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

Carole Laffont, Ariel Ivanovici, Pierre Gautrat, Mathias Brault, Michael Anthony Djordjevic, Florian Frugier

Research output: Contribution to journalArticleAcademicpeer-review


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.

Original languageEnglish
Article number3167
Number of pages13
JournalNature Communications
Issue number1
Publication statusPublished - 23 Jun 2020
Externally publishedYes


  • Cytokinins/metabolism
  • Epidermis
  • Gene Expression Regulation, Plant
  • Lotus/metabolism
  • Medicago truncatula
  • Peptides/chemistry
  • Plant Proteins
  • Plant Root Nodulation/genetics
  • Plant Roots/metabolism
  • Promoter Regions, Genetic
  • Protein Kinases
  • Protein Sorting Signals/genetics
  • Rhizobium/metabolism
  • Root Nodules, Plant
  • Sinorhizobium meliloti/metabolism
  • Symbiosis
  • Transcription Factors/metabolism


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