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

  1. Chenggang Wang
  2. Mingqi Zhou
  3. Xudong Zhang
  4. Jin Yao
  5. Yanping Zhang
  6. Zhonglin Mou  Is a corresponding author
  1. University of Florida, United States
  2. GlaxoSmithKline, United States

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.

Data availability

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Chenggang Wang

    Department of Microbiology and Cell Science, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Mingqi Zhou

    Department of Microbiology and Cell Science, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4605-5467
  3. Xudong Zhang

    Department of Microbiology and Cell Science, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jin Yao

    Target Sciences, GlaxoSmithKline, King of Prussia, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Yanping Zhang

    Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Zhonglin Mou

    Department of Microbiology and Cell Science, University of Florida, Gainesville, United States
    For correspondence
    zhlmou@ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0243-4905

Funding

National Science Foundation (IOS-0842716)

  • Zhonglin Mou

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Thorsten Nürnberger, University of Tubingen, Germany

Publication history

  1. Received: January 25, 2017
  2. Accepted: July 18, 2017
  3. Accepted Manuscript published: July 19, 2017 (version 1)
  4. Version of Record published: August 17, 2017 (version 2)

Copyright

© 2017, Wang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 3,178
    Page views
  • 621
    Downloads
  • 48
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Chenggang Wang
  2. Mingqi Zhou
  3. Xudong Zhang
  4. Jin Yao
  5. Yanping Zhang
  6. Zhonglin Mou
(2017)
A lectin receptor kinase as a potential sensor for extracellular nicotinamide adenine dinucleotide in Arabidopsis thaliana
eLife 6:e25474.
https://doi.org/10.7554/eLife.25474

Further reading

    1. Plant Biology
    2. Structural Biology and Molecular Biophysics
    Koji Kato et al.
    Research Article

    Photosystem I (PSI) is a multi-subunit pigment-protein complex that functions in light-harvesting and photochemical charge-separation reactions, followed by reduction of NADP to NADPH required for CO2 fixation in photosynthetic organisms. PSI from different photosynthetic organisms has a variety of chlorophylls (Chls), some of which are at lower-energy levels than its reaction center P700, a special pair of Chls, and are called low-energy Chls. However, the sites of low-energy Chls are still under debate. Here, we solved a 2.04-Å resolution structure of a PSI trimer by cryo-electron microscopy from a primordial cyanobacterium Gloeobacter violaceus PCC 7421, which has no low-energy Chls. The structure shows the absence of some subunits commonly found in other cyanobacteria, confirming the primordial nature of this cyanobacterium. Comparison with the known structures of PSI from other cyanobacteria and eukaryotic organisms reveals that one dimeric and one trimeric Chls are lacking in the Gloeobacter PSI. The dimeric and trimeric Chls are named Low1 and Low2, respectively. Low2 is missing in some cyanobacterial and eukaryotic PSIs, whereas Low1 is absent only in Gloeobacter. These findings provide insights into not only the identity of low-energy Chls in PSI, but also the evolutionary changes of low-energy Chls in oxyphototrophs.

    1. Plant Biology
    Sylvia P Kinosian, Paul G Wolf
    Feature Article Updated

    The fern Ceratopteris richardii has been studied as a model organism for over 50 years because it is easy to grow and has a short life cycle. In particular, as the first homosporous vascular plant for which genomic resources were developed, C. richardii has been an important system for studying plant evolution. However, we know relatively little about the natural history of C. richardii. In this article, we summarize what is known about this aspect of C. richardii, and discuss how learning more about its natural history could greatly increase our understanding of the evolution of land plants.