Extracellular pyridine nucleotides trigger plant systemic immunity through a lectin receptor kinase/BAK1 complex

Chenggang Wang,Zhonglin Mou,Qi Li,Xiaoen Huang,Yanping Zhang,Jian-Liang Li

doi:10.1038/s41467-019-12781-7

Abstract

Systemic acquired resistance (SAR) is a long-lasting broad-spectrum plant immunity induced by mobile signals produced in the local leaves where the initial infection occurs. Although multiple structurally unrelated signals have been proposed, the mechanisms responsible for perception of these signals in the systemic leaves are unknown. Here, we show that exogenously applied nicotinamide adenine dinucleotide (NAD+) moves systemically and induces systemic immunity. We demonstrate that the lectin receptor kinase (LecRK), LecRK-VI.2, is a potential receptor for extracellular NAD+ (eNAD+) and NAD+ phosphate (eNADP+) and plays a central role in biological induction of SAR. LecRK-VI.2 constitutively associates with BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 (BAK1) in vivo. Furthermore, BAK1 and its homolog BAK1-LIKE1 are required for eNAD(P)+ signaling and SAR, and the kinase activities of LecR-VI.2 and BAK1 are indispensable to their function in SAR. Our results indicate that eNAD+ is a putative mobile signal, which triggers SAR through its receptor complex LecRK-VI.2/BAK1 in Arabidopsis thaliana.

Highlights

Systemic acquired resistance (SAR) is a long-lasting broad-spectrum plant immunity induced by mobile signals produced in the local leaves where the initial infection occurs
NADP+-induced PR gene expression and Psm resistance were significantly suppressed in all three alleles but not in the extracellular ATP receptor mutant dorn[1-326] (Fig. 2a–d). These results suggest that lectin receptor kinase (LecRK)-VI.[2] may play a more important role in eNADP+ signaling than in eNAD+ signaling in the local leaves
The majority of the genes that were induced or suppressed twofold or higher with a low q value (≤0.05) in the wild type were induced or suppressed to a smaller extent in bak[1,2,3,4,5] and the smallest extent in lecrk-VI.[2] (Supplementary Fig. 7 and Supplementary Data 1). These results indicate that the bak[1,2,3,4,5] mutation suppressed SAR activation-induced signaling, but the strength of the suppression was not as strong as that in lecrk-VI.[2], which may be attributed to the presence of BKK1 that might have some redundant functions with BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 (BAK1) in biological induction of SAR (Fig. 5d)

Summary

Introduction

Systemic acquired resistance (SAR) is a long-lasting broad-spectrum plant immunity induced by mobile signals produced in the local leaves where the initial infection occurs. Our results indicate that eNAD+ is a putative mobile signal, which triggers SAR through its receptor complex LecRK-VI.2/BAK1 in Arabidopsis thaliana. Resistant plants in turn exploit resistance proteins to detect the presence of pathogen effectors, inducing effector-triggered immunity These plant–pathogen battles often cause injuries to the plant cells, resulting in release of host-derived damage-associated molecular patterns (DAMPs) that further potentiate immunity through PRRs2. Transgenic expression of the human NAD(P)+-hydrolyzing ectoenzyme CD38 in Arabidopsis thaliana (Arabidopsis) partially compromises biological induction of SAR21 These results suggest that eNAD(P)+ may be an SAR signal molecule. We show that eNAD+ is a putative SAR mobile signal and demonstrate that the eNAD(P)+ receptor complex LecRK-VI.2/BAK1 (Brassinosteroid insensitive1-Associated Kinase1) is a key signaling component of SAR in Arabidopsis

Methods

Results

Conclusion