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The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically

Legumes tightly regulate nodule number to balance the cost of supporting symbiotic rhizobia with the benefits of nitrogen fixation. C-terminally Encoded Peptides (CEPs) and CLAVATA3-like (CLE) peptides positively and negatively regulate nodulation, respectively, through independent systemic pathways...

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Autores principales: Laffont, Carole, Ivanovici, Ariel, Gautrat, Pierre, Brault, Mathias, Djordjevic, Michael Anthony, Frugier, Florian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7311451/
https://www.ncbi.nlm.nih.gov/pubmed/32576831
http://dx.doi.org/10.1038/s41467-020-16968-1
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author Laffont, Carole
Ivanovici, Ariel
Gautrat, Pierre
Brault, Mathias
Djordjevic, Michael Anthony
Frugier, Florian
author_facet Laffont, Carole
Ivanovici, Ariel
Gautrat, Pierre
Brault, Mathias
Djordjevic, Michael Anthony
Frugier, Florian
author_sort Laffont, Carole
collection PubMed
description Legumes tightly regulate nodule number to balance the cost of supporting symbiotic rhizobia with the benefits of nitrogen fixation. C-terminally Encoded Peptides (CEPs) and CLAVATA3-like (CLE) peptides positively and negatively regulate nodulation, respectively, through independent systemic pathways, but how these regulations are coordinated remains unknown. Here, we show that rhizobia, Nod Factors, and cytokinins induce a symbiosis-specific CEP gene, MtCEP7, which positively regulates rhizobial infection. Via grafting and split root studies, we reveal that MtCEP7 increases nodule number systemically through the MtCRA2 receptor. MtCEP7 and MtCLE13 expression in rhizobia-inoculated roots rely on the MtCRE1 cytokinin receptor and on the MtNIN transcription factor. MtNIN binds and transactivates MtCEP7 and MtCLE13, and a NIN Binding Site (NBS) identified within the proximal MtCEP7 promoter is required for its symbiotic activation. Overall, these results demonstrate that a cytokinin-MtCRE1-MtNIN regulatory module coordinates the expression of two antagonistic, symbiosis-related, peptide hormones from different families to fine-tune nodule number.
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spelling pubmed-73114512020-06-26 The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically Laffont, Carole Ivanovici, Ariel Gautrat, Pierre Brault, Mathias Djordjevic, Michael Anthony Frugier, Florian Nat Commun Article Legumes tightly regulate nodule number to balance the cost of supporting symbiotic rhizobia with the benefits of nitrogen fixation. C-terminally Encoded Peptides (CEPs) and CLAVATA3-like (CLE) peptides positively and negatively regulate nodulation, respectively, through independent systemic pathways, but how these regulations are coordinated remains unknown. Here, we show that rhizobia, Nod Factors, and cytokinins induce a symbiosis-specific CEP gene, MtCEP7, which positively regulates rhizobial infection. Via grafting and split root studies, we reveal that MtCEP7 increases nodule number systemically through the MtCRA2 receptor. MtCEP7 and MtCLE13 expression in rhizobia-inoculated roots rely on the MtCRE1 cytokinin receptor and on the MtNIN transcription factor. MtNIN binds and transactivates MtCEP7 and MtCLE13, and a NIN Binding Site (NBS) identified within the proximal MtCEP7 promoter is required for its symbiotic activation. Overall, these results demonstrate that a cytokinin-MtCRE1-MtNIN regulatory module coordinates the expression of two antagonistic, symbiosis-related, peptide hormones from different families to fine-tune nodule number. Nature Publishing Group UK 2020-06-23 /pmc/articles/PMC7311451/ /pubmed/32576831 http://dx.doi.org/10.1038/s41467-020-16968-1 Text en © The Author(s) 2020 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Laffont, Carole
Ivanovici, Ariel
Gautrat, Pierre
Brault, Mathias
Djordjevic, Michael Anthony
Frugier, Florian
The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically
title The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically
title_full The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically
title_fullStr The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically
title_full_unstemmed The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically
title_short The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically
title_sort nin transcription factor coordinates cep and cle signaling peptides that regulate nodulation antagonistically
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7311451/
https://www.ncbi.nlm.nih.gov/pubmed/32576831
http://dx.doi.org/10.1038/s41467-020-16968-1
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