Molecular mechanisms controlling legume autoregulation of nodulation

Abstract

Background: High input costs and environmental pressures to reduce nitrogen use in agriculture have increased the competitive advantage of legume crops. The symbiotic relationship that legumes form with nitrogen-fixing soil bacteria in root nodules is central to this advantage.

Scope: Understanding how legume plants maintain control of nodulation to balance the nitrogen gains with their energy needs and developmental costs will assist in increasing their productivity and relative advantage. For this reason, the regulation of nodulation has been extensively studied since the first mutants exhibiting increased nodulation were isolated almost three decades ago.

Conclusions: Nodulation is regulated primarily via a systemic mechanism known as the autoregulation of nodulation (AON), which is controlled by a CLAVATA1-like receptor kinase. Multiple components sharing homology with the CLAVATA signalling pathway that maintains control of the shoot apical meristem in arabidopsis have now been identified in AON. This includes the recent identification of several CLE peptides capable of activating nodule inhibition responses, a low molecular weight shoot signal and a role for CLAVATA2 in AON. Efforts are now being focused on directly identifying the interactions of these components and to identify the form that long-distance transport molecules take.

Fig. 1.

A working model of root and shoot mechanisms in autoregulation of nodulation (AON). Legumes regulate nodulation in response to pre-existing infections and soil nitrogen levels. Nitrate induces the production of a nitrate-induced CLE peptide (NIC1; A) that acts locally in the root via the AON receptor kinase, NARK (B; or its orthologues in other species), to inhibit nodule progression (C). NARK may act in concert with other components to perceive NIC1. Rhizobia-induced CLE peptides (RICs) are induced at several stages of nodule development and may be transported via the xylem (D) to the shoot. In the shoot, NARK and possibly also CLV2, KLV and CRN are required for the perception of these putative ligands (E). Two kinase-associated protein phosphatases (KAPP1/2) are phosphorylated by NARK and in turn dephosphorylate the NARK kinase (F). An equilibrium of phosphorylation between these components may be required preceding the production of the shoot-derived inhibitor (SDI; G). SDI is transported via the phloem to the roots where it inhibits further nodule progression and cell divisions (H). A compound similar to SDI may also be involved in the nitrate pathway that acts locally to inhibit the progression of nodule formation (C).