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. In this study, we show that ALEX1, a previously identified pathogen-induced long noncoding RNA, localizes to the nucleus and directly binds AUXIN RESPONSE FACTOR 3 (ARF3). We showed that ARF3 forms the condensates in the nucleus via its intrinsically disordered middle region (MR), and that these ARF3 condensates display solid-like properties. We further revealed that ALEX1 directly binds the MR of ARF3 to regulate ARF3 condensate dynamics and promote ARF3 homodimerization. The dispersed, dimeric form of ARF3, referred to as its functional phase state, enhances its ability to transcriptionally repress the expression of downstream target genes such as JAZ13, thereby modulating the jasmonic acid signaling pathway and enhancing pathogen resistance in rice. Collectively, this study reveals the role of a long noncoding RNA in regulating protein condensation and complex assembly, thus contributing to plant pathogen resistance.