RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections
- University of Freiburg, Germany
- University of Toulouse-Jean Jaurès, France
- University of Science and Technology of China, China
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
Marta Rodriguez-Franco
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.
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.
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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
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