Research Progress in Plant Antiviral Silencing: Argonaute-Centered Perspective

In the long-term evolution process, plants have evolved multi-layered defense mechanisms to sense and respond to the invasion of harmful organisms such as viruses, to adapt to the adverse environment and avoid attacks from harmful organisms. Similarly, in order to infect host plants, viruses have evolved counter-defense strategies. RNA silencing plays an important role in plant antiviral defense mechanisms, and Argonaute (AGO), as the core component of the RNA-induced silencing complex, is crucial in plant antiviral defense. This review describes that AGO participates in the molecular arms race between plants and viruses through gene silencing mediated by small RNA or DNA methylation. AGO targets complementary viral RNA or DNA by binding to virus-derived small RNA, and degradation of viruses at transcriptional or post-transcriptional levels; or with endogenous small RNA to regulate host gene expression. To successfully cause virus disease, plant viruses have evolved viral suppressor (VSR). By binding viral siRNA, double-stranded RNA or directly interacting with AGO protein, VSR inhibits the host's RNA silencing and defense system, successfully achieving virus infection. In nature, the coevolution of plants and viruses causes natural variation in the RNA silencing component of AGO protein, allowing it to evolve diversified functions in response to different virus attacks. AGO protein acts as a positive regulator in host antiviral defense and is required for resistance against broad-spectrum plant viruses. Meanwhile, the natural selection pressure endowed AGOs with polymorphism, so that then have diversified antiviral activities. AGO protein can also act as a negative regulator of host antiviral defense, promoting the infection of the double-stranded RNA virus of Fijivirus. AGO protein has antiviral activity and broad-spectrum resistance to various viruses. It can also be hijacked by viruses and used as a specific virus attack strategy to inhibit rice resistance. The discovery of host silencing factors necessary for antiviral RNA silencing will provide new ideas for RNA silencing pathways and antiviral functions. In summary, this review systematically elaborates on the recent progress of the function and mechanism of AGO protein in antiviral defense, and discusses the diversity strategies of AGO protein in response to different virus attacks. It provides theoretical support for broad-spectrum antiviral breeding of crops.