNA segment 10 of Rice black streaked dwarf virus isolated from China during 2007–2010. Archives of Virology, 157, 1351–1356.

    Article  CAS  PubMed  Google Scholar 

  • Marzachi, C., Boccardo, G., Milne, R., Isogai, M., & Uyeda, I. (1995). Genome structure and variability of Fijivirus. Seminars in Virology, 6, 103–108.

    Article  CAS  Google Scholar 

  • McMahon, J., Dale, J., & Harding, R. (1999). Taxonomic implications for Fijiviruses based on the terminal sequences of Fiji disease fijivirus. Archives of Virology, 144, 2259–2263.

    Article  CAS  PubMed  Google Scholar 

  • McQualter, R. B., Burns, P., Smith, G. R., Dale, J. L., & Harding, R. M. (2004). Molecular analysis of Fiji disease virus genome segments 5, 6, 8 and 10. Archives of Virology, 149, 713–721.

    Article  CAS  PubMed  Google Scholar 

  • Milne, R. G., & Lovisolo, O. (1977). Maize rough dwarf and related viruses. Advances in Virus Research, 21, 267–341.

    Article  CAS  PubMed  Google Scholar 

  • Milne, R. G., & Luisoni, E. (1977). Serological relationships among maize rough dwarf-like viruses. Virology, 80, 12–20.

    Article  CAS  PubMed  Google Scholar 

  • Mingfang, L., Li, X., Jian, Y., Jianping, C., & Heng-Mu, Z. (2016). Complete genomic sequence of maize rough dwarf virus, a fijivirus transmitted by the small brown planthopper. Genome Announcements, 4, e01529–e01515.

    Google Scholar 

  • Mirarab, S., & Warnow, T. (2015). ASTRAL-II: Coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics, 31, 44–52.

    Article  CAS  Google Scholar 

  • Nakashima, N., Koizumi, M., Watanabe, H., & Noda, H. (1996). Complete nucleotide sequence of the Nilaparvata lugens reovirus: A putative member of the genus Fijivirus. Journal of General Virology, 77, 139–146.

    Article  CAS  PubMed  Google Scholar 

  • Nuss, D. L., & Dall, D. J. (1990). Structural and functional properties of plant reovirus genomes. Advances in Virus Research, 38, 249–306.

    Article  CAS  PubMed  Google Scholar 

  • Rambaut, A. & Drummond, A. J. (2012) FigTree v1.4.0 in computer program and documentation distributed by the author. Internet resource: Research, software and publications of Andrew Rambaut and members of his research. http://tree.bio.ed.ac.uk/software/figtree.

  • Soorni, A., Borna, T., Alemardan, A., Chakrabarti, M., Hunt, A. G., & Bombarley, A. (2019). Transcriptom landscape variation in the genus thymus. Genes, 10, 620. https://doi.org/10.3390/genes10080620.

    Article  CAS  PubMed Central  Google Scholar 

  • Stamatakis, A., Ludwig, T., & Meier, H. (2005). RAxML-III: A fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics, 21, 456–463.

    Article  CAS  PubMed  Google Scholar 

  • Svanella-Dumas, L., Marais, A., Faure, C., Theil, S., Thibord, J. B., & Candresse, T. (2016). Complete nucleotide sequence of a French isolate of maize rough dwarf virus, a Fijivirus member in the family Reoviridae. Genome Announcements, 4, e00623–e00616.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uyeda, I., Bong-Choon, L., Ando, Y. (1998) Reovirus isolation and RNA extraction. In G. D Foster, S. C. Taylor. (Eds) Methods in Molecular Biology, Vol. 81: Plant virology protocols: From Virus Isolation to Transgenic Resistance (pp. 65-75). Totowa, New Jersey: Humana press.

  • Vaidya, G., Lohman, D. J., & Meier, R. (2011). SequenceMatrix: Concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27, 171–180.

    Article  PubMed  Google Scholar 

  • Wang, Z. H., Fang, S. G, Xu, J. L., Sun, L. Y., Li, D. W. & Yu, J. L. (2003) Sequence analysis of the complete genome of Rice black-streaked dwarf virus isolated from maize with rough dwarf disease. Virus Genes, 27, 163–168.

  • Wang, Q., Yang, J., Zhou, G. H., Zhang, H. M., Chen, J. P., & Adams, M. J. (2010). The complete genome sequence of two isolates of a new rice-infecting fijivirus from China. Journal of Phytopathology, 158, 733–737.

    Article  Google Scholar 

  • Yang, B. R., & Ma, Q. Y. (1983). Host range of maize rough dwarf virus disease. Acta Phytopathology Sinica, 13, 1–8.

    Google Scholar 

  • Zhang, H. M., Chen, J. P., Lei, J. L., & Adams, M. J. (2001). Sequence analysis shows that a dwarfing disease on rice, maize and wheat in China is caused by Rice black-streaked dwarf virus (RBSDV). European Journal of Plant Pathology, 107, 563–567.

    Article  CAS  Google Scholar 

  • Zhou, G. H., Wen, J. J., Cai, D. J., Li, P., Xu, D. L., & Zhang, S. G. (2008). Southern rice black-streaked dwarf virus: A new proposed Fijivirus species in the family Reoviridae. Chinese Science Bulletin, 53(23), 3677–3685.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Protection, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran

    Asieh Eyvazi & Amir Massah

  2. Department of Biotechnology, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran

    Aboozar Soorni

  3. Agriculture and Natural Resources Research Center of Shahrekord, Shahrekord, Iran

    Ghobad Babaie

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  1. Asieh Eyvazi
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  2. Amir Massah
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  3. Aboozar Soorni
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  4. Ghobad Babaie
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Correspondence to Amir Massah.

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They have no conflicts of interest.

We used the insects as vector in this work. All applicable international guidelines for the care and use of animals were followed.

This article contains no studies involving human participants performed by any of the authors.

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Eyvazi, A., Massah, A., Soorni, A. et al. Molecular phylogenetic analysis shows that causal agent of maize rough dwarf disease in Iran is closer to rice black-streaked dwarf virus. Eur J Plant Pathol 160, 411–425 (2021). https://doi.org/10.1007/s10658-021-02253-4

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