The AUX1-AFB1-CNGC14 module establishes a longitudinal root surface pH profile

  1. Nelson BC Serre
  2. Daša Wernerová
  3. Pruthvi Vittal
  4. Shiv Mani Dubey
  5. Eva Medvecká
  6. Adriana Jelínková
  7. Jan Petrášek
  8. Guido Grossmann
  9. Matyáš Fendrych  Is a corresponding author
  1. Charles University, Czech Republic
  2. Czech Academy of Sciences, Czech Republic
  3. Heinrich-Heine-University Düsseldorf, Germany

Abstract

Plant roots navigate in the soil environment following the gravity vector. Cell divisions in the meristem and rapid cell growth in the elongation zone propel the root tips through the soil. Actively elongating cells acidify their apoplast to enable cell wall extension by the activity of plasma membrane AHA H+-ATPases. The phytohormone auxin, central regulator of gravitropic response and root development, inhibits root cell growth, likely by rising the pH of the apoplast. However, the role of auxin in the regulation of the apoplastic pH gradient along the root tip is unclear. Here we show, by using an improved method for visualization and quantification of root surface pH, that the Arabidopsis thaliana root surface pH shows distinct acidic and alkaline zones, which are not primarily determined by the activity of AHA H+-ATPases. Instead, the distinct domain of alkaline pH in the root transition zone is controlled by a rapid auxin response module, consisting of the AUX1 auxin influx carrier, the AFB1 auxin co-receptor and the CNCG14 calcium channel. We demonstrate that the rapid auxin response pathway is required for an efficient navigation of the root tip.

Data availability

All the data used for the the manuscript are available at Zenodo.The statistics used and p-values are available as supplementary file.

The following data sets were generated

Article and author information

Author details

  1. Nelson BC Serre

    Department of Experimental Plant Biology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  2. Daša Wernerová

    Department of Experimental Plant Biology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  3. Pruthvi Vittal

    Department of Experimental Plant Biology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  4. Shiv Mani Dubey

    Department of Experimental Plant Biology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  5. Eva Medvecká

    Department of Experimental Plant Biology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  6. Adriana Jelínková

    Institute of Experimental Botany, Czech Academy of Sciences, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  7. Jan Petrášek

    Department of Experimental Plant Biology, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  8. Guido Grossmann

    Institute of Cell and Interaction Biology, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Matyáš Fendrych

    Department of Experimental Plant Biology, Charles University, Prague, Czech Republic
    For correspondence
    matyas.fendrych@natur.cuni.cz
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9767-8699

Funding

European Research Council (803048)

  • Nelson BC Serre
  • Daša Wernerová
  • Pruthvi Vittal
  • Shiv Mani Dubey
  • Eva Medvecká
  • Matyáš Fendrych

Deutsche Forschungsgemeinschaft (GR4559)

  • Guido Grossmann

Deutsche Forschungsgemeinschaft (CRC1208)

  • Guido Grossmann

EPLAS-EXC-2048/1 (390686111)

  • Guido Grossmann

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

Copyright

© 2023, Serre 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

  • 2,333
    views
  • 498
    downloads
  • 26
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Nelson BC Serre
  2. Daša Wernerová
  3. Pruthvi Vittal
  4. Shiv Mani Dubey
  5. Eva Medvecká
  6. Adriana Jelínková
  7. Jan Petrášek
  8. Guido Grossmann
  9. Matyáš Fendrych
(2023)
The AUX1-AFB1-CNGC14 module establishes a longitudinal root surface pH profile
eLife 12:e85193.
https://doi.org/10.7554/eLife.85193

Share this article

https://doi.org/10.7554/eLife.85193

Further reading

    1. Plant Biology
    Marie-Dominique Jolivet, Anne Flore Deroubaix ... Véronique Germain
    Research Article

    Plant viruses represent a risk to agricultural production and as only a few treatments exist, it is urgent to identify resistance mechanisms and factors. In plant immunity, plasma membrane (PM)-localized proteins play an essential role in sensing the extracellular threat presented by bacteria, fungi, or herbivores. Viruses are intracellular pathogens and as such the role of the plant PM in detection and resistance against viruses is often overlooked. We investigated the role of the partially PM-bound Calcium-dependent protein kinase 3 (CPK3) in viral infection and we discovered that it displayed a specific ability to hamper viral propagation over CPK isoforms that are involved in immune response to extracellular pathogens. More and more evidence supports that the lateral organization of PM proteins and lipids underlies signal transduction in plants. We showed here that CPK3 diffusion in the PM is reduced upon activation as well as upon viral infection and that such immobilization depended on its substrate, Remorin (REM1.2), a scaffold protein. Furthermore, we discovered that the viral infection induced a CPK3-dependent increase of REM1.2 PM diffusion. Such interdependence was also observable regarding viral propagation. This study unveils a complex relationship between a kinase and its substrate that contrasts with the commonly described co-stabilisation upon activation while it proposes a PM-based mechanism involved in decreased sensitivity to viral infection in plants.

    1. Plant Biology
    Hanbin Bao, Yanan Wang ... Yangrong Cao
    Research Article

    It is well documented that type-III effectors are required by Gram-negative pathogens to directly target different host cellular pathways to promote bacterial infection. However, in the context of legume–rhizobium symbiosis, the role of rhizobial effectors in regulating plant symbiotic pathways remains largely unexplored. Here, we show that NopT, a YopT-type cysteine protease of Sinorhizobium fredii NGR234 directly targets the plant’s symbiotic signaling pathway by associating with two Nod factor receptors (NFR1 and NFR5 of Lotus japonicus). NopT inhibits cell death triggered by co-expression of NFR1/NFR5 in Nicotiana benthamiana. Full-length NopT physically interacts with NFR1 and NFR5. NopT proteolytically cleaves NFR5 both in vitro and in vivo, but can be inactivated by NFR1 as a result of phosphorylation. NopT plays an essential role in mediating rhizobial infection in L. japonicus. Autocleaved NopT retains the ability to cleave NFR5 but no longer interacts with NFR1. Interestingly, genomes of certain Sinorhizobium species only harbor nopT genes encoding truncated proteins without the autocleavage site. These results reveal an intricate interplay between rhizobia and legumes, in which a rhizobial effector protease targets NFR5 to suppress symbiotic signaling. NFR1 appears to counteract this process by phosphorylating the effector. This discovery highlights the role of a bacterial effector in regulating a signaling pathway in plants and opens up the perspective of developing kinase-interacting proteases to fine-tune cellular signaling processes in general.