Non-self recognition is a common phenomenon among organisms; it often leads to innate immunity to prevent the invasion of parasites and maintain the genetic polymorphism of organisms. Fungal vegetative incompatibility is a type of non-self recognition which often induces programmed cell death (PCD) and restricts the spread of molecular parasites. It is not clearly known whether virus infection could attenuate non-self recognition among host individuals to facilitate its spread. Here, we report that a hypovirulence-associated mycoreovirus, named Sclerotinia sclerotiorum mycoreovirus 4 (SsMYRV4), could suppress host non-self recognition and facilitate horizontal transmission of heterologous viruses. We found that cell death in intermingled colony regions between SsMYRV4-infected Sclerotinia sclerotiorum strain and other tested vegetatively incompatible strains was markedly reduced and inhibition barrage lines were not clearly observed. Vegetative incompatibility, which involves Heterotrimeric guanine nucleotide-binding proteins (G proteins) signaling pathway, is controlled by specific loci termed het (heterokaryon incompatibility) loci. Reactive oxygen species (ROS) plays a key role in vegetative incompatibility-mediated PCD. The expression of G protein subunit genes, het genes, and ROS-related genes were significantly down-regulated, and cellular production of ROS was suppressed in the presence of SsMYRV4. Furthermore, SsMYRV4-infected strain could easily accept other viruses through hyphal contact and these viruses could be efficiently transmitted from SsMYRV4-infected strain to other vegetatively incompatible individuals. Thus, we concluded that SsMYRV4 is capable of suppressing host non-self recognition and facilitating heterologous viruses transmission among host individuals. These findings may enhance our understanding of virus ecology, and provide a potential strategy to utilize hypovirulence-associated mycoviruses to control fungal diseases.

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Notes/Citation Information

Published in PLOS Pathogens, v. 13, 3, e1006234, p. 1-25.

© 2017 Wu et al.

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Funding Information

This study was supported by the National Nature Science Foundation of China 31371982 (to JX), the China National Funds for Distinguished Young Scientists 31125023 (to DJ), the Special Fund for Agro-scientific Research in the Public Interest 201103016 (to DJ), the Key Project of the Chinese Ministry of Education 313024 (to DJ), the China Agriculture Research System CARS-13 (to DJ).

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All sequences reported in this paper are available from the NCBI database. The GenBank accession numbers for the full genome sequence of SsMYRV4 are KU128375 to KU128386; The expression data sets used in this study are available at the NCBI Gene Expression Omnibus (GEO) (http://www.ncbi.nlm.nih.gov/geo/) under accession number GSE94575.

journal.ppat.1006234.s001.tif (2125 kB)
S1 Fig. Biological characteristics of SsMYRV4-free strain Ep-1PNA367, and SsMYRV4-infected strains SX10 and Ep-1PNA367T1.

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S2 Fig. Transfection of protoplasts of S. sclerotiorum virulent strain Ep-1PNA367 with purified SsMYRV4 particles.

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S3 Fig. Genome size and organization of SsMYRV4.

journal.ppat.1006234.s004.tif (3367 kB)
S4 Fig. Amino acid sequence alignment of core RdRp motifs of SsMYRV4 and selected viruses from family Reoviridae.

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S5 Fig. SsMYRV4-mediated horizontal transmission of hypovirulence-associated heterologous viruses and consequent control of Sclerotinia diseases.

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S6 Fig. SsMYRV4-mediated enhancement of tolerance to environmental stress in S. sclerotiorum.

journal.ppat.1006234.s007.docx (17 kB)
S1 Table. Accession numbers of SsMYRV4 and sequence information compared with RnMYRV3.

journal.ppat.1006234.s008.docx (17 kB)
S2 Table. List of Reoviridae members used in phylogenetic analysis.

journal.ppat.1006234.s009.docx (39 kB)
S3 Table. Peptide mass fingerprinting analysis of purified particles preparations.

journal.ppat.1006234.s010.docx (17 kB)
S4 Table. Transmission efficiency of SsDRV and SsRV-L between different VCGs in presence or absence of SsMYRV4.

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S5 Table. Primers used in this study.