Auxin response factors (ARFs) differentially regulate rice antiviral immune response against rice dwarf virus

There are 25 auxin response factors (ARFs) in the rice genome, which play critical roles in regulating myriad aspects of plant development, but their role (s) in host antiviral immune defense and the underneath mechanism remain largely unknown. By using the rice-rice dwarf virus (RDV) model system, here we report that auxin signaling enhances rice defense against RDV infection. In turn, RDV infection triggers increased auxin biosynthesis and accumulation in rice, and that treatment with exogenous auxin reduces OsIAA10 protein level, thereby unleashing a group of OsIAA10-interacting OsARFs to mediate downstream antiviral responses. Strikingly, our genetic data showed that loss-of-function mutants of osarf12 or osarf16 exhibit reduced resistance whereas osarf11 mutants display enhanced resistance to RDV. In turn, OsARF12 activates the down-stream OsWRKY13 expression through direct binding to its promoter, loss-of-function mutants of oswrky13 exhibit reduced resistance. These results demonstrated that OsARF 11, 12 and 16 differentially regulate rice antiviral defense. Together with our previous discovery that the viral P2 protein stabilizes OsIAA10 protein via thwarting its interaction with OsTIR1 to enhance viral infection and pathogenesis, our results reveal a novel auxin-IAA10-ARFs-mediated signaling mechanism employed by rice and RDV for defense and counter defense responses. Author summary The phytohormone auxin is often critical for plant growth and orchestrates many developmental processes. Here we find that rice accumulates more auxin upon RDV infection and treatment with exogenous auxin enhances rice tolerance to RDV infection. Auxin treatment reduces the protein level of OsIAA10, thus releasing a group of OsIAA10-interacting OsARFs to mediate downstream antiviral responses. Among the 25 ARFs in the rice genome, their functions on regulation of rice antiviral defense are diversified. Our findings elucidate a novel auxin-OsIAA10-ARFs-mediated signaling mechanism employed by rice and RDV for defense and counter defense responses. These findings significantly deepen our understanding of virus-host interactions and provide novel targets for molecular breeding (or engineering) rice cultivars resistant to RDV.