The OsBDR1-MPK3 module negatively regulates blast resistance by suppressing the jasmonate signaling and terpenoid biosynthesis pathway

Abstract

Receptor-like kinases (RLKs) may initiate signaling pathways by perceiving and transmitting environmental signals to cellular machinery and play diverse roles in plant development and stress responses. The rice genome encodes more than one thousand RLKs, but only a small number have been characterized as receptors for phytohormones, polypeptides, elicitors, and effectors. Here, we screened the function of 11 RLKs in rice resistance to the blast fungus <i>Magnaporthe oryzae</i> (<i>M. oryzae</i>) and identified a negative regulator named BDR1 (Blast Disease Resistance 1). The expression of <i>BDR1</i> was rapidly increased under <i>M. oryzae</i> infection, while silencing or knockout of <i>BDR1</i> significantly enhanced <i>M. oryzae</i> resistance in two rice varieties. Protein interaction and kinase activity assays indicated that BDR1 directly interacted with and phosphorylated mitogen-activated kinase 3 (MPK3). Knockout of <i>BDR1</i> compromised <i>M. oryzae</i>-induced MPK3 phosphorylation levels. Moreover, transcriptome analysis revealed that <i>M. oryzae</i>-elicited jasmonate (JA) signaling and terpenoid biosynthesis pathway were negatively regulated by BDR1 and MPK3. Mutation of JA biosynthetic (<i>allene oxide cyclase</i> (<i>AOC</i>)/signaling (<i>MYC2</i>) genes decreased rice resistance to <i>M. oryzae.</i> Besides diterpenoid, the monoterpene linalool and the sesquiterpene caryophyllene were identified as unique defensive compounds against <i>M. oryzae</i>, and their biosynthesis genes (<i>TPS3</i> and <i>TPS29</i>) were transcriptionally regulated by JA signaling and suppressed by BDR1 and MPK3. These findings demonstrate the existence of a BDR1-MPK3 cascade that negatively mediates rice blast resistance by affecting JA-related defense responses.