A planthopper-secreted miRNA facilitates viral infection by disrupting plant growth-defense balance in rice.

Abstract

Insect vectors can enhance the pathogenicity of plant arboviruses, yet the molecular mechanisms driving this cross-kingdom manipulation remain elusive. Here, we demonstrate that white-backed planthoppers secrete a specific microRNA, miR-133, into rice to facilitate southern rice black-streaked dwarf virus (SRBSDV) infection. Mechanistically, insect-derived miR-133 functions via cross-kingdom RNA interference to directly repress the GOLDEN2-LIKE transcription factor 31 (OsGLK31). OsGLK31 acts as a dual regulator that promotes growth via OsYUCCA-mediated auxin biosynthesis and confers antiviral immunity through OsLOX11-mediated jasmonic acid (JA) biosynthesis. In the absence of infection, the plant repressor OsJAZ10 binds to OsGLK31 to specifically inhibit its immune function, thereby prioritizing growth. However, insect infestation disrupts this balance: insect-secreted miR-133 represses OsGLK31 expression, while OsJAZ10 blocks the transcriptional activity of residual OsGLK31 protein on OsLOX11. This coordinated blockade suppresses both auxin and JA biosynthesis, causing severe dwarfism and dampened viral resistance. Our findings reveal miR-133 as a cross-kingdom effector that disrupts the host plant growth-defense balance to pave the way for viral invasion, offering potential targets for antiviral crop improvement.