Integrated roles of BclA and DD-carboxypeptidase 1 in Bradyrhizobium differentiation within NCR-producing and NCR-lacking root nodules

Abstract Legumes harbor in their symbiotic nodule organs nitrogen fixing rhizobium bacteria called bacteroids. Some legumes produce Nodule-specific Cysteine-Rich (NCR) peptides in the nodule cells to control the intracellular bacterial population. NCR peptides have antimicrobial activity and drive b...

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Autores principales: Quentin Barrière, Ibtissem Guefrachi, Djamel Gully, Florian Lamouche, Olivier Pierre, Joël Fardoux, Clémence Chaintreuil, Benoît Alunni, Tatiana Timchenko, Eric Giraud, Peter Mergaert
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Publicado: Nature Portfolio 2017
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spelling oai:doaj.org-article:25b27326b493425680f9e748b5ddc18a2021-12-02T15:06:12ZIntegrated roles of BclA and DD-carboxypeptidase 1 in Bradyrhizobium differentiation within NCR-producing and NCR-lacking root nodules10.1038/s41598-017-08830-02045-2322https://doaj.org/article/25b27326b493425680f9e748b5ddc18a2017-08-01T00:00:00Zhttps://doi.org/10.1038/s41598-017-08830-0https://doaj.org/toc/2045-2322Abstract Legumes harbor in their symbiotic nodule organs nitrogen fixing rhizobium bacteria called bacteroids. Some legumes produce Nodule-specific Cysteine-Rich (NCR) peptides in the nodule cells to control the intracellular bacterial population. NCR peptides have antimicrobial activity and drive bacteroids toward terminal differentiation. Other legumes do not produce NCR peptides and their bacteroids are not differentiated. Bradyrhizobia, infecting NCR-producing Aeschynomene plants, require the peptide uptake transporter BclA to cope with the NCR peptides as well as a specific peptidoglycan-modifying DD-carboxypeptidase, DD-CPase1. We show that Bradyrhizobium diazoefficiens strain USDA110 forms undifferentiated bacteroids in NCR-lacking soybean nodules. Unexpectedly, in Aeschynomene afraspera nodules the nitrogen fixing USDA110 bacteroids are hardly differentiated despite the fact that this host produces NCR peptides, suggesting that USDA110 is insensitive to the host peptide effectors and that nitrogen fixation can be uncoupled from differentiation. In agreement with the absence of bacteroid differentiation, USDA110 does not require its bclA gene for nitrogen fixing symbiosis with these two host plants. Furthermore, we show that the BclA and DD-CPase1 act independently in the NCR-induced morphological differentiation of bacteroids. Our results suggest that BclA is required to protect the rhizobia against the NCR stress but not to induce the terminal differentiation pathway.Quentin BarrièreIbtissem GuefrachiDjamel GullyFlorian LamoucheOlivier PierreJoël FardouxClémence ChaintreuilBenoît AlunniTatiana TimchenkoEric GiraudPeter MergaertNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 7, Iss 1, Pp 1-13 (2017)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Quentin Barrière
Ibtissem Guefrachi
Djamel Gully
Florian Lamouche
Olivier Pierre
Joël Fardoux
Clémence Chaintreuil
Benoît Alunni
Tatiana Timchenko
Eric Giraud
Peter Mergaert
Integrated roles of BclA and DD-carboxypeptidase 1 in Bradyrhizobium differentiation within NCR-producing and NCR-lacking root nodules
description Abstract Legumes harbor in their symbiotic nodule organs nitrogen fixing rhizobium bacteria called bacteroids. Some legumes produce Nodule-specific Cysteine-Rich (NCR) peptides in the nodule cells to control the intracellular bacterial population. NCR peptides have antimicrobial activity and drive bacteroids toward terminal differentiation. Other legumes do not produce NCR peptides and their bacteroids are not differentiated. Bradyrhizobia, infecting NCR-producing Aeschynomene plants, require the peptide uptake transporter BclA to cope with the NCR peptides as well as a specific peptidoglycan-modifying DD-carboxypeptidase, DD-CPase1. We show that Bradyrhizobium diazoefficiens strain USDA110 forms undifferentiated bacteroids in NCR-lacking soybean nodules. Unexpectedly, in Aeschynomene afraspera nodules the nitrogen fixing USDA110 bacteroids are hardly differentiated despite the fact that this host produces NCR peptides, suggesting that USDA110 is insensitive to the host peptide effectors and that nitrogen fixation can be uncoupled from differentiation. In agreement with the absence of bacteroid differentiation, USDA110 does not require its bclA gene for nitrogen fixing symbiosis with these two host plants. Furthermore, we show that the BclA and DD-CPase1 act independently in the NCR-induced morphological differentiation of bacteroids. Our results suggest that BclA is required to protect the rhizobia against the NCR stress but not to induce the terminal differentiation pathway.
format article
author Quentin Barrière
Ibtissem Guefrachi
Djamel Gully
Florian Lamouche
Olivier Pierre
Joël Fardoux
Clémence Chaintreuil
Benoît Alunni
Tatiana Timchenko
Eric Giraud
Peter Mergaert
author_facet Quentin Barrière
Ibtissem Guefrachi
Djamel Gully
Florian Lamouche
Olivier Pierre
Joël Fardoux
Clémence Chaintreuil
Benoît Alunni
Tatiana Timchenko
Eric Giraud
Peter Mergaert
author_sort Quentin Barrière
title Integrated roles of BclA and DD-carboxypeptidase 1 in Bradyrhizobium differentiation within NCR-producing and NCR-lacking root nodules
title_short Integrated roles of BclA and DD-carboxypeptidase 1 in Bradyrhizobium differentiation within NCR-producing and NCR-lacking root nodules
title_full Integrated roles of BclA and DD-carboxypeptidase 1 in Bradyrhizobium differentiation within NCR-producing and NCR-lacking root nodules
title_fullStr Integrated roles of BclA and DD-carboxypeptidase 1 in Bradyrhizobium differentiation within NCR-producing and NCR-lacking root nodules
title_full_unstemmed Integrated roles of BclA and DD-carboxypeptidase 1 in Bradyrhizobium differentiation within NCR-producing and NCR-lacking root nodules
title_sort integrated roles of bcla and dd-carboxypeptidase 1 in bradyrhizobium differentiation within ncr-producing and ncr-lacking root nodules
publisher Nature Portfolio
publishDate 2017
url https://doaj.org/article/25b27326b493425680f9e748b5ddc18a
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