The ex planta signal activity of a Medicago ribosomal uL2 protein suggests a moonlighting role in controlling secondary rhizobial infection

We recently described a regulatory loop, which we termed autoregulation of infection (AOI), by which Sinorhizobium meliloti, a Medicago endosymbiont, downregulates the root susceptibility to secondary infection events via ethylene. AOI is initially triggered by so-far unidentified Medicago nodule si...

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Main Authors: Fernando Sorroche, Violette Morales, Saïda Mouffok, Carole Pichereaux, A. Marie Garnerone, Lan Zou, Badrish Soni, Marie-Anne Carpéné, Audrey Gargaros, Fabienne Maillet, Odile Burlet-Schiltz, Verena Poinsot, Patrice Polard, Clare Gough, Jacques Batut, Francisco Martinez-Abarca
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7529298/?tool=EBI
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author Fernando Sorroche
Violette Morales
Saïda Mouffok
Carole Pichereaux
A. Marie Garnerone
Lan Zou
Badrish Soni
Marie-Anne Carpéné
Audrey Gargaros
Fabienne Maillet
Odile Burlet-Schiltz
Verena Poinsot
Patrice Polard
Clare Gough
Jacques Batut
Francisco Martinez-Abarca
author_facet Fernando Sorroche
Violette Morales
Saïda Mouffok
Carole Pichereaux
A. Marie Garnerone
Lan Zou
Badrish Soni
Marie-Anne Carpéné
Audrey Gargaros
Fabienne Maillet
Odile Burlet-Schiltz
Verena Poinsot
Patrice Polard
Clare Gough
Jacques Batut
Francisco Martinez-Abarca
author_sort Fernando Sorroche
collection DOAJ
description We recently described a regulatory loop, which we termed autoregulation of infection (AOI), by which Sinorhizobium meliloti, a Medicago endosymbiont, downregulates the root susceptibility to secondary infection events via ethylene. AOI is initially triggered by so-far unidentified Medicago nodule signals named signal 1 and signal 1’ whose transduction in bacteroids requires the S. meliloti outer-membrane-associated NsrA receptor protein and the cognate inner-membrane-associated adenylate cyclases, CyaK and CyaD1/D2, respectively. Here, we report on advances in signal 1 identification. Signal 1 activity is widespread as we robustly detected it in Medicago nodule extracts as well as in yeast and bacteria cell extracts. Biochemical analyses indicated a peptidic nature for signal 1 and, together with proteomic analyses, a universally conserved Medicago ribosomal protein of the uL2 family was identified as a candidate signal 1. Specifically, MtRPuL2A (MtrunA17Chr7g0247311) displays a strong signal activity that requires S. meliloti NsrA and CyaK, as endogenous signal 1. We have shown that MtRPuL2A is active in signaling only in a non-ribosomal form. A Medicago truncatula mutant in the major symbiotic transcriptional regulator MtNF-YA1 lacked most signal 1 activity, suggesting that signal 1 is under developmental control. Altogether, our results point to the MtRPuL2A ribosomal protein as the candidate for signal 1. Based on the Mtnf-ya1 mutant, we suggest a link between root infectiveness and nodule development. We discuss our findings in the context of ribosomal protein moonlighting.
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spelling doaj.art-a8bdde53bebf4a89bdd4fbb9f06371fa2022-12-22T00:50:08ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-011510The ex planta signal activity of a Medicago ribosomal uL2 protein suggests a moonlighting role in controlling secondary rhizobial infectionFernando SorrocheViolette MoralesSaïda MouffokCarole PichereauxA. Marie GarneroneLan ZouBadrish SoniMarie-Anne CarpénéAudrey GargarosFabienne MailletOdile Burlet-SchiltzVerena PoinsotPatrice PolardClare GoughJacques BatutFrancisco Martinez-AbarcaWe recently described a regulatory loop, which we termed autoregulation of infection (AOI), by which Sinorhizobium meliloti, a Medicago endosymbiont, downregulates the root susceptibility to secondary infection events via ethylene. AOI is initially triggered by so-far unidentified Medicago nodule signals named signal 1 and signal 1’ whose transduction in bacteroids requires the S. meliloti outer-membrane-associated NsrA receptor protein and the cognate inner-membrane-associated adenylate cyclases, CyaK and CyaD1/D2, respectively. Here, we report on advances in signal 1 identification. Signal 1 activity is widespread as we robustly detected it in Medicago nodule extracts as well as in yeast and bacteria cell extracts. Biochemical analyses indicated a peptidic nature for signal 1 and, together with proteomic analyses, a universally conserved Medicago ribosomal protein of the uL2 family was identified as a candidate signal 1. Specifically, MtRPuL2A (MtrunA17Chr7g0247311) displays a strong signal activity that requires S. meliloti NsrA and CyaK, as endogenous signal 1. We have shown that MtRPuL2A is active in signaling only in a non-ribosomal form. A Medicago truncatula mutant in the major symbiotic transcriptional regulator MtNF-YA1 lacked most signal 1 activity, suggesting that signal 1 is under developmental control. Altogether, our results point to the MtRPuL2A ribosomal protein as the candidate for signal 1. Based on the Mtnf-ya1 mutant, we suggest a link between root infectiveness and nodule development. We discuss our findings in the context of ribosomal protein moonlighting.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7529298/?tool=EBI
spellingShingle Fernando Sorroche
Violette Morales
Saïda Mouffok
Carole Pichereaux
A. Marie Garnerone
Lan Zou
Badrish Soni
Marie-Anne Carpéné
Audrey Gargaros
Fabienne Maillet
Odile Burlet-Schiltz
Verena Poinsot
Patrice Polard
Clare Gough
Jacques Batut
Francisco Martinez-Abarca
The ex planta signal activity of a Medicago ribosomal uL2 protein suggests a moonlighting role in controlling secondary rhizobial infection
PLoS ONE
title The ex planta signal activity of a Medicago ribosomal uL2 protein suggests a moonlighting role in controlling secondary rhizobial infection
title_full The ex planta signal activity of a Medicago ribosomal uL2 protein suggests a moonlighting role in controlling secondary rhizobial infection
title_fullStr The ex planta signal activity of a Medicago ribosomal uL2 protein suggests a moonlighting role in controlling secondary rhizobial infection
title_full_unstemmed The ex planta signal activity of a Medicago ribosomal uL2 protein suggests a moonlighting role in controlling secondary rhizobial infection
title_short The ex planta signal activity of a Medicago ribosomal uL2 protein suggests a moonlighting role in controlling secondary rhizobial infection
title_sort ex planta signal activity of a medicago ribosomal ul2 protein suggests a moonlighting role in controlling secondary rhizobial infection
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7529298/?tool=EBI
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