1. Plant Biology

RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections

  1. Beatrice Lace  Is a corresponding author
  2. Chao Su
  3. Daniel Invernot Perez
  4. Marta Rodriguez-Franco
  5. Tatiana Vernié
  6. Morgane Batzenschlager
  7. Sabrina Egli
  8. Cheng-Wu Liu
  9. Thomas Ott  Is a corresponding author
  1. University of Freiburg, Germany
  2. University of Toulouse-Jean Jaurès, France
  3. University of Science and Technology of China, China
https://doi.org/10.7554/eLife.80741
Share this article
Cite this article
  1. Beatrice Lace
  2. Chao Su
  3. Daniel Invernot Perez
  4. Marta Rodriguez-Franco
  5. Tatiana Vernié
  6. Morgane Batzenschlager
  7. Sabrina Egli
  8. Cheng-Wu Liu
  9. Thomas Ott
(2023)
RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections
eLife 12:e80741.
https://doi.org/10.7554/eLife.80741
  2. Download BibTeX
  3. Download .RIS

Abstract

Host-controlled intracellular accommodation of nitrogen-fixing bacteria is essential for the establishment of a functional Root Nodule Symbiosis (RNS). In many host plants, this occurs via transcellular tubular structures (infection threads - ITs) that extend across cell layers via polar tip-growth. Comparative phylogenomic studies have identified RPG (RHIZOBIUM-DIRECTED POLAR GROWTH) among the critical genetic determinants for bacterial infection. In Medicago truncatula, RPG is required for effective IT progression within root hairs but the cellular and molecular function of the encoded protein remains elusive. Here, we show that RPG resides in the protein complex formed by the core endosymbiotic components VAPYRIN (VPY) and LUMPY INFECTION (LIN) required for IT polar growth, co-localizes with both VPY and LIN in IT tip- and perinuclear-associated puncta of M. truncatula root hairs undergoing infection and is necessary for VPY recruitment into these structures. Fluorescence Lifetime Imaging Microscopy (FLIM) of phosphoinositide species during bacterial infection revealed that functional RPG is required to sustain strong membrane polarization at the advancing tip of the IT. In addition, loss of RPG functionality alters the cytoskeleton-mediated connectivity between the IT tip and the nucleus and affects polar secretion of the cell wall modifying enzyme NODULE PECTATE LYASE (NPL). Our results integrate RPG into a core host machinery required to support symbiont accommodation, suggesting that its occurrence in plant host genomes is essential to co-opt a multimeric protein module committed to endosymbiosis to sustain IT-mediated bacterial infection.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files

Article and author information

Author details

  1. Beatrice Lace

    Faculty of Biology, Cell Biology, University of Freiburg, Freiburg, Germany
    For correspondence
    beatrice.lace@biologie.uni-freiburg.de
    Competing interests
    The authors declare that no competing interests exist.

  2. Chao Su

    Faculty of Biology, Cell Biology, University of Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Daniel Invernot Perez

    Faculty of Biology, Cell Biology, University of Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  4. Marta Rodriguez-Franco

    Faculty of Biology, Cell Biology, University of Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1183-2075

  5. Tatiana Vernié

    University of Toulouse-Jean Jaurès, Castanet, France
    Competing interests
    The authors declare that no competing interests exist.

  6. Morgane Batzenschlager

    Faculty of Biology, Cell Biology, University of Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  7. Sabrina Egli

    Faculty of Biology, Cell Biology, University of Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  8. Cheng-Wu Liu

    Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6650-6245

  9. Thomas Ott

    Faculty of Biology, Cell Biology, University of Freiburg, Freiburg, Germany
    For correspondence
    Thomas.Ott@biologie.uni-freiburg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4494-9811

Funding

Bill and Melinda Gates Foundation (OPP1172165)

  • Thomas Ott

Deutsche Forschungsgemeinschaft (431626755)

  • Thomas Ott

Deutsche Forschungsgemeinschaft (39093984)

  • Thomas Ott

Deutsche Forschungsgemeinschaft (414136422)

  • Thomas Ott

Deutsche Forschungsgemeinschaft (426849454)

  • Thomas Ott

China Scholarship Council (201708080016)

  • Chao Su

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

Reviewing Editor

  1. Dominique C Bergmann, Stanford University, United States

Version history

  1. Received: June 1, 2022
  2. Preprint posted: June 4, 2022 (view preprint)
  3. Accepted: February 21, 2023
  4. Accepted Manuscript published: March 1, 2023 (version 1)
  5. Version of Record published: March 7, 2023 (version 2)

Copyright

© 2023, Lace 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

  • 1,120
    Page views
  • 243
    Downloads
  • 3
    Citations

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

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. Beatrice Lace
  2. Chao Su
  3. Daniel Invernot Perez
  4. Marta Rodriguez-Franco
  5. Tatiana Vernié
  6. Morgane Batzenschlager
  7. Sabrina Egli
  8. Cheng-Wu Liu
  9. Thomas Ott
(2023)
RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections
eLife 12:e80741.
https://doi.org/10.7554/eLife.80741

Categories and tags

Further reading

    1. Ecology
    2. Plant Biology

    Unprecedented yet gradual nature of first millennium CE intercontinental crop plant dispersal revealed in ancient Negev desert refuse

    Daniel Fuks, Yoel Melamed ... Ehud Weiss
    Research Article

    Global agro-biodiversity has resulted from processes of plant migration and agricultural adoption. Although critically affecting current diversity, crop diffusion from Classical antiquity to the Middle Ages is poorly researched, overshadowed by studies on that of prehistoric periods. A new archaeobotanical dataset from three Negev Highland desert sites demonstrates the first millennium CE&'s significance for long-term agricultural change in southwest Asia. This enables evaluation of the 'Islamic Green Revolution' (IGR) thesis compared to 'Roman Agricultural Diffusion' (RAD), and both versus crop diffusion during and since the Neolithic. Among the finds, some of the earliest aubergine (Solanum melongena) seeds in the Levant represent the proposed IGR. Several other identified economic plants, including two unprecedented in Levantine archaeobotany-jujube (Ziziphus jujuba/mauritiana) and white lupine (Lupinus albus)-implicate RAD as the greater force for crop migrations. Altogether the evidence supports a gradualist model for Holocene-wide crop diffusion, within which the first millennium CE contributed more to global agricultural diversity than any earlier period.

    1. Microbiology and Infectious Disease
    2. Plant Biology

    Soil-borne fungi alter the apoplastic purinergic signaling in plants by deregulating the homeostasis of extracellular ATP and its metabolite adenosine

    Christopher Kesten, Valentin Leitner ... Clara Sanchez-Rodriguez
    Research Article

    Purinergic signaling activated by extracellular nucleotides and their derivative nucleosides trigger sophisticated signaling networks. The outcome of these pathways determine the capacity of the organism to survive under challenging conditions. Both extracellular ATP (eATP) and Adenosine (eAdo) act as primary messengers in mammals, essential for immunosuppressive responses. Despite the clear role of eATP as a plant damage-associated molecular pattern, the function of its nucleoside, eAdo, and of the eAdo/eATP balance in plant stress response remain to be fully elucidated. This is particularly relevant in the context of plant-microbe interaction, where the intruder manipulates the extracellular matrix. Here, we identify Ado as a main molecule secreted by the vascular fungus Fusarium oxysporum. We show that eAdo modulates the plant's susceptibility to fungal colonization by altering the eATP-mediated apoplastic pH homeostasis, an essential physiological player during the infection of this pathogen. Our work indicates that plant pathogens actively imbalance the apoplastic eAdo/eATP levels as a virulence mechanism.

    1. Plant Biology
    2. Structural Biology and Molecular Biophysics

    Vicia faba SV channel VfTPC1 is a hyperexcitable variant of plant vacuole Two Pore Channels

    Jinping Lu, Ingo Dreyer ... Rainer Hedrich
    Research Article

    To fire action-potential-like electrical signals, the vacuole membrane requires the two-pore channel TPC1, formerly called SV channel. The TPC1/SV channel functions as a depolarization-stimulated, non-selective cation channel that is inhibited by luminal Ca2+. In our search for species-dependent functional TPC1 channel variants with different luminal Ca2+ sensitivity, we found in total three acidic residues present in Ca2+ sensor sites 2 and 3 of the Ca2+-sensitive AtTPC1 channel from Arabidopsis thaliana that were neutral in its Vicia faba ortholog and also in those of many other Fabaceae. When expressed in the Arabidopsis AtTPC1-loss-of-function background, wild-type VfTPC1 was hypersensitive to vacuole depolarization and only weakly sensitive to blocking luminal Ca2+. When AtTPC1 was mutated for these VfTPC1-homologous polymorphic residues, two neutral substitutions in Ca2+ sensor site 3 alone were already sufficient for the Arabidopsis At-VfTPC1 channel mutant to gain VfTPC1-like voltage and luminal Ca2+ sensitivity that together rendered vacuoles hyperexcitable. Thus, natural TPC1 channel variants exist in plant families which may fine-tune vacuole excitability and adapt it to environmental settings of the particular ecological niche.