MicroRNAs control resistance to viral pathogens
The miRNA-mediated gene regulation has emerged as a novel strategy to enhance antiviral defenses in crop plants (Ding & Voinnet 2007). Plants have evolved different RNA silencing mechanisms to respond to diverse classes of viral infections. Antiviral RNA silencing is triggered by virus-derived double-stranded RNA (dsRNA) that are directly recognized and processed by the host dicer-like proteins (DCL) to form virus-derived small-interfering RNAs (vsiRNAs) (Baulcombe 2004). The vsiRNAs are incorporated to the ARGONAUTE (AGO ) proteins that form the core component of RNA-induced silencing complex (RISC). The functional RISC either cleaves the viral RNA or arrests the viral protein translation. Single-stranded viral RNAs require endogenous RNA-dependent RNA polymerases (RDRs) to synthesize dsRNA that serves as the substrate for DCLs to produce secondary vsiRNAs. To counteract the defense response of plant, most viruses have developed specialized proteins known as viral suppressors of RNA silencing (VSRs) that impede the antiviral RNA silencing pathway and suppress the defense response (Csorba, Kontra & Burgyán 2015).
MicroRNAs provide an additional layer of intrinsic defense against viral attack. In rice, the Osa-miR528 is well characterized and known to be involved in the regulation of defenses against the rice stripe virus (RSV). The Osa-miR528 is sequestered away from AGO1by cleavage-defective AGO18 of rice, which is known to be monocot-specific, upon RSV infection. This in turn prevents the formation of functional RNA induced silencing complex. These events further lead to the enhanced expression of downstream gene AO, which encode for, L-ascorbate oxidase, and functions by initiating the resistance response against RSV through enhanced accumulation of reactive oxygen species (ROS) (Wu et al. 2017a). Further research suggested that the transcription factor OsSPL9 specifically regulates the expression of the Osa-miR528-AO module by binding to the promoter of the Osa-miR528 . Mutation in the OsSPL9has been shown to cause the dramatic downregulation of Osa-miR528thereby inducing the expression of AO that leads to enhanced resistance to RSV (Yao et al. 2019).
The AGO18 also sequester the Osa-miR168 upon RSV infection. It has been shown that AGO18 competes with AGO1 for binding to Osa-miR168 resulting in an elevated level ofAGO1 -mediated resistance (Wu et al., 2015). RSV invasion triggered the expression of Osa-miR444 , which positively regulates the immunity against viral pathogen. Transgenic plant overexpressing the Osa-miR444 displayed a broad-spectrum resistance to RSV by inducing OsRDR1 and silencing severalMADS box genes (Wang et al. 2016).
RSV infection perturbs the expression of Osa-miR171 . Reduced accumulation of Osa-miR171 has been shown to severely affect plant height and chlorophyll content and caused the RSV-like symptoms in rice. Plants expressing miR171b were less susceptible to RSV and attenuate RSV symptoms (Tong et al. 2017). In rice, theOsa-miR319 acts as a negative regulator of antiviral immunity against ragged stunt virus (RRSV). Transgenic plants overexpressing theOsa-miR319 exhibit severe disease like symptoms by down regulating target gene OsTCP21 (TEOSINTE BRANCHED/CYCLOIDEA/PCF ) and suppressing JA-mediated plant defense pathways (Zhang et al. 2016).