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The Lotus japonicus ROP3 Is Involved in the Establishment of the Nitrogen-Fixing Symbiosis but Not of the Arbuscular Mycorrhizal Symbiosis

Legumes form root mutualistic symbioses with some soil microbes promoting their growth, rhizobia, and arbuscular mycorrhizal fungi (AMF). A conserved set of plant proteins rules the transduction of symbiotic signals from rhizobia and AMF in a so-called common symbiotic signaling pathway (CSSP). Desp...

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Autores principales: García-Soto, Ivette, Boussageon, Raphael, Cruz-Farfán, Yareni Marlene, Castro-Chilpa, Jesus Daniel, Hernández-Cerezo, Liz Xochiquetzal, Bustos-Zagal, Victor, Leija-Salas, Alfonso, Hernández, Georgina, Torres, Martha, Formey, Damien, Courty, Pierre-Emmanuel, Wipf, Daniel, Serrano, Mario, Tromas, Alexandre
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8636059/
https://www.ncbi.nlm.nih.gov/pubmed/34868100
http://dx.doi.org/10.3389/fpls.2021.696450
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author García-Soto, Ivette
Boussageon, Raphael
Cruz-Farfán, Yareni Marlene
Castro-Chilpa, Jesus Daniel
Hernández-Cerezo, Liz Xochiquetzal
Bustos-Zagal, Victor
Leija-Salas, Alfonso
Hernández, Georgina
Torres, Martha
Formey, Damien
Courty, Pierre-Emmanuel
Wipf, Daniel
Serrano, Mario
Tromas, Alexandre
author_facet García-Soto, Ivette
Boussageon, Raphael
Cruz-Farfán, Yareni Marlene
Castro-Chilpa, Jesus Daniel
Hernández-Cerezo, Liz Xochiquetzal
Bustos-Zagal, Victor
Leija-Salas, Alfonso
Hernández, Georgina
Torres, Martha
Formey, Damien
Courty, Pierre-Emmanuel
Wipf, Daniel
Serrano, Mario
Tromas, Alexandre
author_sort García-Soto, Ivette
collection PubMed
description Legumes form root mutualistic symbioses with some soil microbes promoting their growth, rhizobia, and arbuscular mycorrhizal fungi (AMF). A conserved set of plant proteins rules the transduction of symbiotic signals from rhizobia and AMF in a so-called common symbiotic signaling pathway (CSSP). Despite considerable efforts and advances over the past 20 years, there are still key elements to be discovered about the establishment of these root symbioses. Rhizobia and AMF root colonization are possible after a deep cell reorganization. In the interaction between the model legume Lotus japonicus and Mesorhizobium loti, this reorganization has been shown to be dependent on a SCAR/Wave-like signaling module, including Rho-GTPase (ROP in plants). Here, we studied the potential role of ROP3 in the nitrogen-fixing symbiosis (NFS) as well as in the arbuscular mycorrhizal symbiosis (AMS). We performed a detailed phenotypic study on the effects of the loss of a single ROP on the establishment of both root symbioses. Moreover, we evaluated the expression of key genes related to CSSP and to the rhizobial-specific pathway. Under our experimental conditions, rop3 mutant showed less nodule formation at 7- and 21-days post inoculation as well as less microcolonies and a higher frequency of epidermal infection threads. However, AMF root colonization was not affected. These results suggest a role of ROP3 as a positive regulator of infection thread formation and nodulation in L. japonicus. In addition, CSSP gene expression was neither affected in NFS nor in AMS condition in rop3 mutant. whereas the expression level of some genes belonging to the rhizobial-specific pathway, like RACK1, decreased in the NFS. In conclusion, ROP3 appears to be involved in the NFS, but is neither required for intra-radical growth of AMF nor arbuscule formation.
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spelling pubmed-86360592021-12-02 The Lotus japonicus ROP3 Is Involved in the Establishment of the Nitrogen-Fixing Symbiosis but Not of the Arbuscular Mycorrhizal Symbiosis García-Soto, Ivette Boussageon, Raphael Cruz-Farfán, Yareni Marlene Castro-Chilpa, Jesus Daniel Hernández-Cerezo, Liz Xochiquetzal Bustos-Zagal, Victor Leija-Salas, Alfonso Hernández, Georgina Torres, Martha Formey, Damien Courty, Pierre-Emmanuel Wipf, Daniel Serrano, Mario Tromas, Alexandre Front Plant Sci Plant Science Legumes form root mutualistic symbioses with some soil microbes promoting their growth, rhizobia, and arbuscular mycorrhizal fungi (AMF). A conserved set of plant proteins rules the transduction of symbiotic signals from rhizobia and AMF in a so-called common symbiotic signaling pathway (CSSP). Despite considerable efforts and advances over the past 20 years, there are still key elements to be discovered about the establishment of these root symbioses. Rhizobia and AMF root colonization are possible after a deep cell reorganization. In the interaction between the model legume Lotus japonicus and Mesorhizobium loti, this reorganization has been shown to be dependent on a SCAR/Wave-like signaling module, including Rho-GTPase (ROP in plants). Here, we studied the potential role of ROP3 in the nitrogen-fixing symbiosis (NFS) as well as in the arbuscular mycorrhizal symbiosis (AMS). We performed a detailed phenotypic study on the effects of the loss of a single ROP on the establishment of both root symbioses. Moreover, we evaluated the expression of key genes related to CSSP and to the rhizobial-specific pathway. Under our experimental conditions, rop3 mutant showed less nodule formation at 7- and 21-days post inoculation as well as less microcolonies and a higher frequency of epidermal infection threads. However, AMF root colonization was not affected. These results suggest a role of ROP3 as a positive regulator of infection thread formation and nodulation in L. japonicus. In addition, CSSP gene expression was neither affected in NFS nor in AMS condition in rop3 mutant. whereas the expression level of some genes belonging to the rhizobial-specific pathway, like RACK1, decreased in the NFS. In conclusion, ROP3 appears to be involved in the NFS, but is neither required for intra-radical growth of AMF nor arbuscule formation. Frontiers Media S.A. 2021-11-12 /pmc/articles/PMC8636059/ /pubmed/34868100 http://dx.doi.org/10.3389/fpls.2021.696450 Text en Copyright © 2021 García-Soto, Boussageon, Cruz-Farfán, Castro-Chilpa, Hernández-Cerezo, Bustos-Zagal, Leija-Salas, Hernández, Torres, Formey, Courty, Wipf, Serrano and Tromas. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
García-Soto, Ivette
Boussageon, Raphael
Cruz-Farfán, Yareni Marlene
Castro-Chilpa, Jesus Daniel
Hernández-Cerezo, Liz Xochiquetzal
Bustos-Zagal, Victor
Leija-Salas, Alfonso
Hernández, Georgina
Torres, Martha
Formey, Damien
Courty, Pierre-Emmanuel
Wipf, Daniel
Serrano, Mario
Tromas, Alexandre
The Lotus japonicus ROP3 Is Involved in the Establishment of the Nitrogen-Fixing Symbiosis but Not of the Arbuscular Mycorrhizal Symbiosis
title The Lotus japonicus ROP3 Is Involved in the Establishment of the Nitrogen-Fixing Symbiosis but Not of the Arbuscular Mycorrhizal Symbiosis
title_full The Lotus japonicus ROP3 Is Involved in the Establishment of the Nitrogen-Fixing Symbiosis but Not of the Arbuscular Mycorrhizal Symbiosis
title_fullStr The Lotus japonicus ROP3 Is Involved in the Establishment of the Nitrogen-Fixing Symbiosis but Not of the Arbuscular Mycorrhizal Symbiosis
title_full_unstemmed The Lotus japonicus ROP3 Is Involved in the Establishment of the Nitrogen-Fixing Symbiosis but Not of the Arbuscular Mycorrhizal Symbiosis
title_short The Lotus japonicus ROP3 Is Involved in the Establishment of the Nitrogen-Fixing Symbiosis but Not of the Arbuscular Mycorrhizal Symbiosis
title_sort lotus japonicus rop3 is involved in the establishment of the nitrogen-fixing symbiosis but not of the arbuscular mycorrhizal symbiosis
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8636059/
https://www.ncbi.nlm.nih.gov/pubmed/34868100
http://dx.doi.org/10.3389/fpls.2021.696450
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