Transcriptional landscape of pathogen‐responsive lncRNAs in rice unveils the role of ALEX1 in jasmonate pathway and disease resistance

Abstract

Summary Plant defence is multilayered and is essential for surviving in a changing environment. The discovery of long noncoding RNAs (lncRNAs) has dramatically extended our understanding of post‐transcriptional gene regulation in diverse biological processes. However, the expression profile and function of lncRNAs in disease resistance are still largely unknown, especially in monocots. Here, we performed strand‐specific RNA sequencing of rice leaves infected by Xanthomonas oryzae pv. Oryzae (Xoo) in different time courses and systematically identified 567 disease‐responsive rice lncRNAs. Target analyses of these lncRNAs showed that jasmonate (JA) pathway was significantly enriched. To reveal the interaction between lncRNAs and JA‐related genes, we studied the coexpression of them and found 39 JA‐related protein‐coding genes to be interplayed with 73 lncRNAs, highlighting the potential modulation of lncRNAs in JA pathway. We subsequently identified an lncRNA, ALEX1, whose expression is highly induced by Xoo infection. A T‐DNA insertion line constructed using enhancer trap system showed a higher expression of ALEX1 and exerted a significant resistance to rice bacterial blight. Functional study revealed that JA signalling is activated and the endogenous content of JA and JA‐Ile is increased. Overexpressing ALEX1 in rice further confirmed the activation of JA pathway and resistance to bacterial blight. Our findings reveal the expression of pathogen‐responsive lncRNAs in rice and provide novel insights into the connection between lncRNAs and JA pathway in the regulation of plant disease resistance.

Discovery, Identification, and Functional Characterization of Long Noncoding RNAs in Arachis hypogaea L.

“…In tomato, a plausible model for TYLCV-induced diseases and host antiviral immunity was uncovered; that is, lncRNAs interact with the IR-derived vsRNAs to control disease development during TYLCV infection, which provide an effective strategy for the control of plant viral pathogens [67]. In rice, the connection between lncRNAs and the JA pathway in the regulation of bacterial blight was confirmed, which provided a novel insight into plant disease resistance [68].…”

“…Furthermore, many studies reported that lncRNAs play important roles in plant defense against pathogens [66][67][68]. In tomato, a plausible model for TYLCV-induced diseases and host antiviral immunity was uncovered; that is, lncRNAs interact with the IR-derived vsRNAs to control disease development during TYLCV infection, which provide an effective strategy for the control of plant viral pathogens [67].…”

Research Progress on Plant Long Non-Coding RNA

“…The basic strategy for the functional verification of plant lncRNAs is still a strategy based on acquisition/loss of function, i.e., studies on lncRNA overexpression based on genetic transformation platforms or loss-of-function studies based on clustered regularly interspaced short palindromic repeat (CRISPR)-associated protein 9 (Cas9) systems, RNAi and siRNA. Yu et al [52] obtained lncRNA ALEX1 (a full-length of 294 nt) through the rapid amplification of cDNA ends (RACE) technology, and the construction of an overexpression vector and genetic transformation revealed that ALEX1 could activate the jasmonic acid signaling pathway and affect resistance to bacterial blight in rice. Cui et al [43] analyzed the overexpression and silencing of lncRNA33732 in tomatoes and found that lncRNA33732 can enhance the resistance of tomatoes to Phytophthora infestans by inducing the expression of respiratory oxidase homolog (RBOH) and the accumulation of H 2 O 2 .…”

Functional Analysis of Long Non-Coding RNAs Reveal Their Novel Roles in Biocontrol of Bacteria-Induced Tomato Resistance to Meloidogyne incognita

“…The rice lncRNAs in response to the infection of Xanthomonas oryzae pv. was identified, and the regulation of lncRNA-mediated JA pathway on rice resistance was described [32]. Some lncRNAs have recently been identified in plants but limited studies have investigated whether biocontrol bacteria induce plant resistance to diseases.…”