A lectin receptor kinase as a potential sensor for extracellular nicotinamide adenine dinucleotide in Arabidopsis thaliana.

Chenggang Wang,Jin Yao,Yanping Zhang,Zhonglin Mou,Mingqi Zhou,Xudong Zhang

doi:10.7554/elife.25474

Chenggang Wang, Jin Yao + Show 4 more

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https://doi.org/10.7554/elife.25474

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Abstract

Nicotinamide adenine dinucleotide (NAD+) participates in intracellular and extracellular signaling events unrelated to metabolism. In animals, purinergic receptors are required for extracellular NAD+ (eNAD+) to evoke biological responses, indicating that eNAD+ may be sensed by cell-surface receptors. However, the identity of eNAD+-binding receptors still remains elusive. Here, we identify a lectin receptor kinase (LecRK), LecRK-I.8, as a potential eNAD+ receptor in Arabidopsis. The extracellular lectin domain of LecRK-I.8 binds NAD+ with a dissociation constant of 436.5 ± 104.8 nM, although much higher concentrations are needed to trigger in vivo responses. Mutations in LecRK-I.8 inhibit NAD+-induced immune responses, whereas overexpression of LecRK-I.8 enhances the Arabidopsis response to NAD+. Furthermore, LecRK-I.8 is required for basal resistance against bacterial pathogens, substantiating a role for eNAD+ in plant immunity. Our results demonstrate that lectin receptors can potentially function as eNAD+-binding receptors and provide direct evidence for eNAD+ being an endogenous signaling molecule in plants.

Highlights

The pyridine nucleotide NAD+ serves as a ubiquitous coenzymatic redox carrier in metabolic reactions, and participates in intracellular signal transduction (Berger et al, 2004; Noctor et al, 2006)
We have shown that expression of the human NAD+-metabolizing ectoenzyme CD38 partially compromises systemic acquired resistance (SAR) in Arabidopsis (Zhang and Mou, 2012), which strongly suggests that plants may use different mechanisms to sense eNAD+
We demonstrate that the lectin receptor kinase (LecRK), LecRK-I.8, is a potential eNAD+ receptor and plays a positive role in plant basal immunity

Summary

Introduction

The pyridine nucleotide NAD+ (nicotinamide adenine dinucleotide) serves as a ubiquitous coenzymatic redox carrier in metabolic reactions, and participates in intracellular signal transduction (Berger et al, 2004; Noctor et al, 2006). Extracellular fluid at concentrations sufficient to induce PR gene expression and disease resistance (Zhang and Mou, 2009) These results provided the first line of evidence that NAD+ may play a signaling role in plant extracellular space. We have shown that expression of the human NAD+-metabolizing ectoenzyme CD38 partially compromises systemic acquired resistance (SAR) in Arabidopsis (Zhang and Mou, 2012), which strongly suggests that plants may use different mechanisms to sense eNAD+. In order to understand eNAD+ and its signaling role in plants, we performed a forward genetic screen in Arabidopsis to identify mutants insensitive to exogenous NAD+ (ien) treatment (Zhang et al, 2012). Our findings indicate that cell-surface lectin receptors can potentially act as eNAD+-sensing receptors and present direct evidence for eNAD+ being a novel endogenous signaling molecule in plants

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Discussion

Materials and methods

Funding Funder National Science Foundation