The NMN Module Conducts Nodule Number Orchestra

Abstract

Legumes control nodule number through nodulation and autoregulation of nodulation (AON) pathways. Nodule Inception (NIN) is essential for rhizobial infection and nodule organogenesis in legumes. The GmNINa-miR172c-NNC1 (NMN) module, which consists of two positive regulators, GmNINa and miR172c, and a suppressor, NNC1, integrates both pathways. GmNINa activates miR172c to downregulate NNC1, leading to nodulation, while NNC1 inhibits miR172c expression, forming a negative feedback loop. GmNINa and NNC1 interact with each other and antagonistically fine-tune GmRIC1/RIC2 expression, turning AON on and off. Conversely, activation of AON inhibits GmNINa and miR172c expression, thereby reducing their inhibitory effects on NNC1 to attenuate both nodulation signaling and AON. The NMN module functions not only as an "accelerator" of the nodulation signal to promote nodulation but also as a "brake" on the signal by activating AON to orchestrate nodule number.

Keywords: Interaction of Plants with Organisms; Plant Biology; Plant Genetics.

Graphical abstract

Figure 1

NMN Module Is a Fine Tuner of Nodule Number NIN and miR172c are positive regulators of nodulation, and NNC1 is a repressor of nodulation. The NMN module integrates both nodulation signaling and AON signaling pathways to systemically control nodule number in legumes. In low-nitrogen conditions, plant exudes flavonoid signals from its root, which are perceived by rhizobia to induce the production of Nod factors. The Nod factors are perceived by the Nod factor receptors (NFR1α and NFR5α in soybean) localized in the plasma membrane of root hair and activate NF signaling pathway. The transcription factors, such as GmNINa in soybean, are induced by NF signaling to activate the expression of miR172c, which then represses NNC1 expression by cleaving its mRNA. NNC1 in turn downregulates the expression of miR172c or interacts with GmNINa to repress its binding to miR172c to form a negative feedback loop. GmNINa and NNC1 activate or repress the expression of GmRIC1 and GmRIC2 in soybean. GmNINa can promote the transcription of GmRIC1 and GmRIC2 alone and/or through alleviating NNC1 inhibition on GmRIC1 and GmRIC2 by activating miR172c. The CLE peptides are transported to the shoot to activate the nodulation autoregulation receptor, GmNARK in soybean, SUNN in Medicago, and HAR1 in Lotus. The activation of AON produces the SDIs, including cytokinins, miR2111, or other factors, which are transported to the root to inhibit the expression of NIN and GmNINa, leading to suppression of the downstream nodulation genes (e.g., EOND40s) that regulate nodulation. In high-nitrogen conditions, nitrogen induces the subcellular localization of NLP1 in Medicago and NRSYM1 in Lotus from cytoplasm to nucleus. NLP1 interacts with NIN to repress its activation of downstream target genes. NRSYM1 promotes production of CLE peptides to activate AON.