Host-secreted antimicrobial peptide enforces symbiotic selectivity in Medicago truncatula

Abstract

Legumes engage in root nodule symbioses with nitrogen-fixing soil bacteria known as rhizobia. In nodule cells, bacteria are enclosed in membrane-bound vesicles called symbiosomes and differentiate into bacteroids that are capable of converting atmospheric nitrogen into ammonia. Bacteroid differentiation and prolonged intracellular survival are essential for development of functional nodules. However, in the Medicago truncatula-Sinorhizobium meliloti symbiosis, incompatibility between symbiotic partners frequently occurs, leading to the formation of infected nodules defective in nitrogen fixation (Fix − ). Here, we report the identification and cloning of the M. truncatula NFS2 gene that regulates this type of specificity pertaining to S. meliloti strain Rm41. We demonstrate that NFS2 encodes a nodule-specific cysteine-rich (NCR) peptide that acts to promote bacterial lysis after differentiation. The negative role of NFS2 in symbiosis is contingent on host genetic background and can be counteracted by other genes encoded by the host. This work extends the paradigm of NCR function to include the negative regulation of symbiotic persistence in host-strain interactions. Our data suggest that NCR peptides are host determinants of symbiotic specificity in M. truncatula and possibly in closely related legumes that form indeterminate nodules in which bacterial symbionts undergo terminal differentiation.legumes | rhizobial symbiosis | nitrogen fixation | symbiotic specificity | NCR peptides

Microsymbiont discrimination mediated by a host-secreted peptide in Medicago truncatula

“…− is not essential for forming Fix − nodules in the A17 background, even though it is required in the RHL-NFS2 background (25).…”

Legumes versus rhizobia: a model for ongoing conflict in symbiosis

“…One mechanism is for hosts to produce nodule‐specific cysteine‐rich (NCR) peptides (Box 1) that induce severe changes to intracellular rhizobia, sometimes causing bacteroids to prematurely die unless they bear a specific transporter to modulate the effects of NCR peptides (Haag et al ., ). Conversely, NCR peptide signaling can ‘backfire’ on hosts by rendering potentially compatible interactions incompatible (Wang et al ., ; Yang et al ., ). Some rhizobia can subvert these host control mechanisms with the plasmid‐borne metallopeptidase HrrP (host range restriction peptidase; Box 1), which cleaves NCR peptides in vitro (Price et al ., ).…”

An interaction between host and microbe genotypes determines colonization success of a key bumble bee gut microbiota member

“…; Wang et al. ), may determine colonization success. The influence of these factors on the success of colonization also depends upon the route of microbe transmission between hosts (Bright and Bulgheresi ).…”

“…Although the interactions between genotypes have been studied in regard to such functional outcomes, the ability for these interactions to determine the successful colonization of beneficial symbionts remains uninvestigated outside of plant systems (Wang et al. ).…”