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.

共生根瘤是植物的根侧器官，固氮细菌（根瘤菌）将大气中的氮转化为氨。豆科植物中根瘤菌引起的信号级联和宿主控制的结瘤自动调节（AON）可精确控制结节的形成和数量。但是，如何整合这些途径及其潜在机制尚不清楚。在这里，我们报道了microRNA172c（miR172c）激活了大豆（Glycine max）根瘤菌诱导的CLE1（GmRIC1）和GmRIC2，通过消除了结节编号对照1（NNC1）的这些基因的转录抑制，从而导致了AON途径的激活。NNC1与GmNINa的大豆同源基因相互作用莲花结节诱导（NIN），并阻碍其转录激活GmRIC1和GmRIC2。重要的是，GmNINa充当miR172c的转录激活因子。有趣的是，NNC1可以转录抑制miR172c表达，从而在NNC1调节网络中增加一个负反馈环。此外，GmNINa与NNC1相互作用，可以缓解NNC1介导的miR172c转录抑制。因此，GmNINa-miR172c-NNC1网络是一个主交换机，可协调调节和优化NF和AON信号，从而支持大豆中结瘤和AON之间的平衡。