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Widespread Bradyrhizobium distribution of diverse Type III effectors that trigger legume nodulation in the absence of Nod factor

The establishment of the rhizobium-legume symbiosis is generally based on plant perception of Nod factors (NFs) synthesized by the bacteria. However, some Bradyrhizobium strains can nodulate certain legume species, such as Aeschynomene spp. or Glycine max, independently of NFs, and via two different...

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Autores principales: Camuel, Alicia, Teulet, Albin, Carcagno, Mélanie, Haq, Fazal, Pacquit, Valérie, Gully, Djamel, Pervent, Marjorie, Chaintreuil, Clémence, Fardoux, Joël, Horta-Araujo, Natasha, Okazaki, Shin, Ratu, Safirah Tasa Nerves, Gueye, Fatou, Zilli, Jerri, Nouwen, Nico, Arrighi, Jean-François, Luo, Haiwei, Mergaert, Peter, Deslandes, Laurent, Giraud, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10432411/
https://www.ncbi.nlm.nih.gov/pubmed/37355742
http://dx.doi.org/10.1038/s41396-023-01458-1
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author Camuel, Alicia
Teulet, Albin
Carcagno, Mélanie
Haq, Fazal
Pacquit, Valérie
Gully, Djamel
Pervent, Marjorie
Chaintreuil, Clémence
Fardoux, Joël
Horta-Araujo, Natasha
Okazaki, Shin
Ratu, Safirah Tasa Nerves
Gueye, Fatou
Zilli, Jerri
Nouwen, Nico
Arrighi, Jean-François
Luo, Haiwei
Mergaert, Peter
Deslandes, Laurent
Giraud, Eric
author_facet Camuel, Alicia
Teulet, Albin
Carcagno, Mélanie
Haq, Fazal
Pacquit, Valérie
Gully, Djamel
Pervent, Marjorie
Chaintreuil, Clémence
Fardoux, Joël
Horta-Araujo, Natasha
Okazaki, Shin
Ratu, Safirah Tasa Nerves
Gueye, Fatou
Zilli, Jerri
Nouwen, Nico
Arrighi, Jean-François
Luo, Haiwei
Mergaert, Peter
Deslandes, Laurent
Giraud, Eric
author_sort Camuel, Alicia
collection PubMed
description The establishment of the rhizobium-legume symbiosis is generally based on plant perception of Nod factors (NFs) synthesized by the bacteria. However, some Bradyrhizobium strains can nodulate certain legume species, such as Aeschynomene spp. or Glycine max, independently of NFs, and via two different processes that are distinguished by the necessity or not of a type III secretion system (T3SS). ErnA is the first known type III effector (T3E) triggering nodulation in Aeschynomene indica. In this study, a collection of 196 sequenced Bradyrhizobium strains was tested on A. indica. Only strains belonging to the photosynthetic supergroup can develop a NF-T3SS-independent symbiosis, while the ability to use a T3SS-dependent process is found in multiple supergroups. Of these, 14 strains lacking ernA were tested by mutagenesis to identify new T3Es triggering nodulation. We discovered a novel T3E, Sup3, a putative SUMO-protease without similarity to ErnA. Its mutation in Bradyrhizobium strains NAS96.2 and WSM1744 abolishes nodulation and its introduction in an ernA mutant of strain ORS3257 restores nodulation. Moreover, ectopic expression of sup3 in A. indica roots led to the formation of spontaneous nodules. We also report three other new T3Es, Ubi1, Ubi2 and Ubi3, which each contribute to the nodulation capacity of strain LMTR13. These T3Es have no homology to known proteins but share with ErnA three motifs necessary for ErnA activity. Together, our results highlight an unsuspected distribution and diversity of T3Es within the Bradyrhizobium genus that may contribute to their symbiotic efficiency by participating in triggering legume nodulation.
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spelling pubmed-104324112023-08-18 Widespread Bradyrhizobium distribution of diverse Type III effectors that trigger legume nodulation in the absence of Nod factor Camuel, Alicia Teulet, Albin Carcagno, Mélanie Haq, Fazal Pacquit, Valérie Gully, Djamel Pervent, Marjorie Chaintreuil, Clémence Fardoux, Joël Horta-Araujo, Natasha Okazaki, Shin Ratu, Safirah Tasa Nerves Gueye, Fatou Zilli, Jerri Nouwen, Nico Arrighi, Jean-François Luo, Haiwei Mergaert, Peter Deslandes, Laurent Giraud, Eric ISME J Article The establishment of the rhizobium-legume symbiosis is generally based on plant perception of Nod factors (NFs) synthesized by the bacteria. However, some Bradyrhizobium strains can nodulate certain legume species, such as Aeschynomene spp. or Glycine max, independently of NFs, and via two different processes that are distinguished by the necessity or not of a type III secretion system (T3SS). ErnA is the first known type III effector (T3E) triggering nodulation in Aeschynomene indica. In this study, a collection of 196 sequenced Bradyrhizobium strains was tested on A. indica. Only strains belonging to the photosynthetic supergroup can develop a NF-T3SS-independent symbiosis, while the ability to use a T3SS-dependent process is found in multiple supergroups. Of these, 14 strains lacking ernA were tested by mutagenesis to identify new T3Es triggering nodulation. We discovered a novel T3E, Sup3, a putative SUMO-protease without similarity to ErnA. Its mutation in Bradyrhizobium strains NAS96.2 and WSM1744 abolishes nodulation and its introduction in an ernA mutant of strain ORS3257 restores nodulation. Moreover, ectopic expression of sup3 in A. indica roots led to the formation of spontaneous nodules. We also report three other new T3Es, Ubi1, Ubi2 and Ubi3, which each contribute to the nodulation capacity of strain LMTR13. These T3Es have no homology to known proteins but share with ErnA three motifs necessary for ErnA activity. Together, our results highlight an unsuspected distribution and diversity of T3Es within the Bradyrhizobium genus that may contribute to their symbiotic efficiency by participating in triggering legume nodulation. Nature Publishing Group UK 2023-06-24 2023-09 /pmc/articles/PMC10432411/ /pubmed/37355742 http://dx.doi.org/10.1038/s41396-023-01458-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Camuel, Alicia
Teulet, Albin
Carcagno, Mélanie
Haq, Fazal
Pacquit, Valérie
Gully, Djamel
Pervent, Marjorie
Chaintreuil, Clémence
Fardoux, Joël
Horta-Araujo, Natasha
Okazaki, Shin
Ratu, Safirah Tasa Nerves
Gueye, Fatou
Zilli, Jerri
Nouwen, Nico
Arrighi, Jean-François
Luo, Haiwei
Mergaert, Peter
Deslandes, Laurent
Giraud, Eric
Widespread Bradyrhizobium distribution of diverse Type III effectors that trigger legume nodulation in the absence of Nod factor
title Widespread Bradyrhizobium distribution of diverse Type III effectors that trigger legume nodulation in the absence of Nod factor
title_full Widespread Bradyrhizobium distribution of diverse Type III effectors that trigger legume nodulation in the absence of Nod factor
title_fullStr Widespread Bradyrhizobium distribution of diverse Type III effectors that trigger legume nodulation in the absence of Nod factor
title_full_unstemmed Widespread Bradyrhizobium distribution of diverse Type III effectors that trigger legume nodulation in the absence of Nod factor
title_short Widespread Bradyrhizobium distribution of diverse Type III effectors that trigger legume nodulation in the absence of Nod factor
title_sort widespread bradyrhizobium distribution of diverse type iii effectors that trigger legume nodulation in the absence of nod factor
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10432411/
https://www.ncbi.nlm.nih.gov/pubmed/37355742
http://dx.doi.org/10.1038/s41396-023-01458-1
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