Wu Songsong, Cheng Jiasen, Fu Yanping, Chen Tao, Jiang Daohong, Ghabrial Said A, Xie Jiatao
State Key Laboratory of Agricultural Microbiology, The Provincial Key Lab of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China.
Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, United States of America.
PLoS Pathog. 2017 Mar 23;13(3):e1006234. doi: 10.1371/journal.ppat.1006234. eCollection 2017 Mar.
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.
非自我识别是生物体中的一种常见现象;它通常会引发先天免疫,以防止寄生虫的入侵并维持生物体的遗传多态性。真菌营养体不亲和性是一种非自我识别类型,它常常诱导程序性细胞死亡(PCD)并限制分子寄生虫的传播。目前尚不清楚病毒感染是否会减弱宿主个体间的非自我识别以促进其传播。在此,我们报道一种与低毒力相关的真菌病毒,命名为核盘菌真菌病毒4(SsMYRV4),它能够抑制宿主的非自我识别并促进异源病毒的水平传播。我们发现,在感染了SsMYRV4的核盘菌菌株与其他经测试的营养体不亲和菌株之间的混合菌落区域,细胞死亡明显减少,并且未清晰观察到抑制性屏障线。营养体不亲和性涉及异源三聚体鸟嘌呤核苷酸结合蛋白(G蛋白)信号通路,由特定的基因座即het(异核体不亲和性)基因座控制。活性氧(ROS)在营养体不亲和性介导的PCD中起关键作用。在存在SsMYRV4的情况下,G蛋白亚基基因、het基因和ROS相关基因的表达显著下调,并且细胞内ROS的产生受到抑制。此外,感染了SsMYRV4的菌株能够通过菌丝接触轻易接受其他病毒,并且这些病毒能够从感染了SsMYRV4的菌株高效传播到其他营养体不亲和的个体。因此,我们得出结论,SsMYRV4能够抑制宿主的非自我识别并促进异源病毒在宿主个体间的传播。这些发现可能会增进我们对病毒生态学的理解,并提供一种利用与低毒力相关的真菌病毒来控制真菌病害的潜在策略。