Virus-Mediated Suppression of Host Non-Self Recognition Facilitates Horizontal Transmission of Heterologous Viruses

Authors

Songsong Wu, Huazhong Agricultural University, China
Jiasen Cheng, Huazhong Agricultural University, China
Yanping Fu, Huazhong Agricultural University, China
Tao Chen, Huazhong Agricultural University, China
Daohong Jiang, Huazhong Agricultural University, China
Said A. Ghabrial, University of KentuckyFollow
Jiatao Xie, Huazhong Agricultural University, China

Abstract

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.

Document Type

Article

Publication Date

3-23-2017

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.

Digital Object Identifier (DOI)

https://doi.org/10.1371/journal.ppat.1006234

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).

Related Content

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.

Repository Citation

Wu, Songsong; Cheng, Jiasen; Fu, Yanping; Chen, Tao; Jiang, Daohong; Ghabrial, Said A.; and Xie, Jiatao, "Virus-Mediated Suppression of Host Non-Self Recognition Facilitates Horizontal Transmission of Heterologous Viruses" (2017). Plant Pathology Faculty Publications. 68.
https://uknowledge.uky.edu/plantpath_facpub/68