Abstract
To date, partitiviruses, including gammapartitiviruses, have been extensively studied in various fungal hosts but have not been reported in Penicillium digitatum (also called green mold, the pathogenic fungus infecting citrus). In the present work, we isolated and molecularly characterized a double-stranded RNA (dsRNA) partitivirus from citrus green mold, which we have named “Penicillium digitatum gammapartitivirus 1” (PdGV1). The bisegmented genome of PdGV1 contains two dsRNA segments (dsRNA1 and dsRNA2) with a length of 1795 bp and 1622 bp, respectively. Each of the two genomic dsRNAs contains a single open reading frame encoding a putative RNA-dependent RNA polymerase (RdRp) and a coat protein (CP), respectively. Phylogenetic analysis based on RdRp and CP sequences showed that PdGV1 clustered with mycoviruses belonging to the genus Gammapartitivirus, family Partitiviridae, e.g., Penicillium stoloniferum virus S. The 5’- and 3’-untranslated regions (UTRs) of the PdGV1 genomic dsRNAs both contained unique conserved RNA motifs that have never been found in any other partitivirus. This is the first report of a new gammapartitivirus that infects the citrus-pathogenic fungus P. digitatum.
Similar content being viewed by others
References
Smilanick JL, Mansour MF, Mlikota Gabler F, Goodwine WR (2006) The effectiveness of pyrimethanil to inhibit germination of Penicillium digitatum and to control citrus green mold after harvest. Postharvest Biol Technol 4:75–85
Macarisin D, Cohen L, Eick A, Rafael G, Belausov E, Wisniewski M, Droby S (2007) Penicillium digitatum suppresses production of hydrogen peroxide in host tissue during infection of citrus fruit. Phytopathol 97:1491–1500
Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368
Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci 107:8387–8392
Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384
Zhang T, Jiang Y, Dong W (2014) A novel monopartite dsRNA virus isolated from the phytopathogenic fungus Ustilaginoidea virens and ancestrally related to a mitochondria-associated dsRNA in the green alga Bryopsis. Virology 462–463:227–235
Nibert ML, Ghabrial SA, Maiss E, Lesker T, Vainio EJ, Jiang D, Suzuki N (2014) Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Res 188:128–141
Niu Y, Zhang T, Zhu Y, Yuan Y, Wang S, Liu J, Liu D (2016) Isolation and characterization of a novel mycovirus from Penicillium digitatum. Virology 494:15–22
Niu YH, Yuan YZ, Mao JL, Yang Z, Cao QW, Zhang TF, Wang SQ, Liu DL (2018) Characterization of two novel mycoviruses from Penicillium digitatum and the related fungicide resistance analysis. Scient Rep 8:5513
Pandey B, Naidu RA, Grove GG (2018) Detection and analysis of mycovirus—related RNA viruses from grape powdery mildew fungus Erysiphe necator. Arch Virol 163:1019–1030
Sotaro C, Lakha S, Lin YH, Sasaki A, Satoko K, Suzuki N (2009) A novel bipartite double-stranded RNA mycovirus from the white root rot fungus Rosellinia necatrix: molecular and biological characterization, taxonomic considerations, and potential for biological control. J Virol 24:12801–12812
Darissa O, Willingmann P, Adam G (2010) Optimized approaches for the sequence determination of double-stranded RNA templates. J Virol Methods 169:397–403
Coutts RHA, Livieratos IC (2003) A rapid method for sequencing the 5’- and 3’-termini of dsRNA viral templates using RLM-RACE. J Phytopathol 151:525–527
Thapa V, Turner GG, Hafenstein S, Overton BE, Vanderwolf KJ, Roossinck MJ (2016) Using a novel partitivirus in Pseudogymnoascus destructans to understand the epidemiology of White-nose syndrome. PLoS Pathog 12(12):e1006076
Yu JX, Zhu JZ, Wang Y, Zhang CJ, Zhong J, Zhu HJ, Gao BD, Zhou Q (2018) Molecular characterization of a putative gammapartitivirus in the phytopathogenic fungus Nigrospora oryzae. Arch Virol 163:1091–1095
Kim JW, Kim SY, Kim KM (2003) Genome organization and expression of Penicillium stoloniferum virus S. Virus Genes 27:249–256
Hacker CV, Brasier CM, Buck KW (2006) Determination of the 5’- and 3’-terminal sequences completes the sequences of the two double-stranded RNAs of Penicillium stoloniferum virus S. Virus Genes 32:137–138
Leticia B, Tero TT, Jarkko H, Julio JD, Libor J (2015) The European race of Gremmeniella abietina hosts a single species of Gammapartitivirus showing a global distribution and possible recombinant events in its history. Fungal Biol 119:125–135
Cañizares MC, Pérez-Artés E, García-Pedrajas NE, García-Pedrajas MD (2015) Characterization of a new partitivirus strain in Verticillium dahlia provides further evidence of the spread of the highly virulent defoliating pathotype through new introductions. Phytopathol Mediterr 54:516–523
Rong R, Rao S, Scott SW, Carner GR, Tainter FH (2002) Complete sequence of the genome of two dsRNA viruses from Discula destructiva. Virus Res 90:217–224
Bhatti MF, Bignell EM, Coutts RHA (2011) Complete nucleotide sequences of two dsRNAs associated with a new partitivirus infecting Aspergillus fumigatus. Arch Virol 156:1677–1680
Crawford LJ, Osman TAM, Coutts RHA, Buck KW (2006) Molecular characterization of a partitivirus from Ophiostoma himal-ulmi. Virus Genes 33:33–39
Nogawa M, Kgeyama T, Nakatani A, Taguchi G, Shimosaka M (1996) Cloning and characterization of mycovirus double-straned RNA from the plant pathogenic fungus, Fusarium solani f. sp. Robiniae +. Biosci Biotech Biochem 60:784–788
Liu WX, Duns G, Chen JS (2008) Genomic characterization of a novel partitivirus infecting Aspergillus ochraceus. Virus Genes 37:322–327
Svanella-Dumas L, Theil S, Barret M, Candresse T (2018) Complete genomic sequence of Raphanus sativus cryptic virus 4 (RsCV4), a novel alphapartitivirus from radish. Arch Virol 163:1097–1100
Zhong J, Chen D, Lei X, Zhu H, Zhu J, Gao B (2014) Detection and characterization of a novel Gammapartitivirus in the phytopathogenic fungus Colletotrichum acutatum strain HNZJ001. Virus Res 190:104–109
Acknowledgments
This work was supported by the National Natural Science Foundation of China (No.31371893 and 31071653), the Self-Determined Research Funds of CCNU from the Colleges’ Basic Research and Operation of MOE (No. CCNU17CG003), and the Open Funding from Hubei Key Laboratory of Economic Forest Germplasm Improvement and Resources Comprehensive Utilization (No. 2017BW03). We sincerely thank Dr. Huazhong Shi (Department of Chemistry and Biochemistry, Texas Tech University, USA) for English language editing.
Funding
This work was financially supported by the National Natural Science Foundations of China (No. 31371893 and 31071653), the Self-Determined Research Funds of CCNU from the Colleges’ Basic Research and Operation of MOE (No. CCNU17CG003), and the Open Funding from Hubei Key Laboratory of Economic Forest Germplasm Improvement and Resources Comprehensive Utilization (No. 2017BW03).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Handling Editor: Robert H.A. Coutts.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yang, Z., Geng, H., Zheng, Y. et al. Molecular characterization of a new gammapartitivirus isolated from the citrus-pathogenic fungus Penicillium digitatum. Arch Virol 163, 3185–3189 (2018). https://doi.org/10.1007/s00705-018-3951-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-018-3951-2