For best viewing of the website please use Mozilla Firefox or Google Chrome.
Citation: Assane Hamidou Abdoulaye, Jichun Jia, Aqleem Abbas, Du Hai, Jiasen Cheng, Yanping Fu, Yang Lin, Daohong Jiang, Jiatao Xie. Fusarivirus accessory helicases present an evolutionary link for viruses infecting plants and fungi [J].VIROLOGICA SINICA, 2022, 37(3) : 427-436.  http://dx.doi.org/10.1016/j.virs.2022.03.010

Fusarivirus accessory helicases present an evolutionary link for viruses infecting plants and fungi

  • Corresponding author: Jiatao Xie, jiataoxie@mail.hzau.edu.cn
  • Received Date: 13 July 2021
    Accepted Date: 16 March 2022
    Available online: 18 March 2022
  • A significant number of mycoviruses have been identified that are related to plant viruses, but their evolutionary relationships are largely unexplored. A fusarivirus, Rhizoctonia solani fusarivirus 4 (RsFV4), was identified in phytopathogenic fungus Rhizoctonia solani (R. solani) strain XY74 co-infected by an alphaendornavirus. RsFV4 had a genome of 10,833 nt (excluding the poly-A tail), and consisted of four non-overlapping open reading frames (ORFs). ORF1 encodes an 825 aa protein containing a conserved helicase domain (Hel1). ORF3 encodes 1550 aa protein with two conserved domains, namely an RNA-dependent RNA polymerase (RdRp) and another helicase (Hel2). The ORF2 and ORF4 likely encode two hypothetical proteins (520 and 542 aa) with unknown functions. The phylogenetic analysis based on Hel2 and RdRp suggest that RsFV4 was positioned within the fusarivirus group, but formed an independent branch with three previously reported fusariviruses of R. solani. Notably, the Hel1 and its relatives were phylogenetically closer to helicases of potyviruses and hypoviruses than fusariviruses, suggesting fusarivirus Hel1 formed an evolutionary link between these three virus groups. This finding provides evidence of the occurrence of a horizontal gene transfer or recombination event between mycoviruses and plant viruses or between mycoviruses. Our findings are likely to enhance the understanding of virus evolution and diversity.

  • 加载中
  • 10.1016j.virs.2022.03.010-ESM.docx
    1. Abdoulaye, A.H., Hai, D., Tang, Q., Jiang, D., Fu, Y., Cheng, J., Lin, Y., Li, B., KottaLoizou, I., Xie, J., 2021. Two distant helicases in one mycovirus:evidence of horizontal gene transfer between mycoviruses, coronaviruses and other nidoviruses.Virus Evol. 7 veab043.

    2. Ballut, L., Marchadier, B., Baguet, A., Tomasetto, C., Séraphin, B., Le Hir, H., 2005. The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat. Struct. Mol. Biol. 12, 861-869.

    3. Bonfante, P., Genre, A., 2010. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1, 1-11.

    4. Bowers, H.A., Maroney, P.A., Fairman, M.E., Kastner, B., Lührmann, R., Nilsen, T.W., Jankowsky, E., 2006. Discriminatory RNP remodeling by the DEAD-box protein DED1. RNA 12, 903-912.

    5. Bräutigam, A., Mullick, T., Schliesky, S., Weber, A.P., 2011. Critical assessment of assembly strategies for non-model species mRNA-Seq data and application of nextgeneration sequencing to the comparison of C3 and C4 species. J. Exp. Bot. 62, 3093-3102.

    6. Capella-Gutiérrez, S., Silla-Martínez, J.M., Gabaldon, T., 2009. trimAl:a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973.

    7. Castanho, B., Butler, E., Shepherd, R., 1978. The Association of double-stranded-RNA with Rhizoctonia decline. Phytopathology 68, 1515-1519.

    8. Chu, W.K., Hickson, I.D., 2009. RecQ helicases:multifunctional genome caretakers. Nat.Rev. Cancer 9, 644-654.

    9. Cordin, O., Banroques, J., Tanner, N.K., Linder, P., 2006. The DEAD-box protein family of RNA helicases. Gene 367, 17-37.

    10. Cui, S., Eisenächer, K., Kirchhofer, A., Brzozka, K., Lammens, A., Lammens, K., Fujita, T.,

    11. Conzelmann, K.K., Krug, A., Hopfner, K.P., 2008. The C-terminal regulatory domain is the RNA 50-triphosphate sensor of RIG-I. Mol. Cell 29, 169-179.

    12. Donaire, L., Pagán, I., Ayllon, M.A.J.V., 2016. Characterization of Botrytis cinerea negative-stranded RNA virus 1, a new mycovirus related to plant viruses, and a reconstruction of host pattern evolution in negative-sense ssRNA viruses. Virology 499, 212-218.

    13. Fairman-Williams, M.E., Guenther, U.P., Jankowsky, E., 2010. SF1 and SF2 helicases:family matters. Curr. Opin. Struct. Biol. 20, 313-324.

    14. Feng, H., Sun, Z., Li, H., Qin, P., Tang, C., Fu, R., Liu, Y., Li, P., Zheng, A., 2012. Preparation, purification and regeneration optimizing research of protoplasts from Rhizoctonia solani. Afr. J. Microbiol. Res. 6, 3222-3230.

    15. Garg, R., Patel, R.K., Tyagi, A.K., Jain, M., 2011. De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA Res. 18, 53-63.

    16. Ghabrial, S.A., Caston, J.R., Jiang, D., Nibert, M.L., Suzuki, N., 2015. 50-plus years of fungal viruses. Virology 479, 356-368.

    17. Gorbalenya, A.E., Koonin, E.V., 1993. Helicases:amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3, 419-429.

    18. Granato, L.M., Picchi, S.C., de Oliveira Andrade, M., Takita, M.A., de Souza, A.A., Wang, N., Machado, M.A., 2016. The ATP-dependent RNA helicase HrpB plays an important role in motility and biofilm formation in Xanthomonas citri subsp. citri.BMC Microbiol. 16, 1-14.

    19. Halls, C., Mohr, S., Del, C.M., Yang, Q., Jankowsky, E., Lambowitz, A.M., 2007. Involvement of DEAD-box proteins in group I and group II intron splicing. Biochemical characterization of Mss116p, ATP hydrolysis-dependent and-independent mechanisms, and general RNA chaperone activity. J. Mol. Biol. 365, 835-855.

    20. He, Y., Andersen, G.R., Nielsen, K.H., 2010. Structural basis for the function of DEAH helicases. EMBO Rep. 11, 180-186.

    21. Hrabáková, L., Grum-Grzhimaylo, A.A., Koloniuk, I., Debets, A.J., Sarkisova, T., Petrzik, K., 2017. The alkalophilic fungus Sodiomyces alkalinus hosts beta-and gammapartitiviruses together with a new fusarivirus. PLoS One 12, e0187799.

    22. Jankowsky, E., Gross, C.H., Shuman, S., Pyle, A.M., 2001. Active disruption of an RNAprotein interaction by a DExH/D RNA helicase. Science 291, 121-125.

    23. Jankowsky, E., 2011. RNA helicases at work:binding and rearranging. Trends Biochem. Sci. 36, 19-29.

    24. Jiang, D., Ghabrial, S.A., 2004. Molecular characterization of Penicillium chrysogenum virus:reconsideration of the taxonomy of the genus Chrysovirus. J. Gen. Virol. 85, 2111-2121.

    25. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K., Von Haeseler, A., Jermiin, L.S., 2017. ModelFinder:fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587-589.

    26. Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7:improvements in performance and usability. Mol. Biol. Evol. 30, 772-780.

    27. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., 2012. Geneious Basic:an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649.

    28. Koonin, E.V., Dolja, V.V., Morris, T.J., 1993. Evolution and taxonomy of positive-strand RNA viruses:implications of comparative analysis of amino acid sequences. Crit. Rev. Biochem. Mol. 28, 375-430.

    29. Koonin, E.V., Choi, G.H., Nuss, D.L., Shapira, R., Carrington, J.C., 1991. Evidence for common ancestry of a chestnut blight hypovirulence-associated double-stranded RNA and a group of positive-strand RNA plant viruses. Proc. Natl. Acad. Sci. U.S.A. 88, 10647-10651.

    30. Koonin, E.V., 1991. The phylogeny of RNA-dependent RNA polymerases of positivestrand RNA viruses. J. Gen. Virol. 72, 2197-2206.

    31. Kwon, S.J., Lim, W.S., Park, S.H., Park, M.R., Kim, K.H., 2007. Molecular characterization of a dsRNA mycovirus, Fusarium graminearum virus-DK21, which is phylogenetically related to hypoviruses but has a genome organization and gene expression strategy resembling those of plant potex-like viruses. Mol. Cell 23, 304-315.

    32. Larsen, N.B., Hickson, I.D., 2013. RecQ helicases:conserved guardians of genomic integrity. Adv. Exp. Med. Biol. 767, 161-184.

    33. Linder-Basso, D., Dynek, J.N., Hillman, B.I., 2005. Genome analysis of Cryphonectria hypovirus 4, the most common hypovirus species in North America. Virology 337, 192-203.

    34. Liu, C., Zeng, M., Zhang, M., Shu, C., Zhou, E., 2018. Complete nucleotide sequence of a partitivirus from Rhizoctonia solani AG-1 IA strain C24. Viruses 10, 703.

    35. Liu, H., Fu, Y., Jiang, D., Li, G., Xie, J., Cheng, J., et al., 2010. Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J. Virol. 84, 11876-11887.

    36. Liu, R., Cheng, J., Fu, Y., Jiang, D., Xie, J., 2015. Molecular Characterization of a novel positive-sense, single-stranded RNA mycovirus infecting the plant pathogenic fungus Sclerotinia sclerotiorum. Viruses 7, 2470-2484.

    37. Liu, W., Hai, D., Mu, F., Yu, X., Zhao, Y., He, B., Xie, J., Jiang, D., Liu, H., 2020. Molecular characterization of a novel fusarivirus infecting the plant-pathogenic fungus Botryosphaeria dothidea. Arch. Virol. 4, 165.

    38. Lyu, R., Zhang, Y., Tang, Q., Li, Y., Cheng, J., Fu, Y., Chen, T., Jiang, D., Xie, J., 2018. Two alphapartitiviruses co-infecting a single isolate of the plant pathogenic fungus Rhizoctonia solani. Arch. Virol. 163, 515-520.

    39. Malloch, D.W., Pirozynski, K.A., Raven, P.H., 1980. Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants (a review). Proc. Natl. Acad. Sci. U.S.A. 77, 2113-2118.

    40. Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., Von Haeseler, A., Lanfear, R., 2020. IQ-TREE 2:new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530-1534.

    41. Morozov, S.Y., Solovyev, A.G., 2015. Phylogenetic relationship of some "accessory" helicases of plant positive-stranded RNA viruses:toward understanding the evolution of triple gene block. Front. Microbiol. 6, 508.

    42. Picarelli, M.A.S., Forgia, M., Rivas, E.B., Nerva, L., Chiapello, M., Turina, M., Colariccio, A., 2019. Extreme diversity of mycoviruses present in isolates of Rhizoctonia solani AG2-2 LP from Zoysia japonica from Brazil. Front. Cell. Infect. Microbiol. 9, 244.

    43. Potgieter, A., Page, N., Liebenberg, J., Wright, I., Landt, O., Van Dijk, A., 2009. Improved strategies for sequence-independent amplification and sequencing of viral doublestranded RNA genomes. J. Gen. Virol. 90, 1423-1432.

    44. Redman, R.S., Sheehan, K.B., Stout, R.G., Rodriguez, R.J., Henson, J.M., 2002.Thermotolerance generated by plant/fungal symbiosis. Science 298, 1581-1581.

    45. Rodriguez, R., Redman, R.J., 2008. More than 400 million years of evolution and some plants still can't make it on their own:plant stress tolerance via fungal symbiosis.J. Exp. Bot. 59, 1109-1114.

    46. Rodriguez, R.J., White Jr., J.F., Arnold, A.E., Redman, R.S., 2009. Fungal endophytes:diversity and functional roles. New Phytol. 182, 314-330.

    47. Roossinck, M.J., 2019. Evolutionary and ecological links between plant and fungal viruses. New Phytol. 221, 86-92.

    48. Sankar, S., Porter, A.J., 1992. Point mutations which drastically affect the polymerization activity of encephalomyocarditis virus RNA-dependent RNA polymerase correspond to the active site of Escherichia coli DNA polymerase I. J. Biol. Chem. 267, 10168-10176.

    49. Shu, B., Gong, P., 2016. Structural basis of viral RNA-dependent RNA polymerase catalysis and translocation. Proc. Natl. Acad. Sci. U.S.A. 113, E4005-E4014.

    50. Singleton, M.R., Dillingham, M.S., Wigley, D.B., 2007. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76, 23-50.

    51. Smart, C., Yuan, W., Foglia, R., Nuss, D., Fulbright, D., Hillman, B., 1999. Cryphonectria hypovirus 3, a virus species in the family Hypoviridae with a single open reading frame. Virology 265, 66-73.

    52. Son, M., Yu, J., Kim, K.-H., 2015. Five questions about mycoviruses. PLoS Pathog. 11, e1005172.

    53. Su, C., Chao, Y.T., Alex Chang, Y.C., Chen, W.C., Chen, C.Y., Lee, A.Y., Hwa, K.T., Shih, M.C., 2011. De novo assembly of expressed transcripts and global analysis of the Phalaenopsis aphrodite transcriptome. Plant Cell Physiol. 52, 1501-1514.

    54. Tanner, N.K., Linder, P., 2001. DExD/H box RNA helicases:from generic motors to specific dissociation functions. Mol. Cell 8, 251-262.

    55. Theuser, M., Hobartner, C., Wahl, M.C., Santos, K.F., 2016. Substrate-assisted mechanism of RNP disruption by the spliceosomal Brr2 RNA helicase. Proc. Natl. Acad. Sci. U.S.A. 113, 7798-7803.

    56. Tuomivirta, T.T., Kaitera, J., Hantula, J., 2009. A novel putative virus of Gremmeniella abietina type B (Ascomycota:Helotiaceae) has a composite genome with endornavirus affinities. J. Gen. Virol. 90, 2299-2305.

    57. Wang, W., 2015. The molecular detection of Corynespora Cassiicola on cucumber by PCR assay using DNAman software and NCBI. In:International Conference on Computer and Computing Technologies in Agriculture. Springer, Cham, pp. 248-258.

    58. Wu, S., Cheng, J., Fu, Y., Chen, T., Jiang, D., Ghabrial, S.A., Xie, J., 2017. Virus-mediated suppression of host non-self recognition facilitates horizontal transmission of heterologous viruses. PLoS Pathog. 13, e1006234.

    59. Wylie, S.J., Adams, M., Chalam, C., Kreuze, J., Lopez-Moya, J.J., Ohshima, K., Praveen, S., Rabenstein, F., Stenger, D., Wang, A., Zerbini, F.M., 2017. ICTV virus taxonomy profile:Potyviridae. J. Gen. Virol. 98, 352.

    60. Xia, Y., Fei, B., He, J., Zhou, M., Zhang, D., Pan, L., Li, S., Liang, Y., Wang, L., Zhu, J., Li, P., 2017. Transcriptome analysis reveals the host selection fitness mechanisms of the Rhizoctonia solani AG-1IA pathogen. Sci. Rep. 7, 10120.

    61. Xie, J., Wei, D., Jiang, D., Fu, Y., Li, G., Ghabrial, S., Peng, Y., 2006. Characterization of debilitation-associated mycovirus infecting the plant-pathogenic fungus Sclerotinia sclerotiorum. J. Gen. Virol. 87, 241-249.

    62. Yang, Q., Jankowsky, E., 2005. ATP-and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemestry 44, 13591-13601.

    63. Zhang, M., Zheng, L., Liu, C., Shu, C., Zhou, E., 2018. Characterization of a novel dsRNA mycovirus isolated from strain A105 of Rhizoctonia solani AG-1 IA. Arch. Virol. 163, 427-430.

    64. Zhang, R., Liu, S., Chiba, S., Kondo, H., Kanematsu, S., Suzuki, N., 2014. A novel singlestranded RNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix, with similarity to hypo-like viruses. Front. Microbiol. 5, 360.

    65. Zhang, S., Grosse, F., 2004. Multiple functions of nuclear DNA helicase II (RNA helicase A) in nucleic acid metabolism. Acta Biochim. Biophys. Sin. 36, 177-183.

    66. Zheng, L., Liu, H., Zhang, M., Cao, X., Zhou, E., 2013. The complete genomic sequence of a novel mycovirus fromRhizoctonia solani AG-1 IA strainB275.Arch. Virol. 158,1609-1612.

    67. Zheng, L., Zhang, M., Chen, Q., Zhu, M., Zhou, E., 2014. A novel mycovirus closely related to viruses in the genus Alphapartitivirus confers hypovirulence in the phytopathogenic fungus Rhizoctonia solani. Virology 456, 220-226.

    68. Zheng, L., Shu, C., Zhang, M., Yang, M., Zhou, E., 2019. Molecular characterization of a novel endornavirus conferring hypovirulence in rice sheath blight fungus Rhizoctonia solani AG-1 IA strain GD-2. Viruses 11 (2), 178.

    69. Zhong, J., Chen, C.Y., Gao, B.D., 2015. Genome sequence of a novel mycovirus of Rhizoctonia solani, a plant pathogenic fungus. Virus Gene. 51, 167-170.

  • 加载中

Article Metrics

Article views(1216) PDF downloads(2) Cited by()

Related
Proportional views
    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Fusarivirus accessory helicases present an evolutionary link for viruses infecting plants and fungi

      Corresponding author: Jiatao Xie, jiataoxie@mail.hzau.edu.cn
    • a State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, 430070, China;
    • b Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China;
    • c Hubei Hongshan Laboratory, Wuhan, 430070, China

    Abstract: A significant number of mycoviruses have been identified that are related to plant viruses, but their evolutionary relationships are largely unexplored. A fusarivirus, Rhizoctonia solani fusarivirus 4 (RsFV4), was identified in phytopathogenic fungus Rhizoctonia solani (R. solani) strain XY74 co-infected by an alphaendornavirus. RsFV4 had a genome of 10,833 nt (excluding the poly-A tail), and consisted of four non-overlapping open reading frames (ORFs). ORF1 encodes an 825 aa protein containing a conserved helicase domain (Hel1). ORF3 encodes 1550 aa protein with two conserved domains, namely an RNA-dependent RNA polymerase (RdRp) and another helicase (Hel2). The ORF2 and ORF4 likely encode two hypothetical proteins (520 and 542 aa) with unknown functions. The phylogenetic analysis based on Hel2 and RdRp suggest that RsFV4 was positioned within the fusarivirus group, but formed an independent branch with three previously reported fusariviruses of R. solani. Notably, the Hel1 and its relatives were phylogenetically closer to helicases of potyviruses and hypoviruses than fusariviruses, suggesting fusarivirus Hel1 formed an evolutionary link between these three virus groups. This finding provides evidence of the occurrence of a horizontal gene transfer or recombination event between mycoviruses and plant viruses or between mycoviruses. Our findings are likely to enhance the understanding of virus evolution and diversity.

    Reference (69) Relative (20)

    目录

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return