Summary: Plant hormones play a vital role in plant immune responses. However, in contrast to the relative wealth of information on hormone‐mediated immunity in dicot plants, little information is available on monocot–virus defense systems. We used a high‐throughput‐sequencing approach to compare the global gene expression of Rice black‐streaked dwarf virus (RBSDV)‐infected rice plants with that of healthy plants. Exogenous hormone applications and transgenic rice were used to test RBSDV infectivity and pathogenicity. Our results revealed that the jasmonic acid (JA) pathway was induced while the brassinosteroid (BR) pathway was suppressed in infected plants. Foliar application of methyl jasmonate (MeJA) or brassinazole (BRZ) resulted in a significant reduction in RBSDV incidence, while epibrassinolide (BL) treatment increased RBSDV infection. Infection studies using coi1‐13 and Go mutants demonstrated JA‐mediated resistance and BR‐mediated susceptibility to RBSDV infection. A mixture of MeJA and BL treatment resulted in a significant reduction in RBSDV infection compared with a single BL treatment. MeJA application efficiently suppressed the expression of BR pathway genes, and this inhibition depended on the JA coreceptor OsCOI1. Collectively, our results reveal that JA‐mediated defense can suppress the BR‐mediated susceptibility to RBSDV infection.

OsGSK2 directly interacts with and destabilizes OsJAZ4 to activate JA-mediated defense signaling.

Significance: Auxin signaling plays essential roles in almost every aspect of plant growth and development. Auxin response factors (ARFs) are key transcriptional regulators of auxin signaling. However, it is not clear what roles ARF transcription factors may play in plant–pathogen, and specifically plant–virus, interactions. This study reveals that an ARF transcription factor is targeted by several independently evolved viral proteins of very different plant RNA viruses. These viral proteins impede the ARF activity in different ways, but in each case, these interactions benefit viral infection. These findings demonstrate that manipulation of the auxin signaling by viral proteins is a common pathogenicity strategy in plant RNA viruses.

Summary: Auxin plays a fundamental role in plant growth and development, and also influences plant defence against various pathogens. Previous studies have examined the different roles of the auxin pathway during infection by biotrophic bacteria and necrotrophic fungi. We now show that the auxin signalling pathway was markedly down‐regulated following infection of rice by Rice black streaked dwarf virus (RBSDV), a dsRNA virus. Repression of the auxin receptor TIR1 by a mutant overexpressing miR393 increased rice susceptibility to RBSDV. Mutants overexpressing the auxin signalling repressors OsIAA20 and OsIAA31 were also more susceptible to RBSDV. The induction of jasmonic acid (JA) pathway genes in response to RBSDV was supressed in auxin signalling mutants, suggesting that activation of the JA pathway may be part of the auxin signalling‐mediated rice defence against RBSDV. More importantly, our results also revealed that OsRboh ‐mediated reactive oxygen species levels played important roles in this defence. The results offer novel insights into the regulatory mechanisms of auxin signalling in the rice–RBSDV interaction.

The functions of microRNA156 (miR156) and its targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factor genes in plant development have been widely investigated. However, the role of the miR156/SPLs regulatory network in plant immune systems remains obscure. Here, we found that the accumulation of reactive oxygen species (ROS) and the transcripts of basal salicylic acid (SA) signaling pathway genes were lower in Arabidopsis Pro35S:MIR156 seedlings (miR156 overexpression mutants) but higher in Pro35S:MIM156 (miR156 repression mutants) and ProSPL9:rSPL9 (SPL9 overexpression mutants) seedlings compared with wild-type Col-0 plants (WT). As a result, Pro35S:MIR156 mutants induced greater susceptibility to Pseudomonas syringae pv. tomato DC3000 following syringe infiltration than WT, while Pro35S:MIM156 and ProSPL9:rSPL9 mutants showed enhanced resistance. In addition, foliar H ₂ O ₂ application resulted in activation of SA-mediated defense response and ablation of miR156-induced susceptibility to P. syringae pv. tomato DC3000 infection. Collectively, our results provide new insights into the function of the miR156/SPL network in Arabidopsis immune response by regulating ROS accumulation and activating the SA signaling pathway.