A jasmonate-mediated MAPK cascade regulates rice structural defense against brown planthoppers.

Abstract

Mitogen-activated protein kinase (MAPK) cascades are multi-step signaling pathways that enable plants to respond to diverse environmental challenges. However, the precise mechanisms and components of MAPK cascades involved in defense responses against herbivores remain poorly understood. Here, we studied the biological function and regulatory mechanism of a herbivore-elicited MAPK cascade by transcriptional activation assays, genetic analysis, protein-protein interaction assays, comparative transcriptome analysis, and chemical quantification. We identified three tandemly arrayed MAPK kinase kinase (MKKK) genes (MKKK55, MKKK62, and MKKK70) on rice Chromosome 1, upregulated in response to brown planthopper (BPH) infestation. These genes are transcriptionally regulated by MYC2, the core regulator of jasmonate (JA) signaling in rice. These MKKKs, together with MKK3 and MPK7/14, form a MAPK cascade that mediates rice responses to herbivore attack. Mutations in any component genes increase rice susceptibility to BPH infestation. Mechanistically, this MAPK signaling cascade enhances physical defenses in rice by increasing cellulose deposition in sclerenchyma cell walls through the regulation of cellulose synthase genes. This study highlights the role of the MYC2-MKKK55/62/70-MKK3-MPK7/14 module in mediating a sector of JA-dependent rice defense against herbivores.