The manifold actions of signaling peptides on subcellular dynamics of a receptor specify stomatal cell fate

  1. Xingyun Qi
  2. Akira Yoshinari
  3. Pengfei Bai
  4. Michal Maes
  5. Scott M Zeng
  6. Keiko U Torii  Is a corresponding author
  1. Unversity of Washington, United States
  2. Nagoya University, Japan
  3. University of Texas at Austin, United States
  4. University of Washington, United States

Abstract

Receptor endocytosis is important for signal activation, transduction, and deactivation. However, how a receptor interprets conflicting signals to adjust cellular output is not clearly understood. Using genetic, cell biological, and pharmacological approaches, we report here that ERECTA-LIKE1 (ERL1), the major receptor restricting plant stomatal differentiation, undergoes dynamic subcellular behaviors in response to different EPIDERMAL PATTERNING FACTOR (EPF) peptides. Activation of ERL1 by EPF1 induces rapid ERL1 internalization via multivesicular bodies/late endosomes to vacuolar degradation, whereas ERL1 constitutively internalizes in the absence of EPF1. The co-receptor, TOO MANY MOUTHS is essential for ERL1 internalization induced by EPF1 but not by EPFL6. The peptide antagonist, Stomagen, triggers retention of ERL1 in the endoplasmic reticulum, likely coupled with reduced endocytosis. In contrast, the dominant-negative ERL1 remained dysfunctional in ligand-induced subcellular trafficking. Our study elucidates that multiple related yet unique peptides specify cell fate by deploying the differential subcellular dynamics of a single receptor.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source R codes are provided.

Article and author information

Author details

  1. Xingyun Qi

    Biology, Unversity of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Akira Yoshinari

    Institute of Transformative Biomolecules, Nagoya University, Nagoya, Aichi, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Pengfei Bai

    Molecular Biosciences, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Michal Maes

    Biology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Scott M Zeng

    Physics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Keiko U Torii

    Molecular Biosciences, University of Texas at Austin, Austin, United States
    For correspondence
    ktorii@utexas.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6168-427X

Funding

Howard Hughes Medical Institute (TORII)

  • Keiko U Torii

Gordon and Betty Moore Foundation (GBMF3035)

  • Keiko U Torii

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

Reviewing Editor

  1. Jürgen Kleine-Vehn, University of Natural Resources and Life Sciences, Austria

Version history

  1. Received: April 21, 2020
  2. Accepted: August 14, 2020
  3. Accepted Manuscript published: August 14, 2020 (version 1)
  4. Version of Record published: September 3, 2020 (version 2)

Copyright

© 2020, Qi 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

  • 2,441
    views
  • 455
    downloads
  • 19
    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. Xingyun Qi
  2. Akira Yoshinari
  3. Pengfei Bai
  4. Michal Maes
  5. Scott M Zeng
  6. Keiko U Torii
(2020)
The manifold actions of signaling peptides on subcellular dynamics of a receptor specify stomatal cell fate
eLife 9:e58097.
https://doi.org/10.7554/eLife.58097

Share this article

https://doi.org/10.7554/eLife.58097

Further reading

    1. Plant Biology
    Ivan Kulich, Julia Schmid ... Jiří Friml
    Research Article

    Root gravitropic bending represents a fundamental aspect of terrestrial plant physiology. Gravity is perceived by sedimentation of starch-rich plastids (statoliths) to the bottom of the central root cap cells. Following gravity perception, intercellular auxin transport is redirected downwards leading to an asymmetric auxin accumulation at the lower root side causing inhibition of cell expansion, ultimately resulting in downwards bending. How gravity-induced statoliths repositioning is translated into asymmetric auxin distribution remains unclear despite PIN auxin efflux carriers and the Negative Gravitropic Response of roots (NGR) proteins polarize along statolith sedimentation, thus providing a plausible mechanism for auxin flow redirection. In this study, using a functional NGR1-GFP construct, we visualized the NGR1 localization on the statolith surface and plasma membrane (PM) domains in close proximity to the statoliths, correlating with their movements. We determined that NGR1 binding to these PM domains is indispensable for NGR1 functionality and relies on cysteine acylation and adjacent polybasic regions as well as on lipid and sterol PM composition. Detailed timing of the early events following graviperception suggested that both NGR1 repolarization and initial auxin asymmetry precede the visible PIN3 polarization. This discrepancy motivated us to unveil a rapid, NGR-dependent translocation of PIN-activating AGCVIII kinase D6PK towards lower PMs of gravity-perceiving cells, thus providing an attractive model for rapid redirection of auxin fluxes following gravistimulation.

    1. Plant Biology
    Daniel S Yu, Megan A Outram ... Simon J Williams
    Research Article

    Plant pathogens secrete proteins, known as effectors, that function in the apoplast or inside plant cells to promote virulence. Effector recognition by cell-surface or cytosolic receptors results in the activation of defence pathways and plant immunity. Despite their importance, our general understanding of fungal effector function and recognition by immunity receptors remains poor. One complication often associated with effectors is their high sequence diversity and lack of identifiable sequence motifs precluding prediction of structure or function. In recent years, several studies have demonstrated that fungal effectors can be grouped into structural classes, despite significant sequence variation and existence across taxonomic groups. Using protein X-ray crystallography, we identify a new structural class of effectors hidden within the secreted in xylem (SIX) effectors from Fusarium oxysporum f. sp. lycopersici (Fol). The recognised effectors Avr1 (SIX4) and Avr3 (SIX1) represent the founding members of the Fol dual-domain (FOLD) effector class, with members containing two distinct domains. Using AlphaFold2, we predicted the full SIX effector repertoire of Fol and show that SIX6 and SIX13 are also FOLD effectors, which we validated experimentally for SIX6. Based on structural prediction and comparisons, we show that FOLD effectors are present within three divisions of fungi and are expanded in pathogens and symbionts. Further structural comparisons demonstrate that Fol secretes effectors that adopt a limited number of structural folds during infection of tomato. This analysis also revealed a structural relationship between transcriptionally co-regulated effector pairs. We make use of the Avr1 structure to understand its recognition by the I receptor, which leads to disease resistance in tomato. This study represents an important advance in our understanding of Fol-tomato, and by extension plant–fungal interactions, which will assist in the development of novel control and engineering strategies to combat plant pathogens.