A GmNINa-miR172c-NNC1 Regulatory Network Coordinates the Nodulation and Autoregulation of Nodulation Pathways in Soybean

Abstract

Symbiotic root nodules are root lateral organs of plants in which nitrogen-fixing bacteria (rhizobia) convert atmospheric nitrogen to ammonia. The formation and number of nodules in legumes are precisely controlled by a rhizobia-induced signal cascade and host-controlled autoregulation of nodulation (AON). However, how these pathways are integrated and their underlying mechanisms are unclear. Here, we report that microRNA172c (miR172c) activates soybean (Glycine max) Rhizobia-Induced CLE1 (GmRIC1) and GmRIC2 by removing the transcriptional repression of these genes by Nodule Number Control 1 (NNC1), leading to the activation of the AON pathway. NNC1 interacts with GmNINa, the soybean ortholog of Lotus NODULE INCEPTION (NIN), and hampers its transcriptional activation of GmRIC1 and GmRIC2. Importantly, GmNINa acts as a transcriptional activator of miR172c. Intriguingly, NNC1 can transcriptionally repress miR172c expression, adding a negative feedback loop into the NNC1 regulatory network. Moreover, GmNINa interacts with NNC1 and can relieve the NNC1-mediated repression of miR172c transcription. Thus, the GmNINa-miR172c-NNC1 network is a master switch that coordinately regulates and optimizes NF and AON signaling, supporting the balance between nodulation and AON in soybean.

Besides and beyond Flowering: Other Roles of EuAP2 Genes in Plant Development

“…These promote nodulation. However, the soybean euAP2 gene, Nodule Number Control 1 (NNC1), has been shown to repress transcriptions of these genes by binding directly to their promoter, thereby inhibiting nodulation [116][117][118]. In addition, downregulation of euAP2 genes either by overexpression of miR172 or RNAi leads to increased nodulation accompanied by upregulation of symbiotic leghemoglobin and non-symbiotic hemoglobin [119].…”

Besides and Beyond Flowering: Other Roles of euAP2 Genes in Plant Development

“…These promote nodulation. However, the soybean euAP2 gene, Nodule Number Control 1 (NNC1), has been shown to repress transcriptions of these genes by binding directly to their promoter thereby inhibiting nodulation [115][116][117]. In addition, downregulation of euAP2 genes either by overexpression miR172 or RNAi leads to increased nodulation accompanied by upregulation of symbiotic leghemoglobin and nonsymbiotic hemoglobin [118].…”

Characterization and Comparative Analysis of RWP-RK Proteins from Arachis duranensis, Arachis ipaensis, and Arachis hypogaea

“…In M. truncatula, MtNIN plays a central role in the temporal and spatial regulation of the nodule development process by competitively inhibiting ERF required for nodulation (ERN1) to suppress the expression of Early Nodulin 11 (ENOD11) and increase the expression of Cytokinin Response 1 (CRE1) [4,16]. Moreover, soybean GmNINa, the ortholog of L. japonicus NIN, regulates nodulation through interactions with Nodule Number Control 1 (NNC1) and the activation of miR172c [18].…”