Advances in Plant Antiviral RNAi: From Host DCLs/RDRs to Diversified Viral Counteracting Strategies

Plant RNA interference (RNAi) is a fundamental antiviral defense that relies on coordinated activities of DICER-like endonucleases (DCLs), Argonaute proteins (AGOs) and RNA-dependent RNA polymerases (RDRs). Over the past decades, studies using model and crop species have uncovered complex and often redundant roles for DCLs and RDRs in generating and amplifying virus-derived small interfering RNAs (vsiRNAs), in addition to connections with transcriptional gene silencing (TGS) and epigenetic defenses against DNA viruses. Concurrently, plant viruses have evolved diverse counterstrategies-proteinaceous RNA silencing suppressors (RSSs), exoribonuclease (XRN)-resistant noncoding RNAs, and indirect manipulation of host pathways-to evade RNAi. Driven by the co-evolutionary arms race, plants have developed sophisticated counter-countermeasures that modulate or overcome viral anti-RNAi activity. Accumulated evidence suggests that plants encode host factor genes that are activated to degrade or sequester viral components such as RSSs against viral infection. On the other hand, plants have also evolved endogenous host modulators of antiviral RNAi that can either reinforce the antiviral response or be co-opted by viruses to antagonize it, representing a furious dynamic molecular battling mechanism. Here, we review recent advances in the molecular functions of DCLs and RDRs across species, summarize newly discovered viral counter-defenses (including RNA-based suppressors), and discuss host counter-countermeasures. We research key areas-such as the roles of RDRγ-class proteins, RTL1 (RNase three-like 1)-mediated competition with DCLs, and the mechanistic impact of viral noncoding RNAs-and outline translational opportunities for improving virus resistance in crops through breeding, biotechnological approaches, and RNA-based applications.