Plant hormonal regulation of nitrogen-fixing nodule organogenesis

Abstract

Legumes have evolved symbiotic interactions with rhizobial bacteria to efficiently utilize nitrogen. Recent progress in symbiosis has revealed several key components of host plants required for nitrogen-fixing nodule organogenesis, in which complicated metabolic and signaling pathways in the host plant are reprogrammed to generate nodules in the cortex upon perception of the rhizobial Nod factor. Following the recognition of Nod factors, plant hormones are likely to be essential throughout nodule organogenesis for integration of developmental and environmental signaling cues into nodule development. Here, we review the molecular events involved in plant hormonal regulation and signaling cross-talk for nitrogen-fixing nodule development, and discuss how these signaling networks are integrated into Nod factor-mediated signaling during plant-microbe interactions.

Fig. 1.

Proposed model for rhizobia-legume symbiotic signaling pathways. Nod factor from rhizobia stimulates its receptor complex (NFR), MtLYK3/NFP or LjNFR1/5. Signal cascades from NFR are transduced via as-yet-unidentified pathways to induce nuclear calcium spiking and activate DMI3 (CCaMK). Activated DMI3 directly interacts with and activates nodule-related transcription factors, including NSP1/2, via phosphorylation. These transcription factors enhance the expression of Nod factor-responsive genes by directly binding to the NF-box (AATTT). It is not clear how DMI3 regulates nodule-related NIN and ERN, but their up-regulation by Nod factor signaling is essential for nodulation. EFD, an AP2/ERF family member, inhibits nodulation, probably by disrupting cytokinin signaling. The dashed arrows indicate unknown biochemical links.

Fig. 2.

Systemic and local inhibitory regulation of nodulation. (A) Schematic model of autoregulation of nodulation (AON). Long distance inhibitory pathways for AON have been proposed, but the root-derived signals are not clearly identified although some CLE peptides including LjCLE-RS1/2 or MtCLE12/13 might function as root-to-shoot signaling molecules. Root-derived signals might directly or indirectly activate the CLV1-like receptor kinase, HAR1/SUNN/NARK. These events create shoot-derived unidentified negative signals that suppress root nodule formation by inhibiting auxin transport and by presumed TML functions in the root. JA and BR are thought to be involved in shoot-derived negative signaling pathways. (B) Local inhibition pathways mediated by the coordination of stress-related hormone actions. Rhizobia and external stress signals activate MAPK signaling cascades and the action of plant hormones including ethylene, SA, ABA, and JA. Ethylene, a major negative regulator in nodulation, probably stimulates SIMKK(AtMKK4/5)-MPK3/6 cascades by suppressing CTR1 activity. The activated MPK3/6 proteins directly or indirectly regulate their downstream signaling components, including SICKLE/EIN2 and various stress-related transcription factors (unknown targets), to inhibit Nod factor signaling pathways. ABA, SA, and JA signaling pathways directly suppress Nod factor signaling, or their negative action could be integrated into SIMKK-mediated MAPK signaling cascades. The dashed arrows indicate unknown biochemical links.

Fig. 3.

Positive regulation of nodulation through the action of plant hormones. The interplay of auxin and cytokinin plays a major role in nodule organogenesis. Cytokinins positively regulate nodule-related NSP2 and NIN expression, and expression of PINs that lead to local auxin accumulation. The local accumulation of auxin during the initiation of nodule primordia is also promoted by cooperation between flavonoids and strigolactone. The dashed arrows indicate unknown biochemical links.