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.
Highlights
Legumes tightly regulate nodule number to balance the cost of supporting symbiotic rhizobia with the benefits of nitrogen fixation
To identify C-terminally Encoded Peptides (CEPs) peptides involved in the regulation of symbiotic nodulation, we analyzed CEP gene expression in response to rhizobia as well as to Nod factor (NF) or cytokinin signals that are required for nodule initiation
Only MtCEP7 was induced, whereas the expression of most of CEP genes (i.e., MtCEP2, MtCEP4, MtCEP5, MtCEP6, and MtCEP8) was reduced (Fig. 1c). These analyses highlight that MtCEP7 has a unique expression pattern, being rapidly induced by rhizobia as well as by the two key signals required for nodule initiation, NFs and cytokinin
Summary
Legumes tightly regulate nodule number to balance the cost of supporting symbiotic rhizobia with the benefits of nitrogen fixation. Legume root nodules initiate following the secretion of rhizobial Nod factor (NF) signals that are perceived at the root epidermis, preferentially in a susceptible region located above the root apical meristem in compatible host plants[2,3,4]. This symbiotic partner recognition triggers a signaling cascade that activates the rhizobial infection of root hairs and subsequently the formation of infection threads (ITs) that grow toward root inner cortical cells. Cytokinin negatively regulates rhizobial infections or NF signaling in L. japonicus and M. truncatula, respectively[10,15,16,17]
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