The long noncoding RNA ALEX1 confers a functional phase state of ARF3 to enhance rice resistance to bacterial pathogens.

Abstract

Rice bacterial blight is a devastating disease worldwide, causing significant yield losses. Understanding how plants defend against microbial infection is critical for sustainable crop production. We previously identified a pathogen-induced long noncoding RNA (ALEX1). In this study, we show that ALEX1 localizes to the nucleus and directly binds to AUXIN RESPONSE FACTOR 3 (ARF3). We demonstrate that ARF3 forms condensates in the nucleus via its intrinsically disordered middle region (MR). Notably, ARF3 condensates takes on solid-like properties. We further revealed that ALEX1 directly binds to the MR of ARF3, regulating ARF3 condensate dynamics and promotes ARF3 homodimerization. The dispersed and dimeric form of ARF3, referred to as its functional phase state, enhances its ability to transcriptionally repress downstream target gene such as JAZ13, thereby modulating the jasmonic acid (JA) signaling pathway and strengthening pathogen resistance in rice. This study highlights the role of a long noncoding RNA in regulating protein condensation and assembly, contributing to pathogen defense in plants.