Inoculation- and Nitrate-Induced CLE Peptides of Soybean Control NARK-Dependent Nodule Formation

Abstract

Systemic autoregulation of nodulation in legumes involves a root-derived signal (Q) that is perceived by a CLAVATA1-like leucine-rich repeat receptor kinase (e.g. GmNARK). Perception of Q triggers the production of a shoot-derived inhibitor that prevents further nodule development. We have identified three candidate CLE peptide-encoding genes (GmRIC1, GmRIC2, and GmNIC1) in soybean (Glycine max) that respond to Bradyrhizobium japonicum inoculation or nitrate treatment. Ectopic overexpression of all three CLE peptide genes in transgenic roots inhibited nodulation in a GmNARK-dependent manner. The peptides share a high degree of amino acid similarity in a 12-amino-acid C-terminal domain, deemed to represent the functional ligand of GmNARK. GmRIC1 was expressed early (12 h) in response to Bradyrhizobium-sp.-produced nodulation factor while GmRIC2 was induced later (48 to 72 h) but was more persistent during later nodule development. Neither GmRIC1 nor GmRIC2 were induced by nitrate. In contrast, GmNIC1 was strongly induced by nitrate (2 mM) treatment but not by Bradyrhizobium sp. inoculation and, unlike the other two GmCLE peptides, functioned locally to inhibit nodulation. Grafting demonstrated a requirement for root GmNARK activity for nitrate regulation of nodulation whereas Bradyrhizobium sp.-induced regulation was contingent on GmNARK function in the shoot.

Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase

“…Conversely, knockdown of Medicago truncatula MtCLE12 and MtCLE13 resulted in a significant increase in nodule number 17 . Functionally similar CLE genes have also been identified in other leguminous species [18][19][20][21] . Thus, CLE-RS peptides are strong candidates for the root-derived signals that might act as ligands for HAR1.…”

The Autoregulation Gene SUNN Mediates Changes in Root Organ Formation in Response to Nitrogen through Alteration of Shoot-to-Root Auxin Transport

“…In this respect, sunn-1 mutants might be an exception to the rule that most autoregulation mutants, including other sunn mutant alleles, still nodulate in the presence of nitrate. The local regulation of nodulation by nitrate is supported by the finding that nitrate induces a CLE-like peptide in soybean, GmNIC1, that probably interacts with NARK in the root to inhibit nodulation (Reid et al, 2011a). Another local regulator of nodulation could be NIP/LATD, a putative nitrate transporter expressed in roots and nodules that affects meristem activity in nodules and lateral roots (Bright et al, 2005;Yendrek et al, 2010).…”

An RNA Sequencing Transcriptome Analysis Reveals Novel Insights into Molecular Aspects of the Nitrate Impact on the Nodule Activity of Medicago truncatula

“…The underlying molecular mechanism is largely understood (Okamoto et al, 2009) and resembles the mechanism governing the autoregulation of nodulation (Reid et al, 2011). It has also been clearly shown that nitrate strongly inhibits the activity of existing nodules (Vessey and Waterer, 1992).…”