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

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  • Carole Laffont

    (Univ d’Evry, Université de Paris; Université Paris-Saclay)

  • Ariel Ivanovici

    (The Australian National University)

  • Pierre Gautrat

    (Univ d’Evry, Université de Paris; Université Paris-Saclay)

  • Mathias Brault

    (Univ d’Evry, Université de Paris; Université Paris-Saclay)

  • Michael Anthony Djordjevic

    (The Australian National University)

  • Florian Frugier

    (Univ d’Evry, Université de Paris; Université Paris-Saclay)

Abstract

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.

Suggested Citation

  • Carole Laffont & Ariel Ivanovici & Pierre Gautrat & Mathias Brault & Michael Anthony Djordjevic & Florian Frugier, 2020. "The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-16968-1
    DOI: 10.1038/s41467-020-16968-1
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    Cited by:

    1. Jieshun Lin & Yuda Purwana Roswanjaya & Wouter Kohlen & Jens Stougaard & Dugald Reid, 2021. "Nitrate restricts nodule organogenesis through inhibition of cytokinin biosynthesis in Lotus japonicus," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Jiahuan Chen & Zhijuan Wang & Lixiang Wang & Yangyang Hu & Qiqi Yan & Jingjing Lu & Ziyin Ren & Yujie Hong & Hongtao Ji & Hui Wang & Xinying Wu & Yanru Lin & Chao Su & Thomas Ott & Xia Li, 2022. "The B-type response regulator GmRR11d mediates systemic inhibition of symbiotic nodulation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

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