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.
Highlights
Non-self recognition is a universal phenomenon among all organisms [1,2,3,4]
The hypovirulence-associated Sclerotinia sclerotiorum mycoreovirus 4 (SsMYRV4), was found to function as a potent inhibitor of G protein signaling pathway, Reactive oxygen species (ROS) production and vegetative incompatibility-mediated programmed cell death (PCD). This SsMYRV4-mediated unique feature enables horizontal transmission of heterologous mycoviruses among vegetatively incompatible S. sclerotiorum individuals in an interaction system (SsMYRV4/S. sclerotiorum) to create a bridge donor strain for mycovirus spread under natural conditions
Strain SX10 exhibits hypovirulence traits similar to those previously reported in S. sclerotiorum strains infected with diverse RNA or DNA mycoviruses [27]
Summary
Non-self recognition is a universal phenomenon among all organisms [1,2,3,4]. Non-self recognition as a fundamental attribute of cell-cell interactions occurs widely among organisms. Non-self recognition is often a major limiting factor for successful organ transplantation [11], and spread of viruses among individuals [12]. $ Strain Ep-1PNA367PT1 was a transfectant of strain Ep-1PNA367 with SsMYRV4 purified particles. To define whether SsMYRV4 is responsible for phenotypic traits of strain SX10 as compared with strain Ep-1PNA367R, SsMYRV4 was successfully transferred from strain SX10 to strain Ep-1PNA367R via horizontal transmission (Fig 1A), and confirmed by dsRNA extraction and subculturing on PDA medium containing hygromycin. Introduction of purified SsMYRV4 particles into strain Ep-1PNA367 resulted in reductions in virulence and mycelial growth (S2 Fig). Combination of virus transfection and transmission results suggested that SsMYRV4 is associated with debilitation symptoms of S. sclerotiorum
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