Two Novel Hypovirulence-Associated Mycoviruses in the Phytopathogenic Fungus : Molecular Characterization and Suppression of Infection Cushion Formation

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2018 May 15

PMID 29757259

Citations 35

Authors

Fangmin Hao

Ting Ding

Mingde Wu

Jing Zhang

Long Yang

Weidong Chen

Guoqing Li

Affiliations

Soon will be listed here.

Abstract

is a necrotrophic fungus causing disease on many important agricultural crops. Two novel mycoviruses, namely Botrytis cinerea hypovirus 1 (BcHV1) and Botrytis cinerea fusarivirus 1 (BcFV1), were fully sequenced. The genome of BcHV1 is 10,214 nt long excluding a poly-A tail and possesses one large open reading frame (ORF) encoding a polyprotein possessing several conserved domains including RNA-dependent RNA polymerase (RdRp), showing homology to hypovirus-encoded polyproteins. Phylogenetic analysis indicated that BcHV1 may belong to the proposed genus Betahypovirus in the viral family . The genome of BcFV1 is 8411 nt in length excluding the poly A tail and theoretically processes two major ORFs, namely ORF1 and ORF2. The larger ORF1 encoded polypeptide contains protein domains of an RdRp and a viral helicase, whereas the function of smaller ORF2 remains unknown. The BcFV1 was phylogenetically clustered with other fusariviruses forming an independent branch, indicating BcFV1 was a member in Fusariviridae. Both BcHV1 and BcFV1 were capable of being transmitted horizontally through hyphal anastomosis. Infection by BcHV1 alone caused attenuated virulence without affecting mycelial growth, significantly inhibited infection cushion (IC) formation, and altered expression of several IC-formation-associated genes. However, wound inoculation could fully rescue the virulence phenotype of the BcHV1 infected isolate. These results indicate the BcHV1-associated hypovirulence is caused by the viral influence on IC-formation-associated pathways.

Citing Articles

Exploring the interaction between endornavirus and : mechanisms of phytopathogenic fungal virulence and antivirus.

Mu F, Xia J, Jia J, Jiang D, Zhang B, Fu Y mBio. 2025; 16(3):e0336524.

PMID: 39969183 PMC: 11898685. DOI: 10.1128/mbio.03365-24.

A Mycovirus Representing a Novel Lineage and a Mitovirus of Co-Infect a Basidiomycetous Fungus, .

Duan J, Zhang A, Fu Y, Lin Y, Xie J, Cheng J Viruses. 2024; 16(11).

PMID: 39599881 PMC: 11598958. DOI: 10.3390/v16111767.

Mycologists and Virologists Align: Proposing for Global Mycovirus Studies.

Khalifa M, Ayllon M, Rodriguez Coy L, Plummer K, Gendall A, Chooi K Viruses. 2024; 16(9).

PMID: 39339959 PMC: 11437445. DOI: 10.3390/v16091483.

Diversity and impact of single-stranded RNA viruses in Czech populations.

Dalya L, Cerny M, de la Pena M, Poimala A, Vainio E, Hantula J mSystems. 2024; 9(10):e0050624.

PMID: 39287383 PMC: 11494978. DOI: 10.1128/msystems.00506-24.

The Effects of Mycovirus BmPV36 on the Cell Structure and Transcription of .

Wang Y, Li Q, Wu Y, Han S, Xiao Y, Kong L J Fungi (Basel). 2024; 10(2).

PMID: 38392805 PMC: 10890528. DOI: 10.3390/jof10020133.

References

Wang J, Wang F, Feng Y, Mi K, Chen Q, Shang J . Comparative vesicle proteomics reveals selective regulation of protein expression in chestnut blight fungus by a hypovirus. J Proteomics. 2012; 78:221-30. DOI: 10.1016/j.jprot.2012.08.013. View

Hu Z, Wu S, Cheng J, Fu Y, Jiang D, Xie J . Molecular characterization of two positive-strand RNA viruses co-infecting a hypovirulent strain of Sclerotinia sclerotiorum. Virology. 2014; 464-465:450-459. DOI: 10.1016/j.virol.2014.07.007. View

Li P, Zhang H, Chen X, Qiu D, Guo L . Molecular characterization of a novel hypovirus from the plant pathogenic fungus Fusarium graminearum. Virology. 2015; 481:151-60. DOI: 10.1016/j.virol.2015.02.047. View

Yaegashi H, Kanematsu S, Ito T . Molecular characterization of a new hypovirus infecting a phytopathogenic fungus, Valsa ceratosperma. Virus Res. 2012; 165(2):143-50. DOI: 10.1016/j.virusres.2012.02.008. View

Howitt R, Beever R, Pearson M, Forster R . Genome characterization of a flexuous rod-shaped mycovirus, Botrytis virus X, reveals high amino acid identity to genes from plant 'potex-like' viruses. Arch Virol. 2005; 151(3):563-79. DOI: 10.1007/s00705-005-0621-y. View

Leroch M, Mueller N, Hinsenkamp I, Hahn M . The signalling mucin Msb2 regulates surface sensing and host penetration via BMP1 MAP kinase signalling in Botrytis cinerea. Mol Plant Pathol. 2015; 16(8):787-98. PMC: 6638485. DOI: 10.1111/mpp.12234. View

Fan X, Zhang J, Yang L, Wu M, Chen W, Li G . Development of PCR-Based Assays for Detecting and Differentiating Three Species of Botrytis Infecting Broad Bean. Plant Dis. 2019; 99(5):691-698. DOI: 10.1094/PDIS-07-14-0701-RE. View

Smart C, Yuan W, Foglia R, Nuss D, Fulbright D, Hillman B . Cryphonectria hypovirus 3, a virus species in the family hypoviridae with a single open reading frame. Virology. 1999; 265(1):66-73. DOI: 10.1006/viro.1999.0039. View

Ghabrial S, Caston J, Jiang D, Nibert M, Suzuki N . 50-plus years of fungal viruses. Virology. 2015; 479-480:356-68. DOI: 10.1016/j.virol.2015.02.034. View

10.

Nerva L, Ciuffo M, Vallino M, Margaria P, Varese G, Gnavi G . Multiple approaches for the detection and characterization of viral and plasmid symbionts from a collection of marine fungi. Virus Res. 2015; 219:22-38. DOI: 10.1016/j.virusres.2015.10.028. View

11.

Yu L, Sang W, Wu M, Zhang J, Yang L, Zhou Y . Novel hypovirulence-associated RNA mycovirus in the plant-pathogenic fungus Botrytis cinerea: molecular and biological characterization. Appl Environ Microbiol. 2015; 81(7):2299-310. PMC: 4357927. DOI: 10.1128/AEM.03992-14. View

12.

Linder-Basso D, Dynek J, Hillman B . Genome analysis of Cryphonectria hypovirus 4, the most common hypovirus species in North America. Virology. 2005; 337(1):192-203. DOI: 10.1016/j.virol.2005.03.038. View

13.

Dawe A, Nuss D . Hypovirus molecular biology: from Koch's postulates to host self-recognition genes that restrict virus transmission. Adv Virus Res. 2013; 86:109-47. DOI: 10.1016/B978-0-12-394315-6.00005-2. View

14.

Zhong J, Shang H, Zhu C, Zhu J, Zhu H, Hu Y . Characterization of a novel single-stranded RNA virus, closely related to fusariviruses, infecting the plant pathogenic fungus Alternaria brassicicola. Virus Res. 2015; 217:1-7. DOI: 10.1016/j.virusres.2015.11.012. View

15.

Bashi T, Shovman O, Fridkin M, Volkov A, Barshack I, Blank M . Novel therapeutic compound tuftsin-phosphorylcholine attenuates collagen-induced arthritis. Clin Exp Immunol. 2015; 184(1):19-28. PMC: 4778098. DOI: 10.1111/cei.12745. View

16.

Feng H, Li G, Du S, Yang S, Li X, de Figueiredo P . The septin protein Sep4 facilitates host infection by plant fungal pathogens via mediating initiation of infection structure formation. Environ Microbiol. 2016; 19(5):1730-1749. DOI: 10.1111/1462-2920.13613. View

17.

Pearson M, Bailey A . Viruses of botrytis. Adv Virus Res. 2013; 86:249-72. DOI: 10.1016/B978-0-12-394315-6.00009-X. View

18.

Kunz C, Vandelle E, Rolland S, Poinssot B, Bruel C, Cimerman A . Characterization of a new, nonpathogenic mutant of Botrytis cinerea with impaired plant colonization capacity. New Phytol. 2006; 170(3):537-50. DOI: 10.1111/j.1469-8137.2006.01682.x. View

19.

Allen T, Dawe A, Nuss D . Use of cDNA microarrays to monitor transcriptional responses of the chestnut blight fungus Cryphonectria parasitica to infection by virulence-attenuating hypoviruses. Eukaryot Cell. 2003; 2(6):1253-65. PMC: 326648. DOI: 10.1128/EC.2.6.1253-1265.2003. View

20.

Xiao X, Xie J, Cheng J, Li G, Yi X, Jiang D . Novel secretory protein Ss-Caf1 of the plant-pathogenic fungus Sclerotinia sclerotiorum is required for host penetration and normal sclerotial development. Mol Plant Microbe Interact. 2013; 27(1):40-55. DOI: 10.1094/MPMI-05-13-0145-R. View